Associate Member, Institute for Stem Cell Biology and Regenerative Medicine, Stanford School of Medicine (2011 - Present)
Adjunct Staff Member, Carnegie Institution for Science, Dept. of Plant Biology (2011 - Present)
PhD, University of Colorado, Boulder, Molecular Biology (2000)
Postdoctoral, Carnegie Institution, Plant Development
Current Research and Scholarly Interests
Generating the full complement of functional cell types requires coordinating the production of cells with the specification programs that distinguish one cell type from another. Asymmetric cell division, in which one cell divides to create daughter cells that differ in size, location, cellular components or fate, is extensively used in the development of animals. In development of the epidermis in the model plant Arabidopsis thaliana, the specification and distribution of stomatal guard cells also requires oriented cell divisions. By studying stomatal development, one can explore how cells choose to initiate asymmetric divisions, how cells establish an internal polarity that can be translated into an asymmetric cell division, and how cells interpret external cues to align their divisions relative to the polarity of the whole tissue. Moreover, approaching these questions in a plant system is likely to reveal new solutions to the problem of balancing the robust specification of cell types with the ability to change development in the face of injury or environmental change.
- Genetics, Biochemistry, and Molecular Biology
BIO 41 (Aut)
Independent Studies (7)
- Advanced Research Laboratory in Experimental Biology
BIO 199 (Aut, Win, Spr, Sum)
- Directed Reading in Biology
BIO 198 (Aut, Win, Spr, Sum)
- Graduate Research
BIO 300 (Aut, Win, Spr, Sum)
- Out-of-Department Advanced Research Laboratory in Experimental Biology
BIO 199X (Aut, Win, Spr, Sum)
- Out-of-Department Directed Reading
BIO 198X (Aut, Win, Spr, Sum)
- Out-of-Department Graduate Research
BIO 300X (Win, Spr, Sum)
- Teaching of Biology
BIO 290 (Aut, Win, Spr)
- Advanced Research Laboratory in Experimental Biology
- Prior Year Courses
Postdoctoral Faculty Sponsor
Martin Bringmann, Andrea Mair, Michael Raissig, Anne Vaten, Annika Weimer
Yang Bi, Therese LaRue, Abigail Simmons
Doctoral Dissertation Reader (AC)
Jae Chung, Miranda Stratton
Doctoral Dissertation Co-Advisor (AC)
Yang Bi, Therese LaRue
Doctoral Dissertation Advisor (AC)
Graduate and Fellowship Programs
Biology (School of Humanities and Sciences) (Phd Program)
Transcriptome Dynamics of the Stomatal Lineage: Birth, Amplification, and Termination of a Self-Renewing Population
2015; 33 (1): 107-118
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 Web of Science ID 000352454200011
View details for PubMedID 25850675
- Irreversible fate commitment in the Arabidopsis stomatal lineage requires a FAMA and RETINOBLASTOMA-RELATED module ELIFE 2014; 3
Fine-scale dissection of the subdomains of polarity protein BASL in stomatal asymmetric cell division.
Journal of experimental botany
2016; 67 (17): 5093-5103
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
Modulators of Stomatal Lineage Signal Transduction Alter Membrane Contact Sites and Reveal Specialization among ERECTA Kinases.
2016; 38 (4): 345-357
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
2016; 113 (29): 8326-8331
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
Arabidopsis CSLD5 Functions in Cell Plate Formation in a Cell Cycle-Dependent Manner.
2016; 28 (7): 1722-1737
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
50 years of Arabidopsis research: highlights and future directions
2016; 209 (3): 921-944
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
2016; 29: 1-8
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 Web of Science ID 000370895100002
View details for PubMedID 26550955
Arabidopsis Reduces Growth Under Osmotic Stress by Decreasing SPEECHLESS Protein
PLANT AND CELL PHYSIOLOGY
2014; 55 (12): 2037-2046
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 Web of Science ID 000348612000002
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 2014; 111 (43): 15585-15590
- Patterning and processes: how stomatal development defines physiological potential CURRENT OPINION IN PLANT BIOLOGY 2014; 21: 67-74
Patterning and processes: how stomatal development defines physiological potential.
Current opinion in plant biology
2014; 21: 67-74
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 2014; 345 (6204): 1605-1609
- Coordinating cell polarity: heading in the right direction? DEVELOPMENT 2014; 141 (17): 3298-3302
Manipulation of Mitogen-Activated Protein Kinase Kinase Signaling in the Arabidopsis Stomatal Lineage Reveals Motifs That Contribute to Protein Localization and Signaling Specificity
2014; 26 (8): 3358-3371
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 2014; 113 (7): 1083-1105
An integrated model of stomatal development and leaf physiology
2014; 201 (4): 1218-1226
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
View details for PubMedID 24251982
The physiological importance of developmental mechanisms that enforce proper stomatal spacing in Arabidopsis thaliana
2014; 201 (4): 1205-1217
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
View details for PubMedID 24206523
Convergence of stem cell behaviors and genetic regulation between animals and plants: insights from the Arabidopsis thaliana stomatal lineage.
2014; 6: 53-?
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
A map of cell type-specific auxin responses
MOLECULAR SYSTEMS BIOLOGY
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
On Fate and Flexibility in Stomatal Development.
Cold Spring Harbor symposia on quantitative biology
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 PubMedID 23444192
Stomatal development: a plant's perspective on cell polarity, cell fate transitions and intercellular communication
2012; 139 (20): 3683-3692
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
Mechanisms of stomatal development: an evolutionary view
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
Brassinosteroid regulates stomatal development by GSK3-mediated inhibition of a MAPK pathway
2012; 482 (7385): 419-U1526
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
Generation of Spatial Patterns Through Cell Polarity Switching
2011; 333 (6048): 1436-1440
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
Generation of Signaling Specificity in Arabidopsis by Spatially Restricted Buffering of Ligand-Receptor Interactions
2011; 23 (8): 2864-2879
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
Peptide Signaling in Plant Development
2011; 21 (9): R356-R364
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
Sequence and function of basic helix-loop-helix proteins required for stomatal development in Arabidopsis are deeply conserved in land plants
EVOLUTION & DEVELOPMENT
2011; 13 (2): 182-192
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
Differentiation of Arabidopsis Guard Cells: Analysis of the Networks Incorporating the Basic Helix-Loop-Helix Transcription Factor, FAMA
2011; 155 (3): 1458-1472
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
The secret to life is being different: asymmetric divisions in plant development
CURRENT OPINION IN PLANT BIOLOGY
2010; 13 (6): 661-669
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
2010; 13 (5): 548-555
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
- From molecule to model, from environment to evolution: an integrated view of growth and development CURRENT OPINION IN PLANT BIOLOGY 2010; 13 (1): 1-4
Regional specification of stomatal production by the putative ligand CHALLAH
2010; 137 (3): 447-455
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
2010; 91: 267-297
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
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
Novel and Expanded Roles for MAPK Signaling in Arabidopsis Stomatal Cell Fate Revealed by Cell Type-Specific Manipulations
2009; 21 (11): 3506-3517
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
Orthologs of Arabidopsis thaliana stomatal bHLH genes and regulation of stomatal development in grasses
2009; 136 (13): 2265-2276
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
2009; 137 (7): 1320-1330
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
2009; 16 (6): 783-796
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
Arabidopsis Stomatal Initiation Is Controlled by MAPK-Mediated Regulation of the bHLH SPEECHLESS
2008; 322 (5904): 1113-1116
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
Regulation of the Arabidopsis root vascular initial population by LONESOME HIGHWAY
2007; 134 (16): 2959-2968
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
The secretory peptide gene EPF1 enforces the stomatal one-cell-spacing rule
GENES & DEVELOPMENT
2007; 21 (14): 1720-1725
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
Transcription factor control of asymmetric cell divisions that establish the stomatal lineage
2007; 445 (7127): 537-540
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
ANNUAL REVIEW OF PLANT BIOLOGY
2007; 58: 163-181
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
2006; 18 (10): 2493-2505
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
Stomatal development: from neighborly to global communication
CURRENT OPINION IN PLANT BIOLOGY
2006; 9 (5): 478-483
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
2004; 304 (5676): 1494-1497
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
2004; 7 (1): 26-32
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