Dominique Bergmann

All Publications

• Century-long timelines of herbarium genomes predict plant stomatal response to climate change. Nature ecology & evolution Lang, P. L., Erberich, J. M., Lopez, L., Weiß, C. L., Amador, G., Fung, H. F., Latorre, S. M., Lasky, J. R., Burbano, H. A., Expósito-Alonso, M., Bergmann, D. C. 2024

  Abstract

  Dissecting plant responses to the environment is key to understanding whether and how plants adapt to anthropogenic climate change. Stomata, plants' pores for gas exchange, are expected to decrease in density following increased CO2 concentrations, a trend already observed in multiple plant species. However, it is unclear whether such responses are based on genetic changes and evolutionary adaptation. Here we make use of extensive knowledge of 43 genes in the stomatal development pathway and newly generated genome information of 191 Arabidopsis thaliana historical herbarium specimens collected over 193 years to directly link genetic variation with climate change. While we find that the essential transcription factors SPCH, MUTE and FAMA, central to stomatal development, are under strong evolutionary constraints, several regulators of stomatal development show signs of local adaptation in contemporary samples from different geographic regions. We then develop a functional score based on known effects of gene knock-out on stomatal development that recovers a classic pattern of stomatal density decrease over the past centuries, suggesting a genetic component contributing to this change. This approach combining historical genomics with functional experimental knowledge could allow further investigations of how different, even in historical samples unmeasurable, cellular plant phenotypes may have already responded to climate change through adaptive evolution.

  View details for DOI 10.1038/s41559-024-02481-x

  View details for PubMedID 39117952

  View details for PubMedCentralID 8542704

• Spatially resolved proteomics of the Arabidopsis stomatal lineage identifies polarity complexes for cell divisions and stomatal pores. Developmental cell Wallner, E., Mair, A., Handler, D., McWhite, C., Xu, S., Dolan, L., Bergmann, D. C. 2024

  Abstract

  Cell polarity is used to guide asymmetric divisions and create morphologically diverse cells. We find that two oppositely oriented cortical polarity domains present during the asymmetric divisions in the Arabidopsis stomatal lineage are reconfigured into polar domains marking ventral (pore-forming) and outward-facing domains of maturing stomatal guard cells. Proteins that define these opposing polarity domains were used as baits in miniTurboID-based proximity labeling. Among differentially enriched proteins, we find kinases, putative microtubule-interacting proteins, and polar SOSEKIs with their effector ANGUSTIFOLIA. Using AI-facilitated protein structure prediction models, we identify potential protein-protein interaction interfaces among them. Functional and localization analyses of the polarity protein OPL2 and its putative interaction partners suggest a positive interaction with mitotic microtubules and a role in cytokinesis. This combination of proteomics and structural modeling with live-cell imaging provides insights into how polarity is rewired in different cell types and cell-cycle stages.

  View details for DOI 10.1016/j.devcel.2024.03.001

  View details for PubMedID 38518768

• Pluripotency of a founding field: rebranding developmental biology. Development (Cambridge, England) Rogers, C. D., Amemiya, C., Arur, S., Babonis, L., Barresi, M., Bartlett, M., Behringer, R., Benham-Pyle, B., Bergmann, D., Blackman, B., Brown, C. T., Browne, B., Camacho, J., Chabu, C. Y., Chow, I., Cleaver, O., Cool, J., Dennis, M. Y., Dickinson, A. J., Di Talia, S., Frank, M., Gillmor, S., Haag, E. S., Hariharan, I., Harland, R., Husbands, A., Jerome-Majewska, L., Koenig, K., Labonne, C., Layden, M., Lowe, C., Mani, M., Martik, M., McKown, K., Moens, C., Mosimann, C., Onyenedum, J., Reed, R., Rivera, A., Rokhsar, D., Royer, L., Rutaganira, F., Shahan, R., Sinha, N., Swalla, B., Van Norman, J. M., Wagner, D. E., Wikramanayake, A., Zebell, S., Brady, S. M. 2024; 151 (3)

  Abstract

  The field of developmental biology has declined in prominence in recent decades, with off-shoots from the field becoming more fashionable and highly funded. This has created inequity in discovery and opportunity, partly due to the perception that the field is antiquated or not cutting edge. A 'think tank' of scientists from multiple developmental biology-related disciplines came together to define specific challenges in the field that may have inhibited innovation, and to provide tangible solutions to some of the issues facing developmental biology. The community suggestions include a call to the community to help 'rebrand' the field, alongside proposals for additional funding apparatuses, frameworks for interdisciplinary innovative collaborations, pedagogical access, improved science communication, increased diversity and inclusion, and equity of resources to provide maximal impact to the community.

  View details for DOI 10.1242/dev.202342

  View details for PubMedID 38345109

• Guidelines for naming and studying plasma membrane domains in plants. Nature plants Jaillais, Y., Bayer, E., Bergmann, D. C., Botella, M. A., Boutté, Y., Bozkurt, T. O., Caillaud, M. C., Germain, V., Grossmann, G., Heilmann, I., Hemsley, P. A., Kirchhelle, C., Martinière, A., Miao, Y., Mongrand, S., Müller, S., Noack, L. C., Oda, Y., Ott, T., Pan, X., Pleskot, R., Potocky, M., Robert, S., Rodriguez, C. S., Simon-Plas, F., Russinova, E., Van Damme, D., Van Norman, J. M., Weijers, D., Yalovsky, S., Yang, Z., Zelazny, E., Gronnier, J. 2024

  Abstract

  Biological membranes play a crucial role in actively hosting, modulating and coordinating a wide range of molecular events essential for cellular function. Membranes are organized into diverse domains giving rise to dynamic molecular patchworks. However, the very definition of membrane domains has been the subject of continuous debate. For example, in the plant field, membrane domains are often referred to as nanodomains, nanoclusters, microdomains, lipid rafts, membrane rafts, signalling platforms, foci or liquid-ordered membranes without any clear rationale. In the context of plant-microbe interactions, microdomains have sometimes been used to refer to the large area at the plant-microbe interface. Some of these terms have partially overlapping meanings at best, but they are often used interchangeably in the literature. This situation generates much confusion and limits conceptual progress. There is thus an urgent need for us as a scientific community to resolve these semantic and conceptual controversies by defining an unambiguous nomenclature of membrane domains. In this Review, experts in the field get together to provide explicit definitions of plasma membrane domains in plant systems and experimental guidelines for their study. We propose that plasma membrane domains should not be considered on the basis of their size alone but rather according to the biological system being considered, such as the local membrane environment or the entire cell.

  View details for DOI 10.1038/s41477-024-01742-8

  View details for PubMedID 39134664

  View details for PubMedCentralID 5256950

• Targeting editing of tomatoSPEECHLESScis-regulatory regions generates plants with altered stomatal density in response to changing climate conditions. bioRxiv : the preprint server for biology Nir, I., Budrys, A., Smoot, N. K., Erberich, J., Bergmann, D. C. 2023

  Abstract

  Flexible developmental programs enable plants to customize their organ size and cellular composition. In leaves of eudicots, the stomatal lineage produces two essential cell types, stomata and pavement cells, but the total numbers and ratio of these cell types can vary. Central to this flexibility is the stomatal lineage initiating transcription factor, SPEECHLESS (SPCH). Here we show, by multiplex CRISPR/Cas9 editing of SlSPCH cis- regulatory sequences in tomato, that we can identify variants with altered stomatal development responses to light and temperature cues. Analysis of tomato leaf development across different conditions, aided by newly-created tools for live-cell imaging and translational reporters of SlSPCH and its paralogues SlMUTE and SlFAMA, revealed the series of cellular events that lead to the environmental change-driven responses in leaf form. Plants bearing the novel SlSPCH variants generated in this study are powerful resources for fundamental and applied studies of tomato resilience in response to climate change.Significance statement: Plants can change their shape, size and cellular composition in response to environmental cues. Here, by precise gene editing of a core stomatal development regulator gene in tomato, we generate new alleles with enhanced or dampened responses to light and temperature cues. Combined with live imaging of development, we show the genetic and cellular pathways that contribute to customization of the leaf epidermis, and how this could lead to better climate-adapted varieties.

  View details for DOI 10.1101/2023.11.02.564550

  View details for PubMedID 37961313

• A cell size threshold triggers commitment to stomatal fate in Arabidopsis. Science advances Gong, Y., Dale, R., Fung, H. F., Amador, G. O., Smit, M. E., Bergmann, D. C. 2023; 9 (38): eadf3497

  Abstract

  How flexible developmental programs integrate information from internal and external factors to modulate stem cell behavior is a fundamental question in developmental biology. Cells of the Arabidopsis stomatal lineage modify the balance of stem cell proliferation and differentiation to adjust the size and cell type composition of mature leaves. Here, we report that meristemoids, one type of stomatal lineage stem cell, trigger the transition from asymmetric self-renewing divisions to commitment and terminal differentiation by crossing a critical cell size threshold. Through computational simulation, we demonstrate that this cell size-mediated transition allows robust, yet flexible termination of stem cell proliferation, and we observe adjustments in the number of divisions before the differentiation threshold under several genetic manipulations. We experimentally evaluate several mechanisms for cell size sensing, and our data suggest that this stomatal lineage transition is dependent on a nuclear factor that is sensitive to DNA content.

  View details for DOI 10.1126/sciadv.adf3497

  View details for PubMedID 37729402

• The stomatal fates: Understanding initiation and enforcement of stomatal cell fate transitions. Current opinion in plant biology Smit, M. E., Bergmann, D. C. 2023: 102449

  Abstract

  In the stomatal lineage, repeated arcs of initiation, stem-cell proliferation, and terminal cell fate commitment are displayed on the surface of aerial organs. Over the past two decades, the core transcription and signaling elements that guide cell divisions, patterning, and fate transitions were defined. Here we highlight recent work that extends the core using a variety of cutting-edge techniques in different plant species. New work has discovered transcriptional circuits that initiate and reinforce stomatal fate transitions, while also enabling the lineage to interpret and respond to environmental inputs. Recent developments show that some key stomatal factors are more flexible or potentially even interchangeable, opening up avenues to explore stomatal fates and regulatory networks.

  View details for DOI 10.1016/j.pbi.2023.102449

  View details for PubMedID 37709566

• Cell Fate Programming by Transcription Factors and Epigenetic Machinery in Stomatal Development. bioRxiv : the preprint server for biology Liu, A., Mair, A., Matos, J. L., Vollbrecht, M., Xu, S., Bergmann, D. C. 2023

  Abstract

  The development of multi-cellular organisms requires coordinated changes in gene expression that are often mediated by the interaction between transcription factors (TFs) and their corresponding cis-regulatory elements (CREs). During development and differentiation, the accessibility of CREs is dynamically modulated by the epigenome. How the epigenome, CREs and TFs together exert control over cell fate commitment remains to be fully understood. In the Arabidopsis leaf epidermis, meristemoids undergo a series of stereotyped cell divisions, then switch fate to commit to stomatal differentiation. Newly created or reanalyzed scRNA-seq and ChIP-seq data confirm that stomatal development involves distinctive phases of transcriptional regulation and that differentially regulated genes are bound by the stomatal basic-helix-loop-helix (bHLH) TFs. Targets of the bHLHs often reside in repressive chromatin before activation. MNase-seq evidence further suggests that the repressive state can be overcome and remodeled upon activation by specific stomatal bHLHs. We propose that chromatin remodeling is mediated through the recruitment of a set of physical interactors that we identified through proximity labeling - the ATPase-dependent chromatin remodeling SWI/SNF complex and the histone acetyltransferase HAC1. The bHLHs and chromatin remodelers localize to overlapping genomic regions in a hierarchical order. Furthermore, plants with stage-specific knock-down of the SWI/SNF components or HAC1 fail to activate specific bHLH targets and display stomatal development defects. Together these data converge on a model for how stomatal TFs and epigenetic machinery cooperatively regulate transcription and chromatin remodeling during progressive fate specification.

  View details for DOI 10.1101/2023.08.23.554515

  View details for PubMedID 37662219

• Arabidopsis stomatal lineage cells establish bipolarity and segregate differential signaling capacity to regulate stem cell potential. Developmental cell Wallner, E. S., Dolan, L., Bergmann, D. C. 2023

  Abstract

  Cell polarity combined with asymmetric cell divisions (ACDs) generates cellular diversity. In the Arabidopsis stomatal lineage, a single cortical polarity domain marked by BASL orients ACDs and is segregated to the larger daughter to enforce cell fate. We discovered a second, oppositely positioned polarity domain defined by OCTOPUS-LIKE (OPL) proteins, which forms prior to ACD and is segregated to the smaller (meristemoid) daughter. Genetic and misexpression analyses show that OPLs promote meristemoid-amplifying divisions and delay stomatal fate progression. Polarity mediates OPL segregation into meristemoids but is not required for OPL function. OPL localization and activity are largely independent of other stomatal polarity genes and of the brassinosteroid signaling components associated with OPLs in other contexts. While OPLs are unique to seed plants, ectopic expression in the liverwort Marchantia suppressed epidermal fate progression, suggesting that OPLs engage ancient and broadly conserved pathways to regulate cell division and cell fate.

  View details for DOI 10.1016/j.devcel.2023.07.024

  View details for PubMedID 37607546

• Cortical polarity ensures its own asymmetric inheritance in the stomatal lineage to pattern the leaf surface. Science (New York, N.Y.) Muroyama, A., Gong, Y., Hartman, K. S., Bergmann, D. C. 2023; 381 (6653): 54-59

  Abstract

  Asymmetric cell divisions specify differential cell fates across kingdoms. In metazoans, preferential inheritance of fate determinants into one daughter cell frequently depends on polarity-cytoskeleton interactions. Despite the prevalence of asymmetric divisions throughout plant development, evidence for analogous mechanisms that segregate fate determinants remains elusive. Here, we describe a mechanism in the Arabidopsis leaf epidermis that ensures unequal inheritance of a fate-enforcing polarity domain. By defining a cortical region depleted of stable microtubules, the polarity domain limits possible division orientations. Accordingly, uncoupling the polarity domain from microtubule organization during mitosis leads to aberrant division planes and accompanying cell identity defects. Our data highlight how a common biological module, coupling polarity to fate segregation through the cytoskeleton, can be reconfigured to accommodate unique features of plant development.

  View details for DOI 10.1126/science.add6162

  View details for PubMedID 37410832

• Function follows form: How cell size is harnessed for developmental decisions. European journal of cell biology Fung, H. F., Bergmann, D. C. 2023; 102 (2): 151312

  Abstract

  Cell size has profound effects on biological function, influencing a wide range of processes, including biosynthetic capacity, metabolism, and nutrient uptake. As a result, size is typically maintained within a narrow, population-specific range through size control mechanisms, which are an active area of study. While the physiological consequences of cell size are relatively well-characterized, less is known about its developmental consequences, and specifically its effects on developmental transitions. In this review, we compare systems where cell size is linked to developmental transitions, paying particular attention to examples from plants. We conclude by proposing that size can offer a simple readout of complex inputs, enabling flexible decisions during plant development.

  View details for DOI 10.1016/j.ejcb.2023.151312

  View details for PubMedID 36989838

• Extensive embryonic patterning without cellular differentiation primes the plant epidermis for efficient post-embryonic stomatal activities. Developmental cell Smit, M. E., Vaten, A., Mair, A., Northover, C. A., Bergmann, D. C. 2023

  Abstract

  Plant leaves feature epidermal stomata that are organized in stereotyped patterns. How does the pattern originate? We provide transcriptomic, imaging, and genetic evidence that Arabidopsis embryos engage known stomatal fate and patterning factors to create regularly spaced stomatal precursor cells. Analysis of embryos from 36 plant species indicates that this trait is widespread among angiosperms. Embryonic stomatal patterning in Arabidopsis is established in three stages: first, broad SPEECHLESS (SPCH) expression; second, coalescence of SPCH and its targets into discrete domains; and third, one round of asymmetric division to create stomatal precursors. Lineage progression is then halted until after germination. We show that the embryonic stomatal pattern enables fast stomatal differentiation and photosynthetic activity upon germination, but it also guides the formation of additional stomata as the leaf expands. In addition, key stomatal regulators are prevented from driving the fate transitions they can induce after germination, identifying stage-specific layers of regulation that control lineage progression during embryogenesis.

  View details for DOI 10.1016/j.devcel.2023.02.014

  View details for PubMedID 36931268

• Opposite polarity programs regulate asymmetric subsidiary cell divisions in grasses. eLife Zhang, D., Spiegelhalder, R. P., Abrash, E. B., Nunes, T. D., Hidalgo, I., Anleu Gil, M. X., Jesenofsky, B., Lindner, H., Bergmann, D. C., Raissig, M. T. 2022; 11

  Abstract

  Grass stomata recruit lateral subsidiary cells (SCs), which are key to the unique stomatal morphology and the efficient plant-atmosphere gas exchange in grasses. Subsidiary mother cells (SMCs) strongly polarise before an asymmetric division forms a SC. Yet apart from a proximal polarity module that includes PANGLOSS1 (PAN1) and guides nuclear migration, little is known regarding the developmental processes that form SCs. Here, we used comparative transcriptomics of developing wild-type and SC-less bdmute leaves in the genetic model grass Brachypodium distachyon to identify novel factors involved in SC formation. This approach revealed BdPOLAR, which forms a novel, distal polarity domain in SMCs that is opposite to the proximal PAN1 domain. Both polarity domains are required for the formative SC division yet exhibit various roles in guiding pre-mitotic nuclear migration and SMC division plane orientation, respectively. Nonetheless, the domains are linked as the proximal domain controls polarisation of the distal domain. In summary, we identified two opposing polarity domains that coordinate the SC division, a process crucial for grass stomatal physiology.

  View details for DOI 10.7554/eLife.79913

  View details for PubMedID 36537077

• Expanded roles and divergent regulation of FAMA in Brachypodium and Arabidopsis stomatal development. The Plant cell McKown, K. H., Gil, M. X., Mair, A., Xu, S., Raissig, M. T., Bergmann, D. C. 2022

  Abstract

  Stomata, cellular valves found on the surfaces of aerial plant tissues, present a paradigm for studying cell fate and patterning in plants. A highly conserved core set of related basic helix-loop-helix (bHLH) transcription factors regulate stomatal development across diverse species. We characterized BdFAMA in the temperate grass Brachypodium distachyon and found this late-acting transcription factor was necessary and sufficient for specifying stomatal guard cell fate, and unexpectedly could also induce the recruitment of subsidiary cells in the absence of its paralogue, BdMUTE. The overlap in function is paralleled by an overlap in expression pattern and by unique regulatory relationships between BdMUTE and BdFAMA. To better appreciate the relationships among the Brachypodium stomatal bHLHs, we used in vivo proteomics in developing leaves and found evidence for multiple shared interaction partners. We reexamined the roles of these genes in Arabidopsis thaliana by testing genetic sufficiency within and across species, and found that while BdFAMA and AtFAMA can rescue stomatal production in Arabidopsis fama and mute mutants, only AtFAMA can specify Brassica -specific myrosin idioblasts. Taken together, our findings refine the current models of stomatal bHLH function and regulatory feedbacks amongst paralogues within grasses as well as across the monocot/dicot divide.

  View details for DOI 10.1093/plcell/koac341

  View details for PubMedID 36440974

• Connected function of PRAF/RLD and GNOM in membrane trafficking controls intrinsic cell polarity in plants. Nature communications Wang, L., Li, D., Yang, K., Guo, X., Bian, C., Nishimura, T., Le, J., Morita, M. T., Bergmann, D. C., Dong, J. 1800; 13 (1): 7

  Abstract

  Cell polarity is a fundamental feature underlying cell morphogenesis and organismal development. In the Arabidopsis stomatal lineage, the polarity protein BASL controls stomatal asymmetric cell division. However, the cellular machinery by which this intrinsic polarity site is established remains unknown. Here, we identify the PRAF/RLD proteins as BASL physical partners and mutating four PRAF members leads to defects in BASL polarization. Members of PRAF proteins are polarized in stomatal lineage cells in a BASL-dependent manner. Developmental defects of the praf mutants phenocopy those of the gnom mutants. GNOM is an activator of the conserved Arf GTPases and plays important roles in membrane trafficking. We further find PRAF physically interacts with GNOM in vitro and in vivo. Thus, we propose that the positive feedback of BASL and PRAF at the plasma membrane and the connected function of PRAF and GNOM in endosomal trafficking establish intrinsic cell polarity in the Arabidopsis stomatal lineage.

  View details for DOI 10.1038/s41467-021-27748-w

  View details for PubMedID 35013279

• Advances in enzyme-mediated proximity labeling and its potential for plant research. Plant physiology Mair, A., Bergmann, D. C. 2021

  Abstract

  Cellular processes rely on the intimate interplay of different molecules, including DNA, RNA, proteins and metabolites. Obtaining and integrating data on their abundance and dynamics at high temporal and spatial resolution is essential for our understanding of plant growth and development. In the past decade, enzymatic proximity labeling (PL) has emerged as a powerful tool to study local protein and nucleotide ensembles, discover protein-protein and -nucleotide interactions and resolve questions about protein localization and membrane topology. An ever-growing number and continuous improvement of enzymes and methods keeps broadening the spectrum of possible applications for PL and makes it more accessible to different organisms, including plants. While initial PL experiments in plants required high expression levels and long labeling times, recently developed faster enzymes now enable PL of proteins on a cell type-specific level, even with low-abundant baits, and in different plant species. Moreover, expanding the use of PL for additional purposes, such as identification of locus-specific gene regulators or high-resolution electron microscopy may now be in reach. In this review, we give an overview of currently available PL enzymes and their applications in mammalian cell culture and plants. We discuss challenges and limitations of PL methods and highlight open questions and possible future directions for PL in plants.

  View details for DOI 10.1093/plphys/kiab479

  View details for PubMedID 34662401

• Vision, challenges and opportunities for a Plant Cell Atlas. eLife Plant Cell Atlas Consortium, Jha, S. G., Borowsky, A. T., Cole, B. J., Fahlgren, N., Farmer, A., Huang, S. C., Karia, P., Libault, M., Provart, N. J., Rice, S. L., Saura-Sanchez, M., Agarwal, P., Ahkami, A. H., Anderton, C. R., Briggs, S. P., Brophy, J. A., Denolf, P., Di Costanzo, L. F., Exposito-Alonso, M., Giacomello, S., Gomez-Cano, F., Kaufmann, K., Ko, D. K., Kumar, S., Malkovskiy, A. V., Nakayama, N., Obata, T., Otegui, M. S., Palfalvi, G., Quezada-Rodriguez, E. H., Singh, R., Uhrig, R. G., Waese, J., Van Wijk, K., Wright, R. C., Ehrhardt, D. W., Birnbaum, K. D., Rhee, S. Y., Ahmed, J., Alaba, O., Ameen, G., Arora, V., Arteaga-Vazquez, M. A., Arun, A., Bailey-Serres, J., Bartley, L. E., Bassel, G. W., Bergmann, D. C., Bertolini, E., Bhati, K. K., Blanco-Tourinan, N., Briggs, S. P., Brumos, J., Buer, B., Burlaocot, A., Cervantes-Perez, S. A., Chen, S., Contreras-Moreira, B., Corpas, F. J., Cruz-Ramirez, A., Cuevas-Velazquez, C. L., Cuperus, J. T., David, L. I., de Folter, S., Denolf, P. H., Ding, P., Dwyer, W. P., Evans, M. M., George, N., Handakumbura, P. P., Harrison, M. J., Haswell, E. S., Herath, V., Jiao, Y., Jinkerson, R. E., John, U., Joshi, S., Joshi, A., Joubert, L., Katam, R., Kaur, H., Kazachkova, Y., Raju, S. K., Khan, M. A., Khangura, R., Kumar, A., Kumar, A., Kumar, P., Kumar, P., Lavania, D., Lew, T. T., Lewsey, M. G., Lin, C., Liu, D., Liu, L., Liu, T., Lokdarshi, A., My Luong, A., Macaulay, I. C., Mahmud, S., Mahonen, A. P., Malukani, K. K., Marand, A. P., Martin, C. A., McWhite, C. D., Mehta, D., Martin, M. M., Mortimer, J. C., Nikolov, L. A., Nobori, T., Nolan, T. M., Ogden, A. J., Otegui, M. S., Ott, M., Palma, J. M., Paul, P., Rehman, A. U., Romera-Branchat, M., Romero, L. C., Roth, R., Sah, S. K., Shahan, R., Solanki, S., Song, B., Sozzani, R., Stacey, G., Stepanova, A. N., Taylor, N. L., Tello-Ruiz, M. K., Tran, T. M., Tripathi, R. K., Vadde, B. V., Varga, T., Vidovic, M., Walley, J. W., Wang, Z., Weizbauer, R. A., Whelan, J., Wijeratne, A. J., Xiang, T., Xu, S., Yadegari, R., Yu, H., Yuan, H. Y., Zanini, F., Zhao, F., Zhu, J., Zhuang, X. 2021; 10

  Abstract

  With growing populations and pressing environmental problems, future economies will be increasingly plant-based. Now is the time to reimagine plant science as a critical component of fundamental science, agriculture, environmental stewardship, energy, technology and healthcare. This effort requires a conceptual and technological framework to identify and map all cell types, and to comprehensively annotate the localization and organization of molecules at cellular and tissue levels. This framework, called the Plant Cell Atlas (PCA), will be critical for understanding and engineering plant development, physiology and environmental responses. A workshop was convened to discuss the purpose and utility of such an initiative, resulting in a roadmap that acknowledges the current knowledge gaps and technical challenges, and underscores how the PCA initiative can help to overcome them.

  View details for DOI 10.7554/eLife.66877

  View details for PubMedID 34491200

• Arabidopsis stomatal polarity protein BASL mediates distinct processes before and after cell division to coordinate cell size and fate asymmetries. Development (Cambridge, England) Gong, Y., Alassimone, J., Muroyama, A., Amador, G., Varnau, R., Liu, A., Bergmann, D. C. 2021

  Abstract

  In many land plants, asymmetric cell divisions (ACDs) create, and pattern differentiated cell types on the leaf surface. In the Arabidopsis stomatal lineage, BREAKING OF ASYMMETRY IN THE STOMATAL LINEAGE (BASL) regulates ACD division plane placement and cell fate enforcement. Polarized subcellular localization of BASL is initiated before ACD and persists for many hours after the division in one of the two daughters. Untangling the respective contributions of polarized BASL before and after division is essential to gain a better understanding of its roles in regulating stomatal lineage ACDs. Here we combine quantitative imaging and lineage tracking with genetic tools that provide temporally restricted BASL expression. We find that pre-division BASL is required for division orientation, whereas BASL polarity post-division ensures proper cell fate commitment. These genetic manipulations allowed us to uncouple daughter-cell size asymmetry from polarity crescent inheritance, revealing independent effects of these two asymmetries on subsequent cell behavior. Finally, we show that there is coordination between the division frequencies of sister cells produced by ACDs, and this coupling requires BASL as an effector of peptide signaling.

  View details for DOI 10.1242/dev.199919

  View details for PubMedID 34463761

• Plant single-cell solutions for energy and the environment. Communications biology Cole, B., Bergmann, D., Blaby-Haas, C. E., Blaby, I. K., Bouchard, K. E., Brady, S. M., Ciobanu, D., Coleman-Derr, D., Leiboff, S., Mortimer, J. C., Nobori, T., Rhee, S. Y., Schmutz, J., Simmons, B. A., Singh, A. K., Sinha, N., Vogel, J. P., O'Malley, R. C., Visel, A., Dickel, D. E. 2021; 4 (1): 962

  Abstract

  Progress in sequencing, microfluidics, and analysis strategies has revolutionized the granularity at which multicellular organisms can be studied. In particular, single-cell transcriptomics has led to fundamental new insights into animal biology, such as the discovery of new cell types and cell type-specific disease processes. However, the application of single-cell approaches to plants, fungi, algae, or bacteria (environmental organisms) has been far more limited, largely due to the challenges posed by polysaccharide walls surrounding these species' cells. In this perspective, we discuss opportunities afforded by single-cell technologies for energy and environmental science and grand challenges that must be tackled to apply these approaches to plants, fungi and algae. We highlight the need to develop better and more comprehensive single-cell technologies, analysis and visualization tools, and tissue preparation methods. We advocate for the creation of a centralized, open-access database to house plant single-cell data. Finally, we consider how such efforts should balance the need for deep characterization of select model species while still capturing the diversity in the plant kingdom. Investments into the development of methods, their application to relevant species, and the creation of resources to support data dissemination will enable groundbreaking insights to propel energy and environmental science forward.

  View details for DOI 10.1038/s42003-021-02477-4

  View details for PubMedID 34385583

• Transcriptional profiling reveals signatures of latent developmental potential in Arabidopsis stomatal lineage ground cells. Proceedings of the National Academy of Sciences of the United States of America Ho, C. K., Bringmann, M., Oshima, Y., Mitsuda, N., Bergmann, D. C. 2021; 118 (17)

  Abstract

  In many developmental contexts, cell lineages have variable or flexible potency to self-renew. What drives a cell to exit from a proliferative state and begin differentiation, or to retain the capacity to divide days or years later is not clear. Here we exploit the mixed potential of the stomatal lineage ground cell (SLGC) in the Arabidopsis leaf epidermis as a model to explore how cells might balance potential to differentiate with a reentry into proliferation. By generating transcriptomes of fluorescence-activated cell sorting-isolated populations that combinatorically define SLGCs and integrating these data with other stomatal lineage datasets, we find that SLGCs appear poised between proliferation and endoreduplication. Furthermore, we found the RNA polymerase II-related mediator complex interactor DEK and the transcription factor MYB16 accumulate differentially in the stomatal lineage and influence the extent of cell proliferation during leaf development. These findings suggest that SLGC latent potential is maintained by poising of the cell cycle machinery, as well as general and site-specific gene-expression regulators.

  View details for DOI 10.1073/pnas.2021682118

  View details for PubMedID 33875598

• Single-cell resolution of lineage trajectories in the Arabidopsis stomatal lineage and developing leaf. Developmental cell Lopez-Anido, C. B., Vaten, A., Smoot, N. K., Sharma, N., Guo, V., Gong, Y., Anleu Gil, M. X., Weimer, A. K., Bergmann, D. C. 2021; 56 (7): 1043

  Abstract

  Dynamic cell identities underlie flexible developmental programs. The stomatal lineage in the Arabidopsis leaf epidermis features asynchronous and indeterminate divisions that can be modulated by environmental cues. The products of the lineage, stomatal guard cells and pavement cells, regulate plant-atmosphere exchanges, and the epidermis as a whole influences overall leaf growth. How flexibility is encoded in development of the stomatal lineage and how cell fates are coordinated in the leaf are open questions. Here, by leveraging single-cell transcriptomics and molecular genetics, we uncovered models of cell differentiation within Arabidopsis leaf tissue. Profiles across leaf tissues identified points of regulatory congruence. In the stomatal lineage, single-cell resolution resolved underlying cell heterogeneity within early stages and provided a fine-grained profile of guard cell differentiation. Through integration of genome-scale datasets and spatiotemporally precise functional manipulations, we also identified an extended role for the transcriptional regulator SPEECHLESS in reinforcing cell fate commitment.

  View details for DOI 10.1016/j.devcel.2021.03.014

  View details for PubMedID 33823130

• Tuning self-renewal in the Arabidopsis stomatal lineage by hormone and nutrient regulation of asymmetric cell division. eLife Gong, Y., Alassimone, J., Varnau, R., Sharma, N., Cheung, L. S., Bergmann, D. C. 2021; 10

  Abstract

  Asymmetric and self-renewing divisions build and pattern tissues. In the Arabidopsis stomatal lineage, asymmetric cell divisions, guided by polarly localized cortical proteins, generate most cells on the leaf surface. Systemic and environmental signals modify tissue development, but the mechanisms by which plants incorporate such cues to regulate asymmetric divisions are elusive. In a screen for modulators of cell polarity, we identified CONSTITUTIVE TRIPLE RESPONSE1, a negative regulator of ethylene signaling. We subsequently revealed antagonistic impacts of ethylene and glucose signaling on the self-renewing capacity of stomatal lineage stem-cells. Quantitative analysis of cell polarity and fate dynamics showed that developmental information may be encoded in both the spatial and temporal asymmetries of polarity proteins. These results provide a framework for a mechanistic understanding of how nutritional status and environmental factors tune stem-cell behavior in the stomatal lineage, ultimately enabling flexibility in leaf size and cell-type composition.

  View details for DOI 10.7554/eLife.63335

  View details for PubMedID 33739283

• Evolution of polarity protein BASL and the capacity for stomatal lineage asymmetric divisions. Current biology : CB Nir, I., Amador, G., Gong, Y., Smoot, N. K., Cai, L., Shohat, H., Bergmann, D. C. 2021

  Abstract

  Asymmetric and oriented stem cell divisions enable the continued production of patterned tissues. The molecules that guide these divisions include several "polarity proteins" that are localized to discrete plasma membrane domains, are differentially inherited during asymmetric divisions, and whose scaffolding activities can guide division plane orientation and subsequent cell fates. In the stomatal lineages on the surfaces of plant leaves, asymmetric and oriented divisions create distinct cell types in physiologically optimized patterns. The polarity protein BREAKING OF ASYMMETRY IN THE STOMATAL LINEAGE (BASL) is a major regulator of stomatal lineage division and cell fate asymmetries in Arabidopsis, but its role in the stomatal lineages of other plants is unclear. Here, using phylogenetic and functional assays, we demonstrate that BASL is a eudicot-specific polarity protein. Dicot BASL orthologs can polarize in heterologous systems and rescue the Arabidopsis BASL mutant. The more widely distributed BASL-like proteins, although they share BASL's conserved C-terminal domain, are neither polarized nor do they function in asymmetric divisions of the stomatal lineage. Comparison of BASL protein localization and loss of function BASL phenotypes in Arabidopsis and tomato revealed previously unappreciated differences in how asymmetric cell divisions are employed for pattern formation in different species. This multi-species analysis therefore provides insight into the evolution of a unique polarity regulator and into the developmental choices available to cells as they build and pattern tissues.

  View details for DOI 10.1016/j.cub.2021.11.013

  View details for PubMedID 34847354

• How to build a crop plant: Defining the cis-regulatory landscape of maize. Cell Liu, A., Bergmann, D. C. 2021; 184 (11): 2804-2806

  Abstract

  The functional regulatory elements of agronomically important plant genomes have been long sought after. Marand et. al. generate a comprehensive atlas of cis-regulatory elements at single cell resolution in maize, providing a powerful resource for inquiries into the rules of multicellular development and for precision crop engineering.

  View details for DOI 10.1016/j.cell.2021.05.006

  View details for PubMedID 34048703

• Stomatal development in the grasses: lessons from models and crops (and crop models). The New phytologist McKown, K. H., Bergmann, D. C. 2020

  Abstract

  When plants emerged from their aquatic origins to colonize land, they needed to avoid desiccation while still enabling gas and water exchange with the environment. The solution was the development of a waxy cuticle interrupted by epidermal pores, known as stomata. Despite the importance of stomata in plant physiology and their contribution to global water and carbon cycles, our knowledge of the genetic basis of stomatal development is limited mostly to the model dicot, Arabidopsis thaliana. This limitation is particularly troublesome when evaluating grasses, whose members represent our most agriculturally-significant crops. Grass stomatal development follows a trajectory strikingly different from Arabidopsis and their uniquely shaped 4-celled stomatal complexes are especially responsive to environmental inputs. Thus, understanding the development and regulation of these efficient complexes is of particular interest for the purposes of crop engineering. This review focuses on genetic regulation of grass stomatal development and prospects for the future, highlighting discoveries enabled by parallel comparative investigations in cereal crops and related genetic model species such as Brachypodium distachyon.

  View details for DOI 10.1111/nph.16450

  View details for PubMedID 31985072

• Opposing, Polarity-Driven Nuclear Migrations Underpin Asymmetric Divisions to Pattern Arabidopsis Stomata. Current biology : CB Muroyama, A. n., Gong, Y. n., Bergmann, D. C. 2020

  Abstract

  Multicellular development depends on generating and precisely positioning distinct cell types within tissues. During leaf development, pores in the epidermis called stomata are spaced at least one cell apart for optimal gas exchange. This pattern is primarily driven by iterative asymmetric cell divisions (ACDs) in stomatal progenitors, which generate most of the cells in the tissue. A plasma membrane-associated polarity crescent defined by BREAKING OF ASYMMETRY IN THE STOMATAL LINEAGE (BASL) and BREVIS RADIX family (BRXf) proteins is required for asymmetric divisions and proper stomatal pattern, but the cellular mechanisms that orient ACDs remain unclear. Here, utilizing long-term, quantitative time-lapse microscopy, we identified two oppositely oriented nuclear migrations that precede and succeed ACD during epidermal patterning. The pre- and post-division migrations are dependent on microtubules and actin, respectively, and the polarity crescent is the unifying landmark that is both necessary and sufficient to orient both nuclear migrations. We identified a specific and essential role for MYOXI-I in controlling post-ACD nuclear migration. Loss of MYOXI-I decreases stomatal density, owing to an inability to accurately orient a specific subset of ACDs. Taken together, our analyses revealed successive and polarity-driven nuclear migrations that regulate ACD orientation in the Arabidopsis stomatal lineage.

  View details for DOI 10.1016/j.cub.2020.08.100

  View details for PubMedID 32946753

• Quantitative and dynamic cell polarity tracking in plant cells. The New phytologist Gong, Y. n., Varnau, R. n., Wallner, E. S., Acharya, R. n., Bergmann, D. C., Cheung, L. S. 2020

  Abstract

  Quantitative information on the spatiotemporal distribution of polarized proteins is central for understanding cell-fate determination, yet collecting sufficient data for statistical analysis is difficult to accomplish with manual measurements. Here we present POME, a semi-automated pipeline for the quantification of cell polarity, and demonstrate its application to a variety of developmental contexts. POME analysis reveals that during asymmetric cell divisions in the Arabidopsis thaliana stomatal lineage, polarity proteins BASL and BRXL2 are more asynchronous and less mutually dependent than previously thought. A similar analysis of the linearly arrayed stomatal lineage of Brachypodium distachyon revealed that the MAPKKK BdYDA1 is segregated and polarized following asymmetric divisions. Our results demonstrate that POME is a versatile tool, which by itself or combined with tissue-level studies and advanced microscopy techniques can help uncover new mechanisms of cell polarity.

  View details for DOI 10.1111/nph.17165

  View details for PubMedID 33378550

• The plant stomatal lineage a a glance JOURNAL OF CELL SCIENCE Lee, L. R., Bergmann, D. C. 2019; 132 (8)

  View details for DOI 10.1242/jcs.228551

  View details for Web of Science ID 000468129600017

• SOL1 and SOL2 regulate fate transition and cell divisions in the Arabidopsis stomatal lineage DEVELOPMENT Simmons, A. R., Davies, K. A., Wang, W., Liu, Z., Bergmann, D. C. 2019; 146 (3)

  View details for DOI 10.1242/dev.171066

  View details for Web of Science ID 000458841100011

• Cell-type-specific transcriptome and histone modification dynamics during cellular reprogramming in the Arabidopsis stomatal lineage. Proceedings of the National Academy of Sciences of the United States of America Lee, L. R., Wengier, D. L., Bergmann, D. C. 2019

  Abstract

  Plant cells maintain remarkable developmental plasticity, allowing them to clonally reproduce and to repair tissues following wounding; yet plant cells normally stably maintain consistent identities. Although this capacity was recognized long ago, our mechanistic understanding of the establishment, maintenance, and erasure of cellular identities in plants remains limited. Here, we develop a cell-type-specific reprogramming system that can be probed at the genome-wide scale for alterations in gene expression and histone modifications. We show that relationships among H3K27me3, H3K4me3, and gene expression in single cell types mirror trends from complex tissue, and that H3K27me3 dynamics regulate guard cell identity. Further, upon initiation of reprogramming, guard cells induce H3K27me3-mediated repression of a regulator of wound-induced callus formation, suggesting that cells in intact tissues may have mechanisms to sense and resist inappropriate dedifferentiation. The matched ChIP-sequencing (seq) and RNA-seq datasets created for this analysis also serve as a resource enabling inquiries into the dynamic and global-scale distribution of histone modifications in single cell types in plants.

  View details for DOI 10.1073/pnas.1911400116

  View details for PubMedID 31594845

• Proximity labeling of protein complexes and cell type-specific organellar proteomes in Arabidopsis enabled by TurboID. eLife Mair, A. n., Xu, S. L., Branon, T. C., Ting, A. Y., Bergmann, D. C. 2019; 8

  Abstract

  Defining specific protein interactions and spatially or temporally restricted local proteomes improves our understanding of all cellular processes, but obtaining such data is challenging, especially for rare proteins, cell types, or events. Proximity labeling enables discovery of protein neighborhoods defining functional complexes and/or organellar protein compositions. Recent technological improvements, namely two highly active biotin ligase variants (TurboID and miniTurbo), allowed us to address two challenging questions in plants: (1) what are in vivo partners of a low abundant key developmental transcription factor and (2) what is the nuclear proteome of a rare cell type? Proteins identified with FAMA-TurboID include known interactors of this stomatal transcription factor and novel proteins that could facilitate its activator and repressor functions. Directing TurboID to stomatal nuclei enabled purification of cell type- and subcellular compartment-specific proteins. Broad tests of TurboID and miniTurbo in Arabidopsis and N. benthamiana and versatile vectors enable customization by plant researchers.

  View details for DOI 10.7554/eLife.47864

  View details for PubMedID 31535972

• Stem-cell-ubiquitous genes spatiotemporally coordinate division through regulation of stem-cell-specific gene networks. Nature communications Clark, N. M., Buckner, E. n., Fisher, A. P., Nelson, E. C., Nguyen, T. T., Simmons, A. R., de Luis Balaguer, M. A., Butler-Smith, T. n., Sheldon, P. J., Bergmann, D. C., Williams, C. M., Sozzani, R. n. 2019; 10 (1): 5574

  Abstract

  Stem cells are responsible for generating all of the differentiated cells, tissues, and organs in a multicellular organism and, thus, play a crucial role in cell renewal, regeneration, and organization. A number of stem cell type-specific genes have a known role in stem cell maintenance, identity, and/or division. Yet, how genes expressed across different stem cell types, referred to here as stem-cell-ubiquitous genes, contribute to stem cell regulation is less understood. Here, we find that, in the Arabidopsis root, a stem-cell-ubiquitous gene, TESMIN-LIKE CXC2 (TCX2), controls stem cell division by regulating stem cell-type specific networks. Development of a mathematical model of TCX2 expression allows us to show that TCX2 orchestrates the coordinated division of different stem cell types. Our results highlight that genes expressed across different stem cell types ensure cross-communication among cells, allowing them to divide and develop harmonically together.

  View details for DOI 10.1038/s41467-019-13132-2

  View details for PubMedID 31811116

• Plant Cell Polarity: Creating Diversity from Inside the Box. Annual review of cell and developmental biology Muroyama, A. n., Bergmann, D. n. 2019; 35: 309–36

  Abstract

  Cell polarity in plants operates across a broad range of spatial and temporal scales to control processes from acute cell growth to systemic hormone distribution. Similar to other eukaryotes, plants generate polarity at both the subcellular and tissue levels, often through polarization of membrane-associated protein complexes. However, likely due to the constraints imposed by the cell wall and their extremely plastic development, plants possess novel polarity molecules and mechanisms highly tuned to environmental inputs. Considerable progress has been made in identifying key plant polarity regulators, but detailed molecular understanding of polarity mechanisms remains incomplete in plants. Here, we emphasize the striking similarities in the conceptual frameworks that generate polarity in both animals and plants. To this end, we highlight how novel, plant-specific proteins engage in common themes of positive feedback, dynamic intracellular trafficking, and posttranslational regulation to establish polarity axes in development. We end with a discussion of how environmental signals control intrinsic polarity to impact postembryonic organogenesis and growth.

  View details for DOI 10.1146/annurev-cellbio-100818-125211

  View details for PubMedID 31590583

• Taking Development to Three Dimensions DEVELOPMENTAL CELL Bergmann, D. C. 2018; 47 (6): 678-679

  View details for DOI 10.1016/j.devcel.2018.11.043

  View details for Web of Science ID 000453390700003

• Modulation of Asymmetric Division Diversity through Cytokinin and SPEECHLESS Regulatory Interactions in the Arabidopsis Stomatal Lineage DEVELOPMENTAL CELL Vaten, A., Soyars, C. L., Tarr, P. T., Nimchuk, Z. L., Bergmann, D. C. 2018; 47 (1): 53-+

  View details for DOI 10.1016/j.devcel.2018.08.007

  View details for Web of Science ID 000446579900005

• Modulation of Asymmetric Division Diversity through Cytokinin and SPEECHLESS Regulatory Interactions in the Arabidopsis Stomatal Lineage. Developmental cell Vaten, A., Soyars, C. L., Tarr, P. T., Nimchuk, Z. L., Bergmann, D. C. 2018

  Abstract

  Coordinated growth of organs requires communication among cells within and between tissues. In plants, leaf growth is largely dictated by the epidermis; here, asymmetric and self-renewing divisions of the stomatal lineage create two essential cell types-pavement cells and guard cells-in proportions reflecting inputs from local, systemic, and environmental cues. The transcription factor SPEECHLESS (SPCH) is the primeregulator of divisions, but whether and how it is influenced by external cues to provide flexible development is enigmatic. Here, we show that the phytohormone cytokinin (CK) can act as an endogenous signal to affect the extent and types of stomatal lineage divisions and forms a regulatory circuit withSPCH. Local domains of low CK signaling are created by SPCH-dependent cell-type-specific activity of two repressive type-A ARABIDOPSIS RESPONSE REGULATORs (ARRs), ARR16 and ARR17, and two secreted peptides, CLE9 and CLE10, which, together with SPCH, can customize epidermal cell-type composition.

  View details for PubMedID 30197241

• Grass stomata. Current biology : CB McKown, K. H., Bergmann, D. C. 2018; 28 (15): R814–R816

  Abstract

  Stomata are adjustable valves through which gas and water exchange occur in plant leaves. Here, McKown and Bergmann highlight the essential function and features of stomata from grasses.

  View details for PubMedID 30086309

• Grass stomata CURRENT BIOLOGY McKown, K. H., Bergmann, D. C. 2018; 28 (15): R814-R816

  View details for DOI 10.1016/j.cub.2018.05.074

  View details for Web of Science ID 000440787800004

• Conservation and divergence of YODA MAPKKK function in regulation of grass epidermal patterning DEVELOPMENT Abrash, E., Gil, M., Matos, J. L., Bergmann, D. C. 2018; 145 (14)

  View details for DOI 10.1242/dev.165860

  View details for Web of Science ID 000440421300020

• Conservation and divergence of YODA MAPKKK function in regulation of grass epidermal patterning. Development (Cambridge, England) Abrash, E., Anleu Gil, M. X., Matos, J. L., Bergmann, D. C. 2018

  Abstract

  All multicellular organisms must properly pattern cell types to generate functional tissues and organs. The organized and predictable cell lineages of the Brachypodium leaf enabled us to characterize the role of the MAPK kinase kinase gene BdYODA1 in regulating asymmetric cell divisions. We find that YODA genes promote normal stomatal spacing patterns in both Arabidopsis and Brachypodium, despite species-specific differences in those patterns. Using lineage tracing and cell fate markers, we show that, unexpectedly, patterning defects in bdyoda1 mutants do not arise from faulty physical asymmetry in cell divisions but rather from improper enforcement of alternative cellular fates after division. These cross-species comparisons allow us to refine our interpretations of MAPK activities during plant asymmetric cell divisions.

  View details for PubMedID 29945871

• Direct Control of SPEECHLESS by PIF4 in the High-Temperature Response of Stomatal Development CURRENT BIOLOGY Lau, O., Song, Z., Zhou, Z., Davies, K. A., Chang, J., Yang, X., Wang, S., Lucyshyn, D., Tay, I., Wigge, P. A., Bergmann, D. C. 2018; 28 (8): 1273-+

  Abstract

  Environmental factors shape the phenotypes of multicellular organisms. The production of stomata-the epidermal pores required for gas exchange in plants-is highly plastic and provides a powerful platform to address environmental influence on cell differentiation [1-3]. Rising temperatures are already impacting plant growth, a trend expected to worsen in the near future [4]. High temperature inhibits stomatal production, but the underlying mechanism is not known [5]. Here, we show that elevated temperature suppresses the expression of SPEECHLESS (SPCH), the basic-helix-loop-helix (bHLH) transcription factor that serves as the master regulator of stomatal lineage initiation [6, 7]. Our genetic and expression analyses indicate that the suppression of SPCH and stomatal production is mediated by the bHLH transcription factor PHYTOCHROME-INTERACTING FACTOR 4 (PIF4), a core component of high-temperature signaling [8]. Importantly, we demonstrate that, upon exposure to high temperature, PIF4 accumulates in the stomatal precursors and binds to the promoter of SPCH. In addition, we find SPCH feeds back negatively to the PIF4 gene. We propose a model where warm-temperature-activated PIF4 binds and represses SPCH expression to restrict stomatal production at elevated temperatures. Our work identifies a molecular link connecting high-temperature signaling and stomatal development and reveals a direct mechanism by which production of a specific cell lineage can be controlled by a broadly expressed environmental signaling factor.

  View details for PubMedID 29628371

  View details for PubMedCentralID PMC5931714

• Dissection of MAPK signaling specificity through protein engineering in a developmental context BMC PLANT BIOLOGY Wengier, D. L., Lampard, G. R., Bergmann, D. C. 2018; 18: 60

  Abstract

  Mitogen-activated protein kinases (MAPK) signaling affects many processes, some of which have different outcomes in the same cell. In Arabidopsis, activation of a MAPK cascade consisting of YODA, MKK4/5 and MPK3/6 inhibits early stages of stomatal developmental, but the ability to halt stomatal progression is lost at the later stage when guard mother cells (GMCs) transition to guard cells (GCs). Rather than downregulating cascade components, stomatal precursors must have a mechanism to prevent late stage inhibition because the same MKKs and MPKs mediate other physiological responses.We artificially activated the MAPK cascade using MKK7, another MKK that can modulate stomatal development, and found that inhibition of stomatal development is still possible in GMCs. This suggests that MKK4/5, but not MKK7, are specifically prevented from inhibiting stomatal development. To identify regions of MKKs responsible for cell-type specific regulation, we used a domain swap approach with MKK7 and a battery of in vitro and in vivo kinase assays. We found that N-terminal regions of MKK5 and MKK7 establish specific signal-to-output connections like they do in other organisms, but they do so in combination with previously undescribed modules in the C-terminus. One of these modules encoding the GMC-specific regulation of MKK5, when swapped with sequences from the equivalent region of MKK7, allows MKK5 to mediate robust inhibition of late stomatal development.Because MKK structure is conserved across species, the identification of new MKK specificity modules and signaling rules furthers our understanding of how eukaryotes create specificity in complex biological systems.

  View details for PubMedID 29636017

• Lineage- and stage-specific expressed CYCD7;1 coordinates the single symmetric division that creates stomatal guard cells DEVELOPMENT Weimer, A. K., Matos, J. L., Sharma, N., Patell, F., Murray, J. H., Dewitte, W., Bergmann, D. C. 2018; 145 (6)

  View details for DOI 10.1242/dev.160671

  View details for Web of Science ID 000601191000002

• Lineage- and stage-specific expressed CYCD7;1 coordinates the single symmetric division that creates stomatal guard cells. Development (Cambridge, England) Weimer, A. K., Matos, J. L., Sharma, N., Patell, F., Murray, J. A., Dewitte, W., Bergmann, D. C. 2018; 145 (6)

  Abstract

  Plants, with cells fixed in place by rigid walls, often utilize spatial and temporally distinct cell division programs to organize and maintain organs. This leads to the question of how developmental regulators interact with the cell cycle machinery to link cell division events with particular developmental trajectories. In Arabidopsis leaves, the development of stomata, two-celled epidermal valves that mediate plant-atmosphere gas exchange, relies on a series of oriented stem cell-like asymmetric divisions followed by a single symmetric division. The stomatal lineage is embedded in a tissue in which other cells transition from proliferation to postmitotic differentiation earlier, necessitating stomatal lineage-specific factors to prolong competence to divide. We show that the D-type cyclin, CYCD7;1, is specifically expressed just prior to the symmetric guard cell-forming division, and that it is limiting for this division. Further, we find that CYCD7;1 is capable of promoting divisions in multiple contexts, likely through RBR1-dependent promotion of the G1/S transition, but that CYCD7;1 is regulated at the transcriptional level by cell type-specific transcription factors that confine its expression to the appropriate developmental window.

  View details for PubMedID 29467245

• Disruption of stomatal lineage signaling or transcriptional regulators has differential effects on mesophyll development, but maintains coordination of gas exchange. The New phytologist Dow, G. J., Berry, J. A., Bergmann, D. C. 2017; 216 (1): 69-75

  Abstract

  Stomata are simultaneously tasked with permitting the uptake of carbon dioxide for photosynthesis while limiting water loss from the plant. This process is mainly regulated by guard cell control of the stomatal aperture, but recent advancements have highlighted the importance of several genes that control stomatal development. Using targeted genetic manipulations of the stomatal lineage and a combination of gas exchange and microscopy techniques, we show that changes in stomatal development of the epidermal layer lead to coupled changes in the underlying mesophyll tissues. This coordinated response tends to match leaf photosynthetic potential (Vcmax ) with gas-exchange capacity (gsmax ), and hence the uptake of carbon dioxide for water lost. We found that different genetic regulators systematically altered tissue coordination in separate ways: the transcription factor SPEECHLESS (SPCH) primarily affected leaf size and thickness, whereas peptides in the EPIDERMAL PATTERNING FACTOR (EPF) family altered cell density in the mesophyll. It was also determined that interlayer coordination required the cell-surface receptor TOO MANY MOUTHS (TMM). These results demonstrate that stomata-specific regulators can alter mesophyll properties, which provides insight into how molecular pathways can organize leaf tissues to coordinate gas exchange and suggests new strategies for improving plant water-use efficiency.

  View details for DOI 10.1111/nph.14746

  View details for PubMedID 28833173

  View details for PubMedCentralID PMC5601202

• Think global, act local: Integrating polarities across developing organs Bergmann, D., Rowe, M., Bringmann, M. ELSEVIER SCIENCE BV. 2017: S4

  View details for DOI 10.1016/j.mod.2017.04.525

  View details for Web of Science ID 000402994800014

• A Celebration of Fred David Sack PLANT PHYSIOLOGY Bergmann, D., Clare, D., Samuels, L., Kiss, J. Z. 2017; 174 (2): 470-472

  View details for DOI 10.1104/pp.16.01832

  View details for Web of Science ID 000403152200002

  View details for PubMedID 28584064

  View details for PubMedCentralID PMC5462016

• Tissue-wide Mechanical Forces Influence the Polarity of Stomatal Stem Cells in Arabidopsis CURRENT BIOLOGY Bringmann, M., Bergmann, D. C. 2017; 27 (6): 877-883

  Abstract

  Mechanical information is an important contributor to cell polarity in uni- and multicellular systems [1-3]. In planar tissues like the Drosophila wing, cell polarity reorients during growth as cells divide and reorganize [4]. In another planar tissue, the Arabidopsis leaf epidermis [5], polarized, asymmetric divisions of stomatal stem cells (meristemoid mother cells [MMCs]) are fundamental for the generation and patterning of multiple cell types, including stomata. The activity of key transcription factors, polarizing factors [6], and peptide signals [7] explains some local stomatal patterns emerging from the behavior of a few lineally related cells [6, 8-11]. Here we demonstrate that, in addition to locally acting signals, tissue-wide mechanical forces can act as organizing cues, and that they do so by influencing the polarity of individual MMCs. If the mechanical stress environment in the tissue is altered through stretching or cell ablations, cellular polarity changes in response. In turn, polarity predicts the orientation of cellular and tissue outgrowth, leading to increased mechanical conflicts between neighboring cells. This interplay among growth, oriented divisions, and cell specification could contribute to the characteristic patterning of stomatal guard cells in the context of a growing leaf.

  View details for DOI 10.1016/j.cub.2017.01.059

  View details for Web of Science ID 000397351800030

  View details for PubMedID 28285992

• Mobile MUTE specifies subsidiary cells to build physiologically improved grass stomata SCIENCE Raissig, M. T., Matos, J. L., Gil, M. X., Kornfeld, A., Bettadapur, A., Abrash, E., Allison, H. R., Badgley, G., Vogel, J. P., Berry, J. A., Bergmann, D. C. 2017; 355 (6330): 1215-1218

  Abstract

  Plants optimize carbon assimilation while limiting water loss by adjusting stomatal aperture. In grasses, a developmental innovation-the addition of subsidiary cells (SCs) flanking two dumbbell-shaped guard cells (GCs)-is linked to improved stomatal physiology. Here, we identify a transcription factor necessary and sufficient for SC formation in the wheat relative Brachypodium distachyon. Unexpectedly, the transcription factor is an ortholog of the stomatal regulator AtMUTE, which defines GC precursor fate in Arabidopsis The novel role of BdMUTE in specifying lateral SCs appears linked to its acquisition of cell-to-cell mobility in Brachypodium Physiological analyses on SC-less plants experimentally support classic hypotheses that SCs permit greater stomatal responsiveness and larger range of pore apertures. Manipulation of SC formation and function in crops, therefore, may be an effective approach to enhance plant performance.

  View details for DOI 10.1126/science.aal3254

  View details for Web of Science ID 000396351200046

  View details for PubMedID 28302860

• Origin and function of stomata in the moss Physcomitrella patens. Nature plants Chater, C. C., Caine, R. S., Tomek, M., Wallace, S., Kamisugi, Y., Cuming, A. C., Lang, D., MacAlister, C. A., Casson, S., Bergmann, D. C., Decker, E. L., Frank, W., Gray, J. E., Fleming, A., Reski, R., Beerling, D. J. 2016; 2: 16179-?

  Abstract

  Stomata are microscopic valves on plant surfaces that originated over 400 million years (Myr) ago and facilitated the greening of Earth's continents by permitting efficient shoot-atmosphere gas exchange and plant hydration(1). However, the core genetic machinery regulating stomatal development in non-vascular land plants is poorly understood(2-4) and their function has remained a matter of debate for a century(5). Here, we show that genes encoding the two basic helix-loop-helix proteins PpSMF1 (SPEECH, MUTE and FAMA-like) and PpSCREAM1 (SCRM1) in the moss Physcomitrella patens are orthologous to transcriptional regulators of stomatal development in the flowering plant Arabidopsis thaliana and essential for stomata formation in moss. Targeted P. patens knockout mutants lacking either PpSMF1 or PpSCRM1 develop gametophytes indistinguishable from wild-type plants but mutant sporophytes lack stomata. Protein-protein interaction assays reveal heterodimerization between PpSMF1 and PpSCRM1, which, together with moss-angiosperm gene complementations(6), suggests deep functional conservation of the heterodimeric SMF1 and SCRM1 unit is required to activate transcription for moss stomatal development, as in A. thaliana(7). Moreover, stomata-less sporophytes of ΔPpSMF1 and ΔPpSCRM1 mutants exhibited delayed dehiscence, implying stomata might have promoted dehiscence in the first complex land-plant sporophytes.

  View details for DOI 10.1038/nplants.2016.179

  View details for PubMedID 27892923

  View details for PubMedCentralID PMC5131878

• Fine-scale dissection of the subdomains of polarity protein BASL in stomatal asymmetric cell division. Journal of experimental botany Zhang, Y., Bergmann, D. C., Dong, J. 2016; 67 (17): 5093-5103

  Abstract

  Cell polarity is a prerequisite for asymmetric cell divisions (ACDs) that generate cell type diversity during development of multicellular organisms. In Arabidopsis, stomatal lineage ACDs are regulated by the plant-specific protein BREAKING OF ASYMMETRY IN THE STOMATAL LINEAGE (BASL). BASL exhibits dynamic subcellular localization, accumulating initially in the nucleus, but then additionally in a highly polarized crescent at the cell cortex before division. BASL polarization requires a phosphorylation-mediated activation process, but how this is achieved remains unknown. In this study, we performed a fine-scale dissection of BASL protein subdomains and elucidated a nuclear localization sequence for nuclear import and a critical FxFP motif for cortical polarity formation, respectively. Artificially tethering BASL subdomains to the plasma membrane suggests that novel protein partner/s might exist and bind to an internal region of BASL. In addition, we suspect the existence of a protein degradation mechanism associated with the amino terminal domain of BASL that accounts for restricting its predominant expression to the stomatal lineage cells of the epidermis. Taken together, our results revealed that BASL, through its distinct subdomains, integrates multiple regulatory inputs to provide a mechanism that promotes difference during stomatal lineage ACDs.

  View details for DOI 10.1093/jxb/erw274

  View details for PubMedID 27422992

  View details for PubMedCentralID PMC5014157

• Modulators of Stomatal Lineage Signal Transduction Alter Membrane Contact Sites and Reveal Specialization among ERECTA Kinases. Developmental cell Ho, C. K., Paciorek, T., Abrash, E., Bergmann, D. C. 2016; 38 (4): 345-357

  Abstract

  Signal transduction from a cell's surface to its interior requires dedicated signaling elements and a cellular environment conducive to signal propagation. Plant development, defense, and homeostasis rely on plasma membrane receptor-like kinases to perceive endogenous and environmental signals, but little is known about their immediate downstream targets and signaling modifiers. Using genetics, biochemistry, and live-cell imaging, we show that the VAP-RELATED SUPPRESSOR OF TMM (VST) family is required for ERECTA-mediated signaling in growth and cell-fate determination and reveal a role for ERECTA-LIKE2 in modulating signaling by its sister kinases. We show that VSTs are peripheral plasma membrane proteins that can form complexes with integral ER-membrane proteins, thereby potentially influencing the organization of the membrane milieu to promote efficient and differential signaling from the ERECTA-family members to their downstream intracellular targets.

  View details for DOI 10.1016/j.devcel.2016.07.016

  View details for PubMedID 27554856

• Grasses use an alternatively wired bHLH transcription factor network to establish stomatal identity. Proceedings of the National Academy of Sciences of the United States of America Raissig, M. T., Abrash, E., Bettadapur, A., Vogel, J. P., Bergmann, D. C. 2016; 113 (29): 8326-8331

  Abstract

  Stomata, epidermal valves facilitating plant-atmosphere gas exchange, represent a powerful model for understanding cell fate and pattern in plants. Core basic helix-loop-helix (bHLH) transcription factors regulating stomatal development were identified in Arabidopsis, but this dicot's developmental pattern and stomatal morphology represent only one of many possibilities in nature. Here, using unbiased forward genetic screens, followed by analysis of reporters and engineered mutants, we show that stomatal initiation in the grass Brachypodium distachyon uses orthologs of stomatal regulators known from Arabidopsis but that the function and behavior of individual genes, the relationships among genes, and the regulation of their protein products have diverged. Our results highlight ways in which a kernel of conserved genes may be alternatively wired to produce diversity in patterning and morphology and suggest that the stomatal transcription factor module is a prime target for breeding or genome modification to improve plant productivity.

  View details for DOI 10.1073/pnas.1606728113

  View details for PubMedID 27382177

  View details for PubMedCentralID PMC4961163

• Arabidopsis CSLD5 Functions in Cell Plate Formation in a Cell Cycle-Dependent Manner. Plant cell Gu, F., Bringmann, M., Combs, J. R., Yang, J., Bergmann, D. C., Nielsen, E. 2016; 28 (7): 1722-1737

  Abstract

  In plants, the presence of a load-bearing cell wall presents unique challenges during cell division. Unlike other eukaryotes, which undergo contractile cytokinesis upon completion of mitosis, plants instead synthesize and assemble a new dividing cell wall to separate newly formed daughter cells. Here, we mine transcriptome data from individual cell types in the Arabidopsis thaliana stomatal lineage and identify CSLD5, a member of the Cellulose Synthase Like-D family, as a cell wall biosynthesis enzyme uniquely enriched in rapidly dividing cell populations. We further show that CSLD5 is a direct target of SPEECHLESS, the master transcriptional regulator of these divisions during stomatal development. Using a combination of genetic analysis and in vivo localization of fluorescently tagged fusion proteins, we show that CSLD5 preferentially accumulates in dividing plant cells where it participates in the construction of newly forming cell plates. We show that CSLD5 is an unstable protein that is rapidly degraded upon completion of cell division and that the protein turnover characteristics of CSLD5 are altered in ccs52a2 mutants, indicating that CSLD5 turnover may be regulated by a cell cycle-associated E3-ubiquitin ligase, the anaphase-promoting complex.

  View details for DOI 10.1105/tpc.16.00203

  View details for PubMedID 27354558

  View details for PubMedCentralID PMC4981133

• 50 years of Arabidopsis research: highlights and future directions NEW PHYTOLOGIST Provart, N. J., Alonso, J., Assmann, S. M., Bergmann, D., Brady, S. M., Brkljacic, J., Browse, J., Chapple, C., Colot, V., Cutler, S., Dangl, J., Ehrhardt, D., Friesner, J. D., Frommer, W. B., Grotewold, E., Meyerowitz, E., Nemhauser, J., Nordborg, M., Pikaard, C., Shanklin, J., Somerville, C., Stitt, M., Torii, K. U., Waese, J., Wagner, D., McCourt, P. 2016; 209 (3): 921-944

  Abstract

  922 I. 922 II. 922 III. 925 IV. 925 V. 926 VI. 927 VII. 928 VIII. 929 IX. 930 X. 931 XI. 932 XII. 933 XIII. Natural variation and genome-wide association studies 934 XIV. 934 XV. 935 XVI. 936 XVII. 937 937 References 937 SUMMARY: The year 2014 marked the 25(th) International Conference on Arabidopsis Research. In the 50 yr since the first International Conference on Arabidopsis Research, held in 1965 in Göttingen, Germany, > 54 000 papers that mention Arabidopsis thaliana in the title, abstract or keywords have been published. We present herein a citational network analysis of these papers, and touch on some of the important discoveries in plant biology that have been made in this powerful model system, and highlight how these discoveries have then had an impact in crop species. We also look to the future, highlighting some outstanding questions that can be readily addressed in Arabidopsis. Topics that are discussed include Arabidopsis reverse genetic resources, stock centers, databases and online tools, cell biology, development, hormones, plant immunity, signaling in response to abiotic stress, transporters, biosynthesis of cells walls and macromolecules such as starch and lipids, epigenetics and epigenomics, genome-wide association studies and natural variation, gene regulatory networks, modeling and systems biology, and synthetic biology.

  View details for DOI 10.1111/nph.13687

  View details for Web of Science ID 000373378000009

  View details for PubMedID 26465351

• Transcriptional control of cell fate in the stomatal lineage. Current opinion in plant biology Simmons, A. R., Bergmann, D. C. 2016; 29: 1-8

  Abstract

  The Arabidopsis stomatal lineage is a microcosm of development; it undergoes selection of precursor cells, asymmetric and stem cell-like divisions, cell commitment and finally, acquisition of terminal cell fates. Recent transcriptomic approaches revealed major shifts in gene expression accompanying each fate transition, and mechanistic analysis of key bHLH transcription factors, along with mathematical modeling, has begun to unravel how these major shifts are coordinated. In addition, stomatal initiation is proving to be a tractable model for defining the genetic and epigenetic basis of stable cell identities and for understanding the integration of environmental responses into developmental programs.

  View details for DOI 10.1016/j.pbi.2015.09.008

  View details for PubMedID 26550955

  View details for PubMedCentralID PMC4753106

• MOBE-ChIP: a large-scale chromatin immunoprecipitation assay for cell type-specific studies PLANT JOURNAL Lau, O. S., Bergmann, D. C. 2015; 84 (2): 443-450

  Abstract

  Cell type-specific transcriptional regulators play critical roles in the generation and maintenance of multicellularity. As they are often expressed at low levels, in vivo DNA-binding studies of these regulators by standard chromatin immunoprecipitation (ChIP) assays are technically challenging. We describe here an optimized ChIP protocol termed Maximized Objects for Better Enrichment (MOBE)-ChIP, which enhances the sensitivity of ChIP assays for detecting cell type-specific signals. The protocol, which is based on the disproportional increase of target signals over background at higher scales, uses substantially greater volume of starting materials than conventional ChIPs to achieve high signal enrichment. This technique can capture weak binding events that are ambiguous in standard ChIP assays, and is useful both in gene-specific and whole-genome analysis. This protocol has been optimized for Arabidopsis, but should be applicable to other model systems with minor modifications. The full procedure can be completed within 3 days.

  View details for DOI 10.1111/tpj.13010

  View details for PubMedID 26332947

  View details for PubMedCentralID PMC4600040

• Manipulation of mitogen-activated protein kinase kinase signaling in the Arabidopsis stomatal lineage reveals motifs that contribute to protein localization and signaling specificity (vol 26, pg 3358, 2014) PLANT CELL Lampard, G. R., Wengier, D. L., Bergmann, D. C. 2015; 27 (7): 2073-2074

  View details for DOI 10.1105/tpc.15.00512

  View details for Web of Science ID 000359358600022

• Transcriptome Dynamics of the Stomatal Lineage: Birth, Amplification, and Termination of a Self-Renewing Population DEVELOPMENTAL CELL Adrian, J., Chang, J., Ballenger, C. E., Bargmann, B. O., Alassimone, J., Davies, K. A., Lau, O. S., Matos, J. L., Hachez, C., Lanctot, A., Vaten, A., Birnbaum, K. D., Bergmann, D. C. 2015; 33 (1): 107-118

  Abstract

  Developmental transitions can be described in terms of morphology and the roles of individual genes, but also in terms of global transcriptional and epigenetic changes. Temporal dissections of transcriptome changes, however, are rare for intact, developing tissues. We used RNA sequencing and microarray platforms to quantify gene expression from labeled cells isolated by fluorescence-activated cell sorting to generate cell-type-specific transcriptomes during development of an adult stem-cell lineage in the Arabidopsis leaf. We show that regulatory modules in this early lineage link cell types that had previously been considered to be under separate control and provide evidence for recruitment of individual members of gene families for different developmental decisions. Because stomata are physiologically important and because stomatal lineage cells exhibit exemplary division, cell fate, and cell signaling behaviors, this dataset serves as a valuable resource for further investigations of fundamental developmental processes.

  View details for DOI 10.1016/j.devcel.2015.01.025

  View details for PubMedID 25850675

• Regulation of Guard Cell Formation by Integration of Transcriptional and Signaling Regulation PLANT CELL WALL PATTERNING AND CELL SHAPE Ho, C., Bergmann, D. C., Fukuda, H. 2015: 321-349

  View details for Web of Science ID 000362178100013

• Dominique Bergmann: Passionate about plant polarity JOURNAL OF CELL BIOLOGY Powell, K., Bergmann, D. 2014; 207 (6): 680-681

  Abstract

  Bergmann studies stomatal development to discover how plant cells parse polarity and fate.

  View details for DOI 10.1083/jcb.2076pi

  View details for Web of Science ID 000346821500002

  View details for PubMedID 25533841

  View details for PubMedCentralID PMC4274260

• Arabidopsis Reduces Growth Under Osmotic Stress by Decreasing SPEECHLESS Protein. Plant and cell physiology Kumari, A., Jewaria, P. K., Bergmann, D. C., Kakimoto, T. 2014; 55 (12): 2037-2046

  Abstract

  Plants, which are sessile unlike most animals, have evolved a system to reduce growth under stress; however, the molecular mechanisms of this stress response are not well known. During programmed development, a fraction of the leaf epidermal precursor cells become meristemoid mother cells (MMCs), which are stem cells that produce both stomatal guard cells and epidermal pavement cells. Here we report that Arabidopsis plants, in response to osmotic stress, post-transcriptionally decrease the protein level of SPEECHLESS, the transcription factor promoting MMC identity, through the action of a mitogen-activated protein kinase (MAPK) cascade. The growth reduction under osmotic stress was lessened by inhibition of the MAPK cascade or by a mutation that disrupted the MAPK target amino acids in SPEECHLESS, indicating that Arabidopsis reduces growth under stress by integrating the osmotic stress signal into the MAPK-SPEECHLESS core developmental pathway.

  View details for DOI 10.1093/pcp/pcu159

  View details for PubMedID 25381317

• Functional specialization of stomatal bHLHs through modification of DNA-binding and phosphoregulation potential PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA Davies, K. A., Bergmann, D. C. 2014; 111 (43): 15585-15590

  Abstract

  Transcription factor duplication events and subsequent specialization can drive evolution by facilitating biological innovation and developmental complexity. Identification of sequences that confer distinct biochemical function in vivo is an important step in understanding how related factors could refine specific developmental processes over time. Functional analysis of the basic helix-loop-helix (bHLH) protein SPEECHLESS, one of three closely related transcription factors required for stomatal lineage progression in Arabidopsis thaliana, allowed a dissection of motifs associated with specific developmental outputs. Phosphorylated residues, shown previously to quantitatively affect activity, also allow a qualitative shift in function between division and cell fate-promoting activities. Our data also provide surprising evidence that, despite deep sequence conservation in DNA-binding domains, the functional requirement for these domains has diverged, with the three stomatal bHLHs exhibiting absolute, partial, or no requirements for DNA-binding residues for their in vivo activities. Using these data, we build a plausible model describing how the current unique and overlapping roles of these proteins might have evolved from a single ancestral protein.

  View details for DOI 10.1073/pnas.1411766111

  View details for Web of Science ID 000343729500076

• Irreversible fate commitment in the Arabidopsis stomatal lineage requires a FAMA and RETINOBLASTOMA-RELATED module ELIFE Matos, J. L., Lau, O. S., Hachez, C., Cruz-Ramirez, A., Scheres, B., Bergmann, D. C. 2014; 3

  Abstract

  The presumed totipotency of plant cells leads to questions about how specific stem cell lineages and terminal fates could be established. In the Arabidopsis stomatal lineage, a transient self-renewing phase creates precursors that differentiate into one of two epidermal cell types, guard cells or pavement cells. We found that irreversible differentiation of guard cells involves RETINOBLASTOMA-RELATED (RBR) recruitment to regulatory regions of master regulators of stomatal initiation, facilitated through interaction with a terminal stomatal lineage transcription factor, FAMA. Disrupting physical interactions between FAMA and RBR preferentially reveals the role of RBR in enforcing fate commitment over its role in cell-cycle control in this developmental context. Analysis of the phenotypes linked to the modulation of FAMA and RBR sheds new light on the way iterative divisions and terminal differentiation are coordinately regulated in a plant stem-cell lineage.

  View details for DOI 10.7554/eLife.03271

  View details for Web of Science ID 000343420700004

• Patterning and processes: how stomatal development defines physiological potential CURRENT OPINION IN PLANT BIOLOGY Dow, G. J., Bergmann, D. C. 2014; 21: 67-74

  Abstract

  Stomata present an excellent opportunity for connecting scientific disciplines: they are governed by complex genetic controls and unique cell biology, while also possessing a large influence over plant productivity and relationships with the environment. For this reason, stomata have engaged scientists for many centuries and continue to be a central interest for many fields of research. Recent technological advances have enabled interdisciplinary studies of stomata that were previously out of reach, and as a result, we are beginning to realize new insights about stomatal biology that place them at the intersection of our changing world. This review is intended to describe these interdisciplinary connections, discuss the relevant scales at which they are having an influence, and highlight ways we can capitalize on such novel approaches. While we incorporate knowledge about molecular advances, this is not intended to be an extensive review of that field, but rather, we focus on how those systems inform plant physiology and are connected to global scales.

  View details for DOI 10.1016/j.pbi.2014.06.007

  View details for Web of Science ID 000345255300011

• Patterning and processes: how stomatal development defines physiological potential. Current opinion in plant biology Dow, G. J., Bergmann, D. C. 2014; 21: 67-74

  Abstract

  Stomata present an excellent opportunity for connecting scientific disciplines: they are governed by complex genetic controls and unique cell biology, while also possessing a large influence over plant productivity and relationships with the environment. For this reason, stomata have engaged scientists for many centuries and continue to be a central interest for many fields of research. Recent technological advances have enabled interdisciplinary studies of stomata that were previously out of reach, and as a result, we are beginning to realize new insights about stomatal biology that place them at the intersection of our changing world. This review is intended to describe these interdisciplinary connections, discuss the relevant scales at which they are having an influence, and highlight ways we can capitalize on such novel approaches. While we incorporate knowledge about molecular advances, this is not intended to be an extensive review of that field, but rather, we focus on how those systems inform plant physiology and are connected to global scales.

  View details for DOI 10.1016/j.pbi.2014.06.007

  View details for PubMedID 25058395

• Direct roles of SPEECHLESS in the specification of stomatal self-renewing cells SCIENCE Lau, O. S., Davies, K. A., Chang, J., Adrian, J., Rowe, M. H., Ballenger, C. E., Bergmann, D. C. 2014; 345 (6204): 1605-1609

  Abstract

  Lineage-specific stem cells are critical for the production and maintenance of specific cell types and tissues in multicellular organisms. In Arabidopsis, the initiation and proliferation of stomatal lineage cells is controlled by the basic helix-loop-helix transcription factor SPEECHLESS (SPCH). SPCH-driven asymmetric and self-renewing divisions allow flexibility in stomatal production and overall organ growth. How SPCH directs stomatal lineage cell behaviors, however, is unclear. Here, we improved the chromatin immunoprecipitation (ChIP) assay and profiled the genome-wide targets of Arabidopsis SPCH in vivo. We found that SPCH controls key regulators of cell fate and asymmetric cell divisions and modulates responsiveness to peptide and phytohormone-mediated intercellular communication. Our results delineate the molecular pathways that regulate an essential adult stem cell lineage in plants.

  View details for DOI 10.1126/science.1256888

  View details for Web of Science ID 000342164500044

  View details for PubMedCentralID PMC4390554

• Direct roles of SPEECHLESS in the specification of stomatal self-renewing cells. Science Lau, O. S., Davies, K. A., Chang, J., Adrian, J., Rowe, M. H., Ballenger, C. E., Bergmann, D. C. 2014; 345 (6204): 1605-1609

  Abstract

  Lineage-specific stem cells are critical for the production and maintenance of specific cell types and tissues in multicellular organisms. In Arabidopsis, the initiation and proliferation of stomatal lineage cells is controlled by the basic helix-loop-helix transcription factor SPEECHLESS (SPCH). SPCH-driven asymmetric and self-renewing divisions allow flexibility in stomatal production and overall organ growth. How SPCH directs stomatal lineage cell behaviors, however, is unclear. Here, we improved the chromatin immunoprecipitation (ChIP) assay and profiled the genome-wide targets of Arabidopsis SPCH in vivo. We found that SPCH controls key regulators of cell fate and asymmetric cell divisions and modulates responsiveness to peptide and phytohormone-mediated intercellular communication. Our results delineate the molecular pathways that regulate an essential adult stem cell lineage in plants.

  View details for DOI 10.1126/science.1256888

  View details for PubMedID 25190717

• Coordinating cell polarity: heading in the right direction? DEVELOPMENT Axelrod, J. D., Bergmann, D. C. 2014; 141 (17): 3298-3302

  Abstract

  A diverse group of researchers working on both plant and animal systems met at a Company of Biologists workshop to discuss 'Coordinating Cell Polarity'. The meeting included considerable free discussion as well as presentations exploring the ways that groups of cells in these various systems achieve coordinated cell polarity. Here, we discuss commonalities, differences and themes that emerged from these sessions that will serve to inform ongoing studies.

  View details for DOI 10.1242/dev.111484

  View details for Web of Science ID 000341305900003

• Coordinating cell polarity: heading in the right direction? Development (Cambridge, England) Axelrod, J. D., Bergmann, D. C. 2014; 141 (17): 3298-302

  Abstract

  A diverse group of researchers working on both plant and animal systems met at a Company of Biologists workshop to discuss 'Coordinating Cell Polarity'. The meeting included considerable free discussion as well as presentations exploring the ways that groups of cells in these various systems achieve coordinated cell polarity. Here, we discuss commonalities, differences and themes that emerged from these sessions that will serve to inform ongoing studies.

  View details for DOI 10.1242/dev.111484

  View details for PubMedID 25139852

• Manipulation of Mitogen-Activated Protein Kinase Kinase Signaling in the Arabidopsis Stomatal Lineage Reveals Motifs That Contribute to Protein Localization and Signaling Specificity PLANT CELL Lampard, G. R., Wengier, D. L., Bergmann, D. C. 2014; 26 (8): 3358-3371

  Abstract

  When multiple mitogen-activated protein kinase (MAPK) components are recruited recurrently to transduce signals of different origins, and often opposing outcomes, mechanisms to enforce signaling specificity are of utmost importance. These mechanisms are largely uncharacterized in plant MAPK signaling networks. The Arabidopsis thaliana stomatal lineage was previously used to show that when rendered constitutively active, four MAPK kinases (MKKs), MKK4/5/7/9, are capable of perturbing stomatal development and that these kinases comprise two pairs, MKK4/5 and MKK7/9, with both overlapping and divergent functions. We characterized the contributions of specific structural domains of these four "stomatal" MKKs to MAPK signaling output and specificity both in vitro and in vivo within the three discrete cell types of the stomatal lineage. These results verify the influence of functional docking (D) domains of MKKs on MAPK signal output and identify novel regulatory functions for previously uncharacterized structures within the N termini of MKK4/5. Beyond this, we present a novel function of the D-domains of MKK7/9 in regulating the subcellular localization of these kinases. These results provide tools to broadly assess the extent to which these and additional motifs within MKKs function to regulate MAPK signal output throughout the plant.

  View details for DOI 10.1105/tpc.114.127415

  View details for Web of Science ID 000345918600012

  View details for PubMedID 25172143

• Omics and modelling approaches for understanding regulation of asymmetric cell divisions in arabidopsis and other angiosperm plants ANNALS OF BOTANY Kajala, K., Ramakrishna, P., Fisher, A., Bergmann, D. C., De Smet, I., Sozzani, R., Weijers, D., Brady, S. M. 2014; 113 (7): 1083-1105

  Abstract

  Asymmetric cell divisions are formative divisions that generate daughter cells of distinct identity. These divisions are coordinated by either extrinsic ('niche-controlled') or intrinsic regulatory mechanisms and are fundamentally important in plant development.This review describes how asymmetric cell divisions are regulated during development and in different cell types in both the root and the shoot of plants. It further highlights ways in which omics and modelling approaches have been used to elucidate these regulatory mechanisms. For example, the regulation of embryonic asymmetric divisions is described, including the first divisions of the zygote, formative vascular divisions and divisions that give rise to the root stem cell niche. Asymmetric divisions of the root cortex endodermis initial, pericycle cells that give rise to the lateral root primordium, procambium, cambium and stomatal cells are also discussed. Finally, a perspective is provided regarding the role of other hormones or regulatory molecules in asymmetric divisions, the presence of segregated determinants and the usefulness of modelling approaches in understanding network dynamics within these very special cells.Asymmetric cell divisions define plant development. High-throughput genomic and modelling approaches can elucidate their regulation, which in turn could enable the engineering of plant traits such as stomatal density, lateral root development and wood formation.

  View details for DOI 10.1093/aob/mcu065

  View details for Web of Science ID 000337033100001

  View details for PubMedCentralID PMC4030820

• An integrated model of stomatal development and leaf physiology NEW PHYTOLOGIST Dow, G. J., Bergmann, D. C., Berry, J. A. 2014; 201 (4): 1218-1226

  Abstract

  Stomatal conductance (gs ) is constrained by the size and number of stomata on the plant epidermis, and the potential maximum rate of gs can be calculated based on these stomatal traits (Anatomical gsmax ). However, the relationship between Anatomical gsmax and operational gs under atmospheric conditions remains undefined. Leaf-level gas-exchange measurements were performed for six Arabidopsis thaliana genotypes that have different Anatomical gsmax profiles resulting from mutations or transgene activity in stomatal development. We found that Anatomical gsmax was an accurate prediction of gs under gas-exchange conditions that maximized stomatal opening, namely high-intensity light, low [CO2 ], and high relative humidity. Plants with different Anatomical gsmax had quantitatively similar responses to increasing [CO2 ] when gs was scaled to Anatomical gsmax . This latter relationship allowed us to produce and test an empirical model derived from the Ball-Woodrow-Berry equation that estimates gs as a function of Anatomical gsmax , relative humidity, and [CO2 ] at the leaf. The capacity to predict operational gs via Anatomical gsmax and the pore-specific short-term response to [CO2 ] demonstrates a precise link between stomatal development and leaf physiology. This connection should be useful to quantify the gas flux of plants in past, present, and future CO2 regimes based upon the anatomical features of stomata.

  View details for DOI 10.1111/nph.12608

  View details for Web of Science ID 000338510200018

• The physiological importance of developmental mechanisms that enforce proper stomatal spacing in Arabidopsis thaliana. The New phytologist Dow, G. J., Berry, J. A., Bergmann, D. C. 2014; 201 (4): 1205-17

  Abstract

  Genetic and cell biological mechanisms that regulate stomatal development are necessary to generate an appropriate number of stomata and enforce a minimum spacing of one epidermal cell between stomata. The ability to manipulate these processes in a model plant system allows us to investigate the physiological importance of stomatal patterning and changes in density, therein testing underlying theories about stomatal biology. Twelve Arabidopsis thaliana genotypes that have varied stomatal characteristics as a result of mutations or transgenes were analyzed in this study. Stomatal traits were used to categorize the genotypes and predict maximum stomatal conductance to water vapor (Anatomical gsmax ) for individuals. Leaf-level gas-exchange measurements determined Diffusive gsmax , net carbon assimilation (A), water-use efficiency (WUE), and stomatal responses to increasing CO2 concentration. Genotypes with proper spacing (< 5% of stomata in clusters) achieved Diffusive gsmax values comparable to Anatomical gsmax across a 10-fold increase in stomatal density, while lines with patterning defects (> 19% clustering) did not. Genotypes with clustering also had reduced A and impaired stomatal responses, while WUE was generally unaffected by patterning. Consequently, optimal function per stoma was dependent on maintaining one epidermal cell spacing and the physiological parameters controlled by stomata were strongly correlated with Anatomical gsmax .

  View details for DOI 10.1111/nph.12586

  View details for PubMedID 24206523

• An integrated model of stomatal development and leaf physiology. The New phytologist Dow, G. J., Bergmann, D. C., Berry, J. A. 2014; 201 (4): 1218-26

  Abstract

  Stomatal conductance (gs ) is constrained by the size and number of stomata on the plant epidermis, and the potential maximum rate of gs can be calculated based on these stomatal traits (Anatomical gsmax ). However, the relationship between Anatomical gsmax and operational gs under atmospheric conditions remains undefined. Leaf-level gas-exchange measurements were performed for six Arabidopsis thaliana genotypes that have different Anatomical gsmax profiles resulting from mutations or transgene activity in stomatal development. We found that Anatomical gsmax was an accurate prediction of gs under gas-exchange conditions that maximized stomatal opening, namely high-intensity light, low [CO2 ], and high relative humidity. Plants with different Anatomical gsmax had quantitatively similar responses to increasing [CO2 ] when gs was scaled to Anatomical gsmax . This latter relationship allowed us to produce and test an empirical model derived from the Ball-Woodrow-Berry equation that estimates gs as a function of Anatomical gsmax , relative humidity, and [CO2 ] at the leaf. The capacity to predict operational gs via Anatomical gsmax and the pore-specific short-term response to [CO2 ] demonstrates a precise link between stomatal development and leaf physiology. This connection should be useful to quantify the gas flux of plants in past, present, and future CO2 regimes based upon the anatomical features of stomata.

  View details for DOI 10.1111/nph.12608

  View details for PubMedID 24251982

• The physiological importance of developmental mechanisms that enforce proper stomatal spacing in Arabidopsis thaliana NEW PHYTOLOGIST Dow, G. J., Berry, J. A., Bergmann, D. C. 2014; 201 (4): 1205-1217

  Abstract

  Genetic and cell biological mechanisms that regulate stomatal development are necessary to generate an appropriate number of stomata and enforce a minimum spacing of one epidermal cell between stomata. The ability to manipulate these processes in a model plant system allows us to investigate the physiological importance of stomatal patterning and changes in density, therein testing underlying theories about stomatal biology. Twelve Arabidopsis thaliana genotypes that have varied stomatal characteristics as a result of mutations or transgenes were analyzed in this study. Stomatal traits were used to categorize the genotypes and predict maximum stomatal conductance to water vapor (Anatomical gsmax ) for individuals. Leaf-level gas-exchange measurements determined Diffusive gsmax , net carbon assimilation (A), water-use efficiency (WUE), and stomatal responses to increasing CO2 concentration. Genotypes with proper spacing (< 5% of stomata in clusters) achieved Diffusive gsmax values comparable to Anatomical gsmax across a 10-fold increase in stomatal density, while lines with patterning defects (> 19% clustering) did not. Genotypes with clustering also had reduced A and impaired stomatal responses, while WUE was generally unaffected by patterning. Consequently, optimal function per stoma was dependent on maintaining one epidermal cell spacing and the physiological parameters controlled by stomata were strongly correlated with Anatomical gsmax .

  View details for DOI 10.1111/nph.12586

  View details for Web of Science ID 000338510200017

• Convergence of stem cell behaviors and genetic regulation between animals and plants: insights from the Arabidopsis thaliana stomatal lineage. F1000prime reports Matos, J. L., Bergmann, D. C. 2014; 6: 53-?

  Abstract

  Plants and animals are two successful, but vastly different, forms of complex multicellular life. In the 1600 million years since they shared a common unicellular ancestor, representatives of these kingdoms have had ample time to devise unique strategies for building and maintaining themselves, yet they have both developed self-renewing stem cell populations. Using the cellular behaviors and the genetic control of stomatal lineage of Arabidopsis as a focal point, we find current data suggests convergence of stem cell regulation at developmental and molecular levels. Comparative studies between evolutionary distant groups, therefore, have the power to reveal the logic behind stem cell behaviors and benefit both human regenerative medicine and plant biomass production.

  View details for DOI 10.12703/P6-53

  View details for PubMedID 25184043

  View details for PubMedCentralID PMC4108953

• A map of cell type-specific auxin responses MOLECULAR SYSTEMS BIOLOGY Bargmann, B. O., Vanneste, S., Krouk, G., Nawy, T., Efroni, I., Shani, E., Choe, G., Friml, J., Bergmann, D. C., Estelle, M., Birnbaum, K. D. 2013; 9

  Abstract

  In plants, changes in local auxin concentrations can trigger a range of developmental processes as distinct tissues respond differently to the same auxin stimulus. However, little is known about how auxin is interpreted by individual cell types. We performed a transcriptomic analysis of responses to auxin within four distinct tissues of the Arabidopsis thaliana root and demonstrate that different cell types show competence for discrete responses. The majority of auxin-responsive genes displayed a spatial bias in their induction or repression. The novel data set was used to examine how auxin influences tissue-specific transcriptional regulation of cell-identity markers. Additionally, the data were used in combination with spatial expression maps of the root to plot a transcriptomic auxin-response gradient across the apical and basal meristem. The readout revealed a strong correlation for thousands of genes between the relative response to auxin and expression along the longitudinal axis of the root. This data set and comparative analysis provide a transcriptome-level spatial breakdown of the response to auxin within an organ where this hormone mediates many aspects of development.

  View details for DOI 10.1038/msb.2013.40

  View details for Web of Science ID 000325297700001

  View details for PubMedID 24022006

  View details for PubMedCentralID PMC3792342

• Mechanisms of stomatal development: an evolutionary view (vol 3, pg 11, 2013) EVODEVO Vaten, A., Bergmann, D. C. 2013; 4

  View details for DOI 10.1186/2041-9139-4-11

  View details for Web of Science ID 000317262400001

  View details for PubMedCentralID PMC3621371

• Stomatal development: a plant's perspective on cell polarity, cell fate transitions and intercellular communication DEVELOPMENT Lau, O. S., Bergmann, D. C. 2012; 139 (20): 3683-3692

  Abstract

  The plant stomatal lineage manifests features common to many developmental contexts: precursor cells are chosen from an initially equivalent field of cells, undergo asymmetric and self-renewing divisions, communicate among themselves and respond to information from a distance. As we review here, the experimental accessibility of these epidermal lineages, particularly in Arabidopsis, has made stomata a conceptual and technical framework for the study of cell fate, stem cells, and cell polarity in plants.

  View details for DOI 10.1242/dev.080523

  View details for Web of Science ID 000308976300003

  View details for PubMedID 22991435

  View details for PubMedCentralID PMC3445305

• Mechanisms of stomatal development: an evolutionary view EVODEVO Vaten, A., Bergmann, D. C. 2012; 3

  Abstract

  Plant development has a significant postembryonic phase that is guided heavily by interactions between the plant and the outside environment. This interplay is particularly evident in the development, pattern and function of stomata, epidermal pores on the aerial surfaces of land plants. Stomata have been found in fossils dating from more than 400 million years ago. Strikingly, the morphology of the individual stomatal complex is largely unchanged, but the sizes, numbers and arrangements of stomata and their surrounding cells have diversified tremendously. In many plants, stomata arise from specialized and transient stem-cell like compartments on the leaf. Studies in the flowering plant Arabidopsis thaliana have established a basic molecular framework for the acquisition of cell fate and generation of cell polarity in these compartments, as well as describing some of the key signals and receptors required to produce stomata in organized patterns and in environmentally optimized numbers. Here we present parallel analyses of stomatal developmental pathways at morphological and molecular levels and describe the innovations made by particular clades of plants.

  View details for DOI 10.1186/2041-9139-3-11

  View details for Web of Science ID 000310696500001

  View details for PubMedID 22691547

  View details for PubMedCentralID PMC3390899

• Brassinosteroid regulates stomatal development by GSK3-mediated inhibition of a MAPK pathway NATURE Kim, T., Michniewicz, M., Bergmann, D. C., Wang, Z. 2012; 482 (7385): 419-U1526

  Abstract

  Plants must coordinate the regulation of biochemistry and anatomy to optimize photosynthesis and water-use efficiency. The formation of stomata, epidermal pores that facilitate gas exchange, is highly coordinated with other aspects of photosynthetic development. The signalling pathways controlling stomata development are not fully understood, although mitogen-activated protein kinase (MAPK) signalling is known to have key roles. Here we demonstrate in Arabidopsis that brassinosteroid regulates stomatal development by activating the MAPK kinase kinase (MAPKKK) YDA (also known as YODA). Genetic analyses indicate that receptor kinase-mediated brassinosteroid signalling inhibits stomatal development through the glycogen synthase kinase 3 (GSK3)-like kinase BIN2, and BIN2 acts upstream of YDA but downstream of the ERECTA family of receptor kinases. Complementary in vitro and in vivo assays show that BIN2 phosphorylates YDA to inhibit YDA phosphorylation of its substrate MKK4, and that activities of downstream MAPKs are reduced in brassinosteroid-deficient mutants but increased by treatment with either brassinosteroid or GSK3-kinase inhibitor. Our results indicate that brassinosteroid inhibits stomatal development by alleviating GSK3-mediated inhibition of this MAPK module, providing two key links; that of a plant MAPKKK to its upstream regulators and of brassinosteroid to a specific developmental output.

  View details for DOI 10.1038/nature10794

  View details for Web of Science ID 000300287100050

  View details for PubMedID 22307275

  View details for PubMedCentralID PMC3292258

• On fate and flexibility in stomatal development. Cold Spring Harbor symposia on quantitative biology Wengier, D. L., Bergmann, D. C. 2012; 77: 53-62

  Abstract

  In plants, the development of the epidermis, and the specialized stomatal lineage within it, exemplifies an old developmental problem that is newly relevant in this current era of stem cell biology: How can a tissue maintain flexibility and change its development midcourse yet still reliably generate differentiated and patterned cells? In this perspective, we endeavor to create a conceptual framework for the widespread questions in development that are raised by observations of stomatal development pathways in "default" settings and in response to environmental challenges. These general issues are related to the molecular pathways and networks recently elucidated for Arabidopsis stomatal development. Finally, the utility of developmental approaches for solving problems of signaling specificity are explored, emphasizing the specific use of the stomatal lineage as an in vivo testing ground for hormone and mitogen-activated protein kinase (MAPK) signaling cascades.

  View details for DOI 10.1101/sqb.2013.77.015883

  View details for PubMedID 23444192

• Generation of spatial patterns through cell polarity switching. Science Robinson, S., Barbier de Reuille, P., Chan, J., Bergmann, D., Prusinkiewicz, P., Coen, E. 2011; 333 (6048): 1436-1440

  Abstract

  The mechanisms that generate dynamic spatial patterns within proliferating tissues are poorly understood, largely because of difficulties in unravelling interactions between cell specification, polarity, asymmetric division, rearrangements, and growth. We address this problem for stomatal spacing in plants, which offer the simplifying advantage that cells do not rearrange. By tracking lineages and gene activities over extended periods, we show that limited stem cell behavior of stomatal precursors depends on maintenance of the SPEECHLESS (SPCH) transcription factor in single daughter cells. Modeling shows how this property can lead to observed stereotypical stomata lineages through a postmitotic polarity-switching mechanism. The model predicts the location of a polarity determinant BASL over multiple divisions, which we validate experimentally. Our results highlight the dynamic two-way interactions between stem cells and their neighborhood during developmental patterning.

  View details for DOI 10.1126/science.1202185

  View details for PubMedID 21903812

  View details for PubMedCentralID PMC3383840

• Generation of Spatial Patterns Through Cell Polarity Switching SCIENCE Robinson, S., de Reuille, P. B., Chan, J., Bergmann, D., Prusinkiewicz, P., Coen, E. 2011; 333 (6048): 1436-1440

  Abstract

  The mechanisms that generate dynamic spatial patterns within proliferating tissues are poorly understood, largely because of difficulties in unravelling interactions between cell specification, polarity, asymmetric division, rearrangements, and growth. We address this problem for stomatal spacing in plants, which offer the simplifying advantage that cells do not rearrange. By tracking lineages and gene activities over extended periods, we show that limited stem cell behavior of stomatal precursors depends on maintenance of the SPEECHLESS (SPCH) transcription factor in single daughter cells. Modeling shows how this property can lead to observed stereotypical stomata lineages through a postmitotic polarity-switching mechanism. The model predicts the location of a polarity determinant BASL over multiple divisions, which we validate experimentally. Our results highlight the dynamic two-way interactions between stem cells and their neighborhood during developmental patterning.

  View details for DOI 10.1126/science.1202185

  View details for Web of Science ID 000294672200040

  View details for PubMedCentralID PMC3383840

• Generation of Signaling Specificity in Arabidopsis by Spatially Restricted Buffering of Ligand-Receptor Interactions PLANT CELL Abrash, E. B., Davies, K. A., Bergmann, D. C. 2011; 23 (8): 2864-2879

  Abstract

  Core signaling pathways function in multiple programs during multicellular development. The mechanisms that compartmentalize pathway function or confer process specificity, however, remain largely unknown. In Arabidopsis thaliana, ERECTA (ER) family receptors have major roles in many growth and cell fate decisions. The ER family acts with receptor TOO MANY MOUTHS (TMM) and several ligands of the EPIDERMAL PATTERNING FACTOR LIKE (EPFL) family, which play distinct yet overlapping roles in patterning of epidermal stomata. Here, our examination of EPFL genes EPFL6/CHALLAH (CHAL), EPFL5/CHALLAH-LIKE1, and EPFL4/CHALLAH-LIKE2 (CLL2) reveals that this family may mediate additional ER-dependent processes. chal cll2 mutants display growth phenotypes characteristic of er mutants, and genetic interactions are consistent with CHAL family molecules acting as ER family ligands. We propose that different classes of EPFL genes regulate different aspects of ER family function and introduce a TMM-based discriminatory mechanism that permits simultaneous, yet compartmentalized and distinct, function of the ER family receptors in growth and epidermal patterning.

  View details for DOI 10.1105/tpc.111.086637

  View details for Web of Science ID 000295254700009

  View details for PubMedID 21862708

  View details for PubMedCentralID PMC3180797

• Peptide Signaling in Plant Development CURRENT BIOLOGY Katsir, L., Davies, K. A., Bergmann, D. C., Laux, T. 2011; 21 (9): R356-R364

  Abstract

  Cell-to-cell communication is integral to the evolution of multicellularity. In plant development, peptide signals relay information coordinating cell proliferation and differentiation. These peptides are often encoded by gene families and bind to corresponding families of receptors. The precise spatiotemporal expression of signals and their cognate receptors underlies developmental patterning, and expressional and biochemical changes over evolutionary time have likely contributed to the refinement and complexity of developmental programs. Here, we discuss two major plant peptide families which have central roles in plant development: the CLAVATA3/ENDOSPERM SURROUNDING REGION (CLE) peptide family and the EPIDERMAL PATTERNING FACTOR (EPF) family. We discuss how specialization has enabled the CLE peptides to modulate stem cell differentiation in various tissue types, and how differing activities of EPF peptides precisely regulate the stomatal developmental program, and we examine the contributions of these peptide families to plant development from an evolutionary perspective.

  View details for DOI 10.1016/j.cub.2011.03.012

  View details for Web of Science ID 000290553800018

  View details for PubMedID 21549958

  View details for PubMedCentralID PMC3139689

• Sequence and function of basic helix-loop-helix proteins required for stomatal development in Arabidopsis are deeply conserved in land plants EVOLUTION & DEVELOPMENT MacAlister, C. A., Bergmann, D. C. 2011; 13 (2): 182-192

  Abstract

  Stomata are a broadly conserved feature of land plants with a crucial role regulating transpiration and gas exchange between the plant and atmosphere. Stereotyped cell divisions within a specialized cell lineage of the epidermis generate stomata and define the pattern of their distribution. The behavior of the stomatal lineage varies in its detail among different plant groups, but general features include asymmetric cell divisions and an immediate precursor (the guard mother cell [GMC]) that divides symmetrically to form the pair of cells that will differentiate into the guard cells. In Arabidopsis, the closely related basic helix-loop-helix (bHLH) subgroup Ia transcription factors SPEECHLESS, MUTE, and FAMA promote asymmetric divisions, the acquisition of GMC identity and guard cell differentiation, respectively. Genome sequence data indicate that these key positive regulators of stomatal development are broadly conserved among land plants. While orthologies can be established among individual family members within the angiosperms, more distantly related groups contain subgroup Ia bHLHs of unclear affinity. We demonstrate group Ia members from the moss Physcomitrella patens can partially complement MUTE and FAMA and recapitulate gain of function phenotypes of group Ia genes in multiple steps in the stomatal lineage in Arabidopsis. Our data are consistent with a mechanism whereby a multifunctional transcription factor underwent duplication followed by specialization to provide the three (now nonoverlapping) functions of the angiosperm stomatal bHLHs.

  View details for DOI 10.1111/j.1525-142X.2011.00468.x

  View details for Web of Science ID 000288502600007

  View details for PubMedID 21410874

  View details for PubMedCentralID PMC3139685

• Differentiation of Arabidopsis Guard Cells: Analysis of the Networks Incorporating the Basic Helix-Loop-Helix Transcription Factor, FAMA PLANT PHYSIOLOGY Hachez, C., Ohashi-Ito, K., Dong, J., Bergmann, D. C. 2011; 155 (3): 1458-1472

  Abstract

  Nearly all extant land plants possess stomata, the epidermal structures that mediate gas exchange between the plant and the environment. The developmental pathways, cell division patterns, and molecules employed in the generation of these structures are simple examples of processes used in many developmental contexts. One specific module is a set of "master regulator" basic helix-loop-helix transcription factors that regulate individual consecutive steps in stomatal development. Here, we profile transcriptional changes in response to inducible expression of Arabidopsis (Arabidopsis thaliana) FAMA, a basic helix-loop-helix protein whose actions during the final stage in stomatal development regulate both cell division and cell fate. Genes identified by microarray and candidate approaches were then further analyzed to test specific hypothesis about the activity of FAMA, the shape of its regulatory network, and to create a new set of stomata-specific or stomata-enriched reporters.

  View details for DOI 10.1104/pp.110.167718

  View details for Web of Science ID 000287843800033

  View details for PubMedID 21245191

  View details for PubMedCentralID PMC3046599

• The secret to life is being different: asymmetric divisions in plant development CURRENT OPINION IN PLANT BIOLOGY Paciorek, T., Bergmann, D. C. 2010; 13 (6): 661-669

  Abstract

  Asymmetric cell divisions (ACDs) are used to create organismal form and cellular diversity during plant development. In several embryonic and postembryonic contexts, genes that specify cell fates and networks that provide positional information have been identified. The cellular mechanisms that translate this information into a physically ACD, however, are still obscure. In this review we examine the cell polarization events that precede asymmetric divisions in plants. Using principles derived from studies of other organisms and from postmitotic polarity generation in plants, we endeavor to provide a framework of what is known, what is on the horizon and what is critically needed to develop a rigorous mechanistic understanding of ACDs in plants.

  View details for DOI 10.1016/j.pbi.2010.09.016

  View details for Web of Science ID 000285663600007

  View details for PubMedID 20970370

• Complex signals for simple cells: the expanding ranks of signals and receptors guiding stomatal development CURRENT OPINION IN PLANT BIOLOGY Rowe, M. H., Bergmann, D. C. 2010; 13 (5): 548-555

  Abstract

  In development, pattern formation requires that cell proliferation and differentiation be precisely coordinated. Stomatal development has served as a useful model system for understanding how this is accomplished in plants. Although it has been known for some time that stomatal development is regulated by a family of receptor-like kinases (RLKs) and an accompanying receptor-like protein (RLP), only recently have putative ligands been identified. Despite the structural homology demonstrated by the genes that encode these small, secreted peptides, they convey different information, vary with one another in their relationship to common signaling components, control distinct aspects of stomatal development, and do so antagonistically. Their discovery has revealed the intricate network of interactions required upstream of RLK signal transduction for the patterning of complex tissues. However, at issue still is whether specific ligand-receptor combinations are responsible for the activation of discrete signaling pathways or spatiotemporal modulation of a common pathway. This review integrates the latest findings regarding RLK-mediated signaling in stomatal development with emerging paradigms in the field.

  View details for DOI 10.1016/j.pbi.2010.06.002

  View details for Web of Science ID 000284658400011

  View details for PubMedID 20638894

  View details for PubMedCentralID PMC2967594

• Asymmetry, fate and self-renewal in stomatal development Bergmann, D. C. ACADEMIC PRESS INC ELSEVIER SCIENCE. 2010: 426

  View details for DOI 10.1016/j.ydbio.2010.05.071

  View details for Web of Science ID 000280426400075

• MSP Domain-Containing Protein Reveals A New Level of Regulation of Stomatal Signaling in Arabidopsis Paciorek, T., Abrash, E., Bergmann, D. SPRINGER. 2010: S149–S150

  View details for Web of Science ID 000285367500334

• From molecule to model, from environment to evolution: an integrated view of growth and development CURRENT OPINION IN PLANT BIOLOGY Bergmann, D. C., Fleming, A. J. 2010; 13 (1): 1-4

  View details for DOI 10.1016/j.pbi.2009.12.001

  View details for Web of Science ID 000275095200001

  View details for PubMedID 20047852

• Regional specification of stomatal production by the putative ligand CHALLAH DEVELOPMENT Abrash, E. B., Bergmann, D. C. 2010; 137 (3): 447-455

  Abstract

  The problem of modulating cell fate programs to create distinct patterns and distributions of specialized cell types in different tissues is common to complex multicellular organisms. Here, we describe the previously uncharacterized CHALLAH (CHAL) gene, which acts as a tissue-specific regulator of epidermal pattern in Arabidopsis thaliana. Arabidopsis plants produce stomata, the cellular valves required for gas exchange, in virtually all aerial organs, but stomatal density and distribution differ among organs and along organ axes. Such regional regulation is particularly evident in plants mutant for the putative receptor TOO MANY MOUTHS (TMM), which produce excess stomata in leaves but no stomata in stems. Mutations in CHAL suppress tmm phenotypes in a tissue-specific manner, restoring stomatal production in stems while minimally affecting leaves. CHAL is similar in sequence to the putative stomatal ligands EPF1 and EPF2 and, like the EPFs, can reduce or eliminate stomatal production when overexpressed. However, CHAL and the EPFs have different relationships to TMM and the ERECTA (ER) family receptors. We propose a model in which CHAL and the EPFs both act through ER family receptors to repress stomatal production, but are subject to opposite regulation by TMM. The existence of two such ligand classes provides an explanation for TMM dual functionality and tissue-specific phenotypes.

  View details for DOI 10.1242/dev.040931

  View details for Web of Science ID 000273691600010

  View details for PubMedID 20056678

• STOMATAL PATTERNING AND DEVELOPMENT PLANT DEVELOPMENT Dong, J., Bergmann, D. C. 2010; 91: 267-297

  Abstract

  Stomata are epidermal pores used for water and gas exchange between a plant and the atmosphere. Both the entry of carbon dioxide for photosynthesis and the evaporation of water that drives transpiration and temperature regulation are modulated by the activities of stomata. Each stomatal pore is surrounded by two highly specialized cells called guard cells (GCs), and may also be associated with neighboring subsidiary cells; this entire unit is referred to as the stomatal complex. Generation of GCs requires stereotyped asymmetric and symmetric cell divisions, and the pattern of stomatal complexes in the epidermis follows a "one-cell-spacing rule" (one complex almost never touches another one). Both stomatal formation and patterning are highly regulated by a number of genetic components identified in the last decade, including, but not limited to, secreted peptide ligands, plasma membrane receptors and receptor-like kinases, a MAP kinase module, and a series of transcription factors. This review will elaborate on the current state of knowledge about components in signaling pathways required for cell fate and pattern, with emphasis on (1) a family of extracellular peptide ligands and their relationship to the TOO MANY MOUTHS receptor-like protein and/or members of the ERECTA receptor-like kinase family, (2) three tiers of a MAP kinase module and the kinases that confer novel regulatory effects in specific stomatal cell types, and (3) transcription factors that generate specific stomatal cell types and the regulatory mechanisms for modulating their activities. We will then consider two new proteins (BASL and PAN1, from Arabidopsis and maize, respectively) that regulate stomatal asymmetric divisions by establishing cell polarity.

  View details for DOI 10.1016/S0070-2153(10)91009-0

  View details for Web of Science ID 000281449100009

  View details for PubMedID 20705185

• Plant asymmetric cell division regulators: pinch-hitting for PARs? F1000 biology reports Metzinger, C. A., Bergmann, D. C. 2010; 2

  Abstract

  Like animals, plants use asymmetric cell divisions to create pattern and diversity. Due to a rigid cell wall and lack of cell migrations, these asymmetric divisions incur the additional constraints of being locked into their initial orientations. How do plants specify and carry out asymmetric divisions? Intercellular communication has been suspected for some time and recent developments identify these signals as well as point to segregated determinants and proteins with PAR-like functions as parts of the answer.

  View details for DOI 10.3410/B2-25

  View details for PubMedID 20948808

  View details for PubMedCentralID PMC2948360

• Novel and Expanded Roles for MAPK Signaling in Arabidopsis Stomatal Cell Fate Revealed by Cell Type-Specific Manipulations PLANT CELL Lampard, G. R., Lukowitz, W., Ellis, B. E., Bergmann, D. C. 2009; 21 (11): 3506-3517

  Abstract

  Mitogen-activated protein kinase (MAPK) signaling networks regulate numerous eukaryotic biological processes. In Arabidopsis thaliana, signaling networks that contain MAPK kinases MKK4/5 and MAPKs MPK3/6 function in abiotic and biotic stress responses and regulate embryonic and stomatal development. However, how single MAPK modules direct specific output signals without cross-activating additional downstream processes is largely unknown. Studying relationships between MAPK components and downstream signaling outcomes is difficult because broad experimental manipulation of these networks is often lethal or associated with multiple phenotypes. Stomatal development in Arabidopsis follows a series of discrete, stereotyped divisions and cell state transitions. By expressing a panel of constitutively active MAPK kinase (MAPKK) variants in discrete stomatal lineage cell types, we identified a new inhibitory function of MKK4 and MKK5 in meristemoid self-renewal divisions. Furthermore, we established roles for MKK7 and MKK9 as both negative and (unexpectedly) positive regulators during the major stages of stomatal development. This has expanded the number of known MAPKKs that regulate stomatal development and allowed us to build plausible and testable subnetworks of signals. This in vivo cell type-specific assay can be adapted to study other protein families and thus may reveal insights into other complex signal transduction pathways in plants.

  View details for DOI 10.1105/tpc.109.070110

  View details for Web of Science ID 000273235600011

  View details for PubMedID 19897669

  View details for PubMedCentralID PMC2798322

• Pattern and polarity in the plant epidermis Bergmann, D., Dong, J., Lampard, G., Paciorek, M., MacAlister, C. ACADEMIC PRESS INC ELSEVIER SCIENCE. 2009: 397

  View details for DOI 10.1016/j.ydbio.2009.05.048

  View details for Web of Science ID 000267777900061

• Orthologs of Arabidopsis thaliana stomatal bHLH genes and regulation of stomatal development in grasses DEVELOPMENT Liu, T., Ohashi-Ito, K., Bergmann, D. C. 2009; 136 (13): 2265-2276

  Abstract

  Stomata are adjustable pores in the plant epidermis that regulate gas exchange between the plant and atmosphere; they are present on the aerial portions of most higher plants. Genetic pathways controlling stomatal development and distribution have been described in some detail for one dicot species, Arabidopsis, in which three paralogous bHLH transcription factors, FAMA, MUTE and SPCH, control discrete sequential stages in stomatal development. Orthologs of FAMA, MUTE and SPCH are present in other flowering plants. This observation is of particular interest when considering the grasses, because both the morphology of guard cells and their tissue distributions differ substantially between Arabidopsis and this group. By examining gene expression patterns, insertional mutants and cross-species complementation studies, we find evidence that FAMA function is conserved between monocots and dicots, despite their different stomatal morphologies, whereas the roles of MUTE and two SPCH paralogs are somewhat divergent.

  View details for DOI 10.1242/dev.032938

  View details for Web of Science ID 000266731800013

  View details for PubMedID 19502487

• BASL Controls Asymmetric Cell Division in Arabidopsis CELL Dong, J., MacAlister, C. A., Bergmann, D. C. 2009; 137 (7): 1320-1330

  Abstract

  Development in multicellular organisms requires the organized generation of differences. A universal mechanism for creating such differences is asymmetric cell division. In plants, as in animals, asymmetric divisions are correlated with the production of cellular diversity and pattern; however, structural constraints imposed by plant cell walls and the absence of homologs of known animal or fungal cell polarity regulators necessitates that plants utilize new molecules and mechanisms to create asymmetries. Here, we identify BASL, a novel regulator of asymmetric divisions in Arabidopsis. In asymmetrically dividing stomatal-lineage cells, BASL accumulates in a polarized crescent at the cell periphery before division, and then localizes differentially to the nucleus and a peripheral crescent in self-renewing cells and their sisters after division. BASL presence at the cell periphery is critical for its function, and we propose that BASL represents a plant-specific solution to the challenge of asymmetric cell division.

  View details for DOI 10.1016/j.cell.2009.04.018

  View details for Web of Science ID 000267373400024

  View details for PubMedID 19523675

• Asymmetric Cell Divisions: A View from Plant Development DEVELOPMENTAL CELL Abrash, E. B., Bergmann, D. C. 2009; 16 (6): 783-796

  Abstract

  All complex multicellular organisms must solve the problem of generating diverse and appropriately patterned cell types. Asymmetric division, in which a single mother cell gives rise to daughters with distinct identities, is instrumental in the generation of cellular diversity and higher-level patterns. In animal systems, there exists considerable evidence for conserved mechanisms of polarization and asymmetric division. Here, we consider asymmetric cell divisions in plants, highlighting the unique aspects of plant cell biology and organismal development that constrain the process, but also emphasizing conceptual and mechanistic similarities with animal asymmetric divisions.

  View details for DOI 10.1016/j.devcel.2009.05.014

  View details for Web of Science ID 000267203700006

  View details for PubMedID 19531350

• Asymmetry and pattern in the leaf epidermis Annual Meeting of the Society-for-Experimental-Biology Bergmann, D., Dong, J., Lampard, G., MacAlister, C., Hachez, C., Rowe, M., Metzinger, C. ELSEVIER SCIENCE INC. 2009: S176–S176

  View details for DOI 10.1016/j.cbpa.2009.04.373

  View details for Web of Science ID 000267520700408

• Arabidopsis Stomatal Initiation Is Controlled by MAPK-Mediated Regulation of the bHLH SPEECHLESS SCIENCE Lampard, G. R., MacAlister, C. A., Bergmann, D. C. 2008; 322 (5904): 1113-1116

  Abstract

  Stomata, epidermal structures that modulate gas exchange between plants and the atmosphere, play critical roles in primary productivity and the global climate. Positively acting transcription factors and negatively acting mitogen-activated protein kinase (MAPK) signaling control stomatal development in Arabidopsis; however, it is not known how the opposing activities of these regulators are integrated. We found that a unique domain in a basic helix-loop-helix (bHLH) stomatal initiating factor, SPEECHLESS, renders it a MAPK phosphorylation target in vitro and modulates its function in vivo. MAPK cascades modulate a diverse set of activities including development, cell proliferation, and response to external stresses. The coupling of MAPK signaling to SPEECHLESS activity provides cell type specificity for MAPK output while allowing the integration of multiple developmental and environmental signals into the production and spacing of stomata.

  View details for DOI 10.1126/science.1162263

  View details for Web of Science ID 000260867700041

  View details for PubMedID 19008449

• 2020 vision for biology: The role of plants in addressing grand challenges in biology MOLECULAR PLANT Raikhel, N. 2008; 1 (4): 561-563

  View details for DOI 10.1093/mp/ssn040

  View details for Web of Science ID 000259104300001

  View details for PubMedID 19825561

• Regulation of the Arabidopsis root vascular initial population by LONESOME HIGHWAY DEVELOPMENT Ohashi-Ito, K., Bergmann, D. C. 2007; 134 (16): 2959-2968

  Abstract

  Complex organisms consist of a multitude of cell types arranged in a precise spatial relation to each other. Arabidopsis roots generally exhibit radial tissue organization; however, within a tissue layer, cells are not identical. Specific vascular cell types are arranged in diametrically opposed longitudinal files that maximize the distance between them and create a bilaterally symmetric (diarch) root. Mutations in the LONESOME HIGHWAY (LHW) gene eliminate bilateral symmetry and reduce the number of cells in the center of the root, resulting in roots with only single xylem and phloem poles. LHW does not appear to be required for the creation of any specific cell type, but coordinately controls the number of all vascular cell types by regulating the size of the pool of cells from which they arise. We cloned LHW and found that it encodes a protein with weak sequence similarity to basic helix-loop-helix (bHLH)-domain proteins. LHW is a transcriptional activator in vitro. In plants, LHW is nuclear-localized and is expressed in the root meristems, where we hypothesize it acts independently of other known root-patterning genes to promote the production of stele cells, but might also indirectly feed into established regulatory networks for the maintenance of the root meristem.

  View details for DOI 10.1242/dev.006296

  View details for Web of Science ID 000248385000008

  View details for PubMedID 17626058

  View details for PubMedCentralID PMC3145339

• The secretory peptide gene EPF1 enforces the stomatal one-cell-spacing rule GENES & DEVELOPMENT Hara, K., Kajita, R., Torii, K. U., Bergmann, D. C., Kakimoto, T. 2007; 21 (14): 1720-1725

  Abstract

  Stomata are innovations of land plants that allow regulated gas exchange. Stomatal precursor cells are produced by asymmetric cell division, and once formed, signal their neighbors to inhibit the formation of stomatal precursors in direct contact. We report a gene of Arabidopsis thaliana, EPIDERMAL PATTERNING FACTOR 1 (EPF1) that encodes a small secretory peptide expressed in stomatal cells and precursors and that controls stomatal patterning through regulation of asymmetric cell division. EPF1 activity is dependent on the TOO MANY MOUTHS receptor-like protein and ERECTA family receptor kinases, suggesting that EPF1 may provide a positional cue interpreted by these receptors.

  View details for DOI 10.1101/gad.1550707

  View details for Web of Science ID 000248078600004

  View details for PubMedID 17639078

  View details for PubMedCentralID PMC1920166

• Transcription factor control of asymmetric cell divisions that establish the stomatal lineage NATURE MacAlister, C. A., Ohashi-Ito, K., Bergmann, D. C. 2007; 445 (7127): 537-540

  Abstract

  The establishment of new cell lineages during development often requires a symmetry-breaking event. An asymmetric division in the epidermis of plants initiates a lineage that ultimately produces stomatal guard cells. Stomata are pores in the epidermis that serve as the main conduits for gas exchange between plants and the atmosphere; they are critical for photosynthesis and exert a major influence on global carbon and water cycles. Recent studies implicated intercellular signalling in preventing the inappropriate production of stomatal complexes. Genes required to make stomata, however, remained elusive. Here we report the identification of a gene, SPEECHLESS (SPCH), encoding a basic helix-loop-helix (bHLH) transcription factor that is necessary and sufficient for the asymmetric divisions that establish the stomatal lineage in Arabidopsis thaliana. We demonstrate that SPCH and two paralogues are successively required for the initiation, proliferation and terminal differentiation of cells in the stomatal lineage. The stomatal bHLHs define a molecular pathway sufficient to create one of the key cell types in plants. Similar molecules and regulatory mechanisms are used during muscle and neural development, highlighting a conserved use of closely related bHLHs for cell fate specification and differentiation.

  View details for DOI 10.1038/nature05491

  View details for Web of Science ID 000243867300043

  View details for PubMedID 17183265

• Stomatal development ANNUAL REVIEW OF PLANT BIOLOGY Bergmann, D. C., Sack, F. D. 2007; 58: 163-181

  Abstract

  Stomata are cellular epidermal valves in plants central to gas exchange and biosphere productivity. The pathways controlling their formation are best understood for Arabidopsis thaliana where stomata are produced through a series of divisions in a dispersed stem cell compartment. The stomatal pathway is an accessible system for analyzing core developmental processes including position-dependent patterning via intercellular signaling and the regulation of the balance between proliferation and cell specification. This review synthesizes what is known about the mechanisms and genes underlying stomatal development. We contrast the functions of genes that act earlier in the pathway, including receptors, kinases, and proteases, with those that act later in the cell lineage. In addition, we discuss the relationships between environmental signals, stomatal development genes, and the capacity for controlling shoot gas exchange.

  View details for DOI 10.1146/annurev.arplant.58.032806.104023

  View details for Web of Science ID 000247703600009

  View details for PubMedID 17201685

• Arabidopsis FAMA controls the final proliferation/differentiation switch during stomatal development PLANT CELL Ohashi-Ito, K., Bergmann, D. C. 2006; 18 (10): 2493-2505

  Abstract

  Coordination between cell proliferation and differentiation is essential to create organized and functional tissues. Arabidopsis thaliana stomata are created through a stereotyped series of symmetric and asymmetric cell divisions whose frequency and orientation are informed by cell-cell interactions. Receptor-like proteins and a mitogen-activated protein kinase kinase kinase were previously identified as negative regulators of stomatal development; here, we present the characterization of a bona fide positive regulator. FAMA is a putative basic helix-loop-helix transcription factor whose activity is required to promote differentiation of stomatal guard cells and to halt proliferative divisions in their immediate precursors. Ectopic FAMA expression is also sufficient to confer stomatal character. Physical and genetic interaction studies combined with functional characterization of FAMA domains suggest that stomatal development relies on regulatory complexes distinct from those used to specify other plant epidermal cells. FAMA behavior provides insights into the control of differentiation in cells produced through the activity of self-renewing populations.

  View details for DOI 10.1105/tpc.106.046136

  View details for Web of Science ID 000241818300008

  View details for PubMedID 17088607

  View details for PubMedCentralID PMC1626605

• Stomatal development: from neighborly to global communication CURRENT OPINION IN PLANT BIOLOGY Bergmann, D. 2006; 9 (5): 478-483

  Abstract

  Stomata are epidermal structures that are responsible for modulating the exchange of gases between the plant and the environment. Stomata are formed and patterned by asymmetric cell divisions. The number and orientation of these asymmetric divisions is informed by plant intrinsic signals acting locally (among epidermal cells) or at a distance (from mature to young leaves) and by plant extrinsic factors such as the quantity of light, water and CO(2) in the atmosphere. Recent studies have implicated a set of conserved cell surface receptors and intracellular signaling molecules in the perception and response to developmental cues. Complementary studies have probed the nature of environmental signals and how these signals are transduced from the site of perception to the cells in the stomatal lineage.

  View details for DOI 10.1016/j.pbi.2006.07.001

  View details for Web of Science ID 000240795900006

  View details for PubMedID 16890476

• Stomatal development and pattern controlled by a MAPKK kinase SCIENCE Bergmann, D. C., Lukowitz, W., Somerville, C. R. 2004; 304 (5676): 1494-1497

  Abstract

  Stomata are epidermal structures that modulate gas exchange between a plant and its environment. During development, stomata are specified and positioned nonrandomly by the integration of asymmetric cell divisions and intercellular signaling. The Arabidopsis mitogen-activated protein kinase kinase kinase gene, YODA, acts as part of a molecular switch controlling cell identities in the epidermis. Null mutations in YODA lead to excess stomata, whereas constitutive activation of YODA eliminated stomata. Transcriptome analysis of seedlings with altered YODA activity was used to identify potential stomatal regulatory genes. A putative transcription factor from this set was shown to regulate the developmental behavior of stomatal precursors.

  View details for Web of Science ID 000221795800042

  View details for PubMedID 15178800

• Integrating signals in stomatal development CURRENT OPINION IN PLANT BIOLOGY Bergmann, D. C. 2004; 7 (1): 26-32

  Abstract

  Stomata are specialized epidermal structures that control the exchange of water and carbon dioxide between the plant and the atmosphere. The classical developmental mechanisms that define cell fate and tissue patterning - cell lineage, cell-cell interactions and signals from a distance - are employed to make stomata and to define their density and distribution within the epidermis. Recent work has shown that two genes that are involved in stomatal pattern may encode components of a classical cell-surface-receptor-mediated signaling cascade. Additional work has suggested that signals from the overlying cuticle and the underlying mesophyll also influence stomatal pattern. These findings highlight the need for models that explain how the signals that regulate stomatal development are integrated and how they act to regulate cell polarity, the cell cycle and, ultimately, cell fate.

  View details for DOI 10.1016/j.pbi.2003.10.001

  View details for Web of Science ID 000189283200005

  View details for PubMedID 14732438

• Asymmetric divisions and cell signaling during epidermal cell specification in Arabidopsis. Bergmann, D., Lukowitz, W., Somerville, C. ACADEMIC PRESS INC ELSEVIER SCIENCE. 2003: 523

  View details for Web of Science ID 000184373300329

• Completion of cytokinesis in C-elegans requires a brefeldin A-sensitive membrane accumulation at the cleavage furrow apex CURRENT BIOLOGY Skop, A. R., Bergmann, D., Mohler, W. A., White, J. G. 2001; 11 (10): 735-746

  Abstract

  The terminal phase of cytokinesis in eukaryotic cells involves breakage of the intercellular canal containing the spindle midzone and resealing of the daughter cells. Recent observations suggest that the spindle midzone is required for this process. In this study, we investigated the possibility that targeted secretion in the vicinity of the spindle midzone is required for the execution of the terminal phase of cytokinesis.We inhibited secretion in early C. elegans embryos by treatment with brefeldin A (BFA). Using 4D recordings of dividing cells, we showed that BFA induced stereotyped failures in the terminal phase of cytokinesis; although the furrow ingressed normally, after a few minutes the furrow completely regressed, even though spindle midzone and midbody microtubules appeared normal. In addition, using an FM1-43 membrane probe, we found that membrane accumulated locally at the apices of the late cleavage furrows that form the persisting intercellular canals between daughter cells. However, in BFA-treated embryos this membrane accumulation did not occur, which possibly accounts for the observed cleavage failures.We have shown that BFA disrupts the terminal phase of cytokinesis in the embryonic blastomeres of C. elegans. We observed that membrane accumulates at the apices of the late cleavage furrow by means of a BFA-sensitive mechanism. We suggest that this local membrane accumulation is necessary for the completion of cytokinesis and speculate that the spindle midzone region of animal cells is functionally equivalent to the phragmoplast of plants and acts to target secretion to the equatorial plane of a cleaving cell.

  View details for DOI 10.1016/S0960-9822(01)00231-7

  View details for Web of Science ID 000168765100015

  View details for PubMedID 11378383

  View details for PubMedCentralID PMC3733387

• Maternal effect of low temperature on handedness determination in C-elegans embryos DEVELOPMENTAL GENETICS Wood, W. B., Bergmann, D., Florance, A. 1996; 19 (3): 222-230

  Abstract

  C. elegans embryos, larvae, and adults exhibit several left-right asymmetries with an invariant dextral handedness, which first becomes evident in the embryo at the 6-cell stage. Reversed (sinistral) handedness was not observed among > 10,000 N2 adults reared at 16 degrees C or 20 degrees C under standard conditions. However, among the progeny of adults reproducing at 10 degrees C, the frequency of animals with sinistral handedness was increased to approximately 0.5%. Cold pulse experiments indicated that the critical period for this increase was in early oogenesis, several hours before the first appearance of left-right asymmetry in the embryo. Hermaphrodites reared at 10 degrees C and mated with males reared at 20 degrees C produced sinistral outcross as well as sinistral self-progeny, indicating that the low temperature effect on oocytes was sufficient to cause reversals. Increased frequency of reversal was also observed among animals developed from embryos lacking the egg shell. Possible mechanisms for the control of embryonic handedness are discussed in the context of these results, including the hypothesis that handedness could be dictated by the chirality of a gametic component.

  View details for DOI 10.1002/(SICI)1520-6408(1996)19:3<222::AID-DVG5>3.0.CO;2-B

  View details for Web of Science ID A1996VV86200005

  View details for PubMedID 8952064