José R. Dinneny

All Publications

• Multi-omics analysis of green lineage osmotic stress pathways unveils crucial roles of different cellular compartments. Nature communications Vilarrasa-Blasi, J., Vellosillo, T., Jinkerson, R. E., Fauser, F., Xiang, T., Minkoff, B. B., Wang, L., Kniazev, K., Guzman, M., Osaki, J., Barrett-Wilt, G. A., Sussman, M. R., Jonikas, M. C., Dinneny, J. R. 2024; 15 (1): 5988

  Abstract

  Maintenance of water homeostasis is a fundamental cellular process required by all living organisms. Here, we use the single-celled green alga Chlamydomonas reinhardtii to establish a foundational understanding of osmotic-stress signaling pathways through transcriptomics, phosphoproteomics, and functional genomics approaches. Comparison of pathways identified through these analyses with yeast and Arabidopsis allows us to infer their evolutionary conservation and divergence across these lineages. 76 genes, acting across diverse cellular compartments, were found to be important for osmotic-stress tolerance in Chlamydomonas through their functions in cytoskeletal organization, potassium transport, vesicle trafficking, mitogen-activated protein kinase and chloroplast signaling. We show that homologs for five of these genes have conserved functions in stress tolerance in Arabidopsis and reveal a novel PROFILIN-dependent stage of acclimation affecting the actin cytoskeleton that ensures tissue integrity upon osmotic stress. This study highlights the conservation of the stress response in algae and land plants, and establishes Chlamydomonas as a unicellular plant model system to dissect the osmotic stress signaling pathway.

  View details for DOI 10.1038/s41467-024-49844-3

  View details for PubMedID 39013881

  View details for PubMedCentralID 120784

• Choreographing root architecture and rhizosphere interactions through synthetic biology. Nature communications Ragland, C. J., Shih, K. Y., Dinneny, J. R. 2024; 15 (1): 1370

  Abstract

  Climate change is driving extreme changes to the environment, posing substantial threats to global food security and bioenergy. Given the direct role of plant roots in mediating plant-environment interactions, engineering the form and function of root systems and their associated microbiota may mitigate these effects. Synthetic genetic circuits have enabled sophisticated control of gene expression in microbial systems for years and a surge of advances has heralded the extension of this approach to multicellular plant species. Targeting these tools to affect root structure, exudation, and microbe activity on root surfaces provide multiple strategies for the advancement of climate-ready crops.

  View details for DOI 10.1038/s41467-024-45272-5

  View details for PubMedID 38355570

  View details for PubMedCentralID PMC10866969

• Philip N. Benfey (1953-2023). Developmental cell Bennett, M. J., Brady, S. M., Dinneny, J. R., Helariutta, Y., Sozzani, R. 2023; 58 (22): 2413-2415

  View details for DOI 10.1016/j.devcel.2023.10.013

  View details for PubMedID 37989080

• PlantACT! - how to tackle the climate crisis. Trends in plant science Hirt, H., Al-Babili, S., Almeida-Trapp, M., Martin, A., Aranda, M., Bartels, D., Bennett, M., Blilou, I., Boer, D., Boulouis, A., Bowler, C., Brunel-Muguet, S., Chardon, F., Colcombet, J., Colot, V., Daszkowska-Golec, A., Dinneny, J. R., Field, B., Froehlich, K., Gardener, C. H., Gojon, A., Gomès, E., Gomez-Alvarez, E. M., Gutierrez, C., Havaux, M., Hayes, S., Heard, E., Hodges, M., Alghamdi, A. K., Laplaze, L., Lauersen, K. J., Leonhardt, N., Johnson, X., Jones, J., Kollist, H., Kopriva, S., Krapp, A., Masson, M. L., McCabe, M. F., Merendino, L., Molina, A., Moreno Ramirez, J. L., Mueller-Roeber, B., Nicolas, M., Nir, I., Orduna, I. O., Pardo, J. M., Reichheld, J. P., Rodriguez, P. L., Rouached, H., Saad, M. M., Schlögelhofer, P., Singh, K. A., De Smet, I., Stanschewski, C., Stra, A., Tester, M., Walsh, C., Weber, A. P., Weigel, D., Wigge, P., Wrzaczek, M., Wulff, B. B., Young, I. M. 2023; 28 (5): 537-543

  Abstract

  Greenhouse gas (GHG) emissions have created a global climate crisis which requires immediate interventions to mitigate the negative effects on all aspects of life on this planet. As current agriculture and land use contributes up to 25% of total GHG emissions, plant scientists take center stage in finding possible solutions for a transition to sustainable agriculture and land use. In this article, the PlantACT! (Plants for climate ACTion!) initiative of plant scientists lays out a road map of how and in which areas plant scientists can contribute to finding immediate, mid-term, and long-term solutions, and what changes are necessary to implement these solutions at the personal, institutional, and funding levels.

  View details for DOI 10.1016/j.tplants.2023.01.005

  View details for PubMedID 36740490

• Genetic Circuit Design in Rhizobacteria. Biodesign research Dundas, C. M., Dinneny, J. R. 2022; 2022: 9858049

  Abstract

  Genetically engineered plants hold enormous promise for tackling global food security and agricultural sustainability challenges. However, construction of plant-based genetic circuitry is constrained by a lack of well-characterized genetic parts and circuit design rules. In contrast, advances in bacterial synthetic biology have yielded a wealth of sensors, actuators, and other tools that can be used to build bacterial circuitry. As root-colonizing bacteria (rhizobacteria) exert substantial influence over plant health and growth, genetic circuit design in these microorganisms can be used to indirectly engineer plants and accelerate the design-build-test-learn cycle. Here, we outline genetic parts and best practices for designing rhizobacterial circuits, with an emphasis on sensors, actuators, and chassis species that can be used to monitor/control rhizosphere and plant processes.

  View details for DOI 10.34133/2022/9858049

  View details for PubMedID 37850138

  View details for PubMedCentralID PMC10521742

• Uncovering natural variation in root system architecture and growth dynamics using a robotics-assisted phenomics platform. eLife LaRue, T., Lindner, H., Srinivas, A., Exposito-Alonso, M., Lobet, G., Dinneny, J. R. 2022; 11

  Abstract

  The plant kingdom contains a stunning array of complex morphologies easily observed above-ground, but more challenging to visualize below-ground. Understanding the magnitude of diversity in root distribution within the soil, termed root system architecture (RSA), is fundamental to determining how this trait contributes to species adaptation in local environments. Roots are the interface between the soil environment and the shoot system and therefore play a key role in anchorage, resource uptake, and stress resilience. Previously, we presented the GLO-Roots (Growth and Luminescence Observatory for Roots) system to study the RSA of soil-grown Arabidopsis thaliana plants from germination to maturity (Rellan-Alvarez et al. 2015). In this study, we present the automation of GLO-Roots using robotics and the development of image analysis pipelines in order to examine the temporal dynamic regulation of RSA and the broader natural variation of RSA in Arabidopsis, over time. These datasets describe the developmental dynamics of two independent panels of accessions and reveal highly complex and polygenic RSA traits that show significant correlation with climate variables of the accessions' respective origins.

  View details for DOI 10.7554/eLife.76968

  View details for PubMedID 36047575

• Burning questions for a warming and changing world: 15 unknowns in plant abiotic stress. The Plant cell Verslues, P. E., Bailey-Serres, J., Brodersen, C., Buckley, T. N., Conti, L., Christmann, A., Dinneny, J. R., Grill, E., Hayes, S., Heckman, R. W., Hsu, P., Juenger, T. E., Mas, P., Munnik, T., Nelissen, H., Sack, L., Schroeder, J. I., Testerink, C., Tyerman, S. D., Umezawa, T., Wigge, P. A. 2022

  Abstract

  We present unresolved questions in plant abiotic stress biology as posed by 15 research groups with expertise spanning eco-physiology to cell and molecular biology. Common themes of these questions include the need to better understand how plants detect water availability, temperature, salinity, and rising CO2 levels; how environmental signals interface with endogenous signaling and development (e.g. circadian clock, flowering time); and how this integrated signaling controls downstream responses (e.g. stomatal regulation, proline metabolism, growth versus defense balance). The plasma membrane comes up frequently as a site of key signaling and transport events (e.g. mechanosensing and lipid-derived signaling, aquaporins). Adaptation to water extremes and rising CO2 affects hydraulic architecture and transpiration, as well as root and shoot growth and morphology, in ways not fully understood. Environmental adaptation involves tradeoffs that limit ecological distribution and crop resilience in the face of changing and increasingly unpredictable environments. Exploration of plant diversity within and among species can help us know which of these tradeoffs represent fundamental limits and which ones can be circumvented by bringing new trait combinations together. Better defining what constitutes beneficial stress resistance in different contexts and making connections between genes and phenotypes, and between laboratory and field observations, are overarching challenges.

  View details for DOI 10.1093/plcell/koac263

  View details for PubMedID 36018271

• Synthetic genetic circuits as a means of reprogramming plant roots. Science (New York, N.Y.) Brophy, J. A., Magallon, K. J., Duan, L., Zhong, V., Ramachandran, P., Kniazev, K., Dinneny, J. R. 2022; 377 (6607): 747-751

  Abstract

  The shape of a plant's root system influences its ability to reach essential nutrients in the soil and to acquire water during drought. Progress in engineering plant roots to optimize water and nutrient acquisition has been limited by our capacity to design and build genetic programs that alter root growth in a predictable manner. We developed a collection of synthetic transcriptional regulators for plants that can be compiled to create genetic circuits. These circuits control gene expression by performing Boolean logic operations and can be used to predictably alter root structure. This work demonstrates the potential of synthetic genetic circuits to control gene expression across tissues and reprogram plant growth.

  View details for DOI 10.1126/science.abo4326

  View details for PubMedID 35951698

• Systematic characterization of gene function in the photosynthetic alga Chlamydomonas reinhardtii. Nature genetics Fauser, F., Vilarrasa-Blasi, J., Onishi, M., Ramundo, S., Patena, W., Millican, M., Osaki, J., Philp, C., Nemeth, M., Salome, P. A., Li, X., Wakao, S., Kim, R. G., Kaye, Y., Grossman, A. R., Niyogi, K. K., Merchant, S. S., Cutler, S. R., Walter, P., Dinneny, J. R., Jonikas, M. C., Jinkerson, R. E. 2022

  Abstract

  Most genes in photosynthetic organisms remain functionally uncharacterized. Here, using a barcoded mutant library of the model eukaryotic alga Chlamydomonas reinhardtii, we determined the phenotypes of more than 58,000 mutants under more than 121 different environmental growth conditions and chemical treatments. A total of 59% of genes are represented by at least one mutant that showed a phenotype, providing clues to the functions of thousands of genes. Mutant phenotypic profiles place uncharacterized genes into functional pathways such as DNA repair, photosynthesis, the CO2-concentrating mechanism and ciliogenesis. We illustrate the value of this resource by validating phenotypes and gene functions, including three new components of an actin cytoskeleton defense pathway. The data also inform phenotype discovery in land plants; mutants in Arabidopsis thaliana genes exhibit phenotypes similar to those we observed in their Chlamydomonas homologs. We anticipate that this resource will guide the functional characterization of genes across the tree of life.

  View details for DOI 10.1038/s41588-022-01052-9

  View details for PubMedID 35513725

• Divergence in the ABA gene regulatory network underlies differential growth control. Nature plants Sun, Y., Oh, D., Duan, L., Ramachandran, P., Ramirez, A., Bartlett, A., Tran, K., Wang, G., Dassanayake, M., Dinneny, J. R. 2022

  Abstract

  The phytohormone abscisic acid (ABA) is a central regulator of acclimation to environmental stress; however, its contribution to differences in stress tolerance between species is unclear. To establish a comparative framework for understanding how stress hormone signalling pathways diverge across species, we studied the growth response of four Brassicaceae species to ABA treatment and generated transcriptomic and DNA affinity purification and sequencing datasets to construct a cross-species gene regulatory network (GRN) for ABA. Comparison of genes bound directly by ABA-responsive element binding factors suggests that cis-factors are most important for determining the target loci represented in the ABA GRN of a particular species. Using this GRN, we reveal how rewiring of growth hormone subnetworks contributes to stark differences in the response to ABA in the extremophyte Schrenkiella parvula. Our study provides a model for understanding how divergence in gene regulation can lead to species-specific physiological outcomes in response to hormonal cues.

  View details for DOI 10.1038/s41477-022-01139-5

  View details for PubMedID 35501452

• A Thermoacoustic Imaging System for Noninvasive and Nondestructive Root Phenotyping IEEE TRANSACTIONS ON CIRCUITS AND SYSTEMS II-EXPRESS BRIEFS Singhvi, A., Fitzpatrick, A., Scharwies, J., Dinneny, J. R., Arbabian, A. 2022; 69 (5): 2493-2497

  View details for DOI 10.1109/TCSII.2022.3159448

  View details for Web of Science ID 000790814000025

• Deconstructing the root system of grasses through an exploration of development, anatomy, and function. Plant, cell & environment Viana, W. G., Scharwies, J. D., Dinneny, J. R. 1800

  Abstract

  Well-adapted root systems allow plants to grow under resource-limiting environmental conditions and are important determinants of yield in agricultural systems. Important staple crops such as rice and maize belong to the family of grasses, which develop a complex root system that consists of an embryonic root system that emerges from the seed, and a postembryonic nodal root system that emerges from basal regions of the shoot after germination. While early seedling establishment is dependent on the embryonic root system, the nodal root system, and its associated branches, gains in importance as the plant matures and will ultimately constitute the bulk of below-ground growth. In this review, we aim to give an overview of the different root types that develop in cereal grass root systems, explore the different physiological roles they play by defining their anatomical features, and outline the genetic networks that control their development. Through this deconstructed view of grass root system function, we provide a parts-list of elements that function together in an integrated root system to promote survival and crop productivity. This article is protected by copyright. All rights reserved.

  View details for DOI 10.1111/pce.14270

  View details for PubMedID 35092025

• Intrinsically disordered protein biosensor tracks the physical-chemical effects of osmotic stress on cells. Nature communications Cuevas-Velazquez, C. L., Vellosillo, T., Guadalupe, K., Schmidt, H. B., Yu, F., Moses, D., Brophy, J. A., Cosio-Acosta, D., Das, A., Wang, L., Jones, A. M., Covarrubias, A. A., Sukenik, S., Dinneny, J. R. 2021; 12 (1): 5438

  Abstract

  Cell homeostasis is perturbed when dramatic shifts in the external environment cause the physical-chemical properties inside the cell to change. Experimental approaches for dynamically monitoring these intracellular effects are currently lacking. Here, we leverage the environmental sensitivity and structural plasticity of intrinsically disordered protein regions (IDRs) to develop a FRET biosensor capable of monitoring rapid intracellular changes caused by osmotic stress. The biosensor, named SED1, utilizes the Arabidopsis intrinsically disordered AtLEA4-5 protein expressed in plants under water deficit. Computational modeling and in vitro studies reveal that SED1 is highly sensitive to macromolecular crowding. SED1 exhibits large and near-linear osmolarity-dependent changes in FRET inside living bacteria, yeast, plant, and human cells, demonstrating the broad utility of this tool for studying water-associated stress. This study demonstrates the remarkable ability of IDRs to sense the cellular environment across the tree of life and provides a blueprint for their use as environmentally-responsive molecular tools.

  View details for DOI 10.1038/s41467-021-25736-8

  View details for PubMedID 34521831

• A plant lipocalin promotes retinal-mediated oscillatory lateral root initiation. Science (New York, N.Y.) Dickinson, A. J., Zhang, J., Luciano, M., Wachsman, G., Sandoval, E., Schnermann, M., Dinneny, J. R., Benfey, P. N. 2021

  Abstract

  In Arabidopsis, de novo organogenesis of lateral roots is patterned by an oscillatory mechanism called the root clock, which is dependent on unidentified metabolites. To determine if retinoids regulate the root clock, we used a chemical reporter for retinaldehyde (retinal) binding proteins. We found that retinal binding precedes the root clock and predicts sites of lateral root organogenesis. Application of retinal increased root clock oscillations and promoted lateral root formation. Expression of an Arabidopsis protein with homology to vertebrate retinoid binding proteins, TEMPERATURE INDUCED LIPOCALIN (TIL) oscillates in the region of retinal binding to the reporter, confers retinal binding activity in a heterologous system, and when mutated, decreases retinal sensitivity. These results demonstrate a role for retinal and its binding partner in lateral root organogenesis.

  View details for DOI 10.1126/science.abf7461

  View details for PubMedID 34446443

• TRANVIA (TVA) facilitates cellulose synthase trafficking and delivery to the plasma membrane. Proceedings of the National Academy of Sciences of the United States of America Vellosillo, T., Dinneny, J. R., Somerville, C. R., Ehrhardt, D. W. 2021; 118 (30)

  Abstract

  Cellulose is synthesized at the plasma membrane by cellulose synthase (CESA) complexes (CSCs), which are assembled in the Golgi and secreted to the plasma membrane through the trans-Golgi network (TGN) compartment. However, the molecular mechanisms that guide CSCs through the secretory system and deliver them to the plasma membrane are poorly understood. Here, we identified an uncharacterized gene, TRANVIA (TVA), that is transcriptionally coregulated with the CESA genes required for primary cell wall synthesis. The tva mutant exhibits enhanced sensitivity to cellulose synthesis inhibitors; reduced cellulose content; and defective dynamics, density, and secretion of CSCs to the plasma membrane as compared to wild type. TVA is a plant-specific protein of unknown function that is detected in at least two different intracellular compartments: organelles labeled by markers for the TGN and smaller compartments that deliver CSCs to the plasma membrane. Together, our data suggest that TVA promotes trafficking of CSCs to the plasma membrane by facilitating exit from the TGN and/or interaction of CSC secretory vesicles with the plasma membrane.

  View details for DOI 10.1073/pnas.2021790118

  View details for PubMedID 34290139

• Broadening the impact of plant science through innovative, integrative, and inclusive outreach. Plant direct Friesner, J., Colon-Carmona, A., Schnoes, A. M., Stepanova, A., Mason, G. A., Macintosh, G. C., Ullah, H., Baxter, I., Callis, J., Sierra-Cajas, K., Elliott, K., Haswell, E. S., Zavala, M. E., Wildermuth, M., Williams, M., Ayalew, M., Henkhaus, N., Prunet, N., Lemaux, P. G., Yadegari, R., Amasino, R., Hangarter, R., Innes, R., Brady, S., Long, T., Woodford-Thomas, T., May, V., Sun, Y., Dinneny, J. R. 2021; 5 (4): e00316

  Abstract

  Population growth and climate change will impact food security and potentially exacerbate the environmental toll that agriculture has taken on our planet. These existential concerns demand that a passionate, interdisciplinary, and diverse community of plant science professionals is trained during the 21st century. Furthermore, societal trends that question the importance of science and expert knowledge highlight the need to better communicate the value of rigorous fundamental scientific exploration. Engaging students and the general public in the wonder of plants, and science in general, requires renewed efforts that take advantage of advances in technology and new models of funding and knowledge dissemination. In November 2018, funded by the National Science Foundation through the Arabidopsis Research and Training for the 21st century (ART 21) research coordination network, a symposium and workshop were held that included a diverse panel of students, scientists, educators, and administrators from across the US. The purpose of the workshop was to re-envision how outreach programs are funded, evaluated, acknowledged, and shared within the plant science community. One key objective was to generate a roadmap for future efforts. We hope that this document will serve as such, by providing a comprehensive resource for students and young faculty interested in developing effective outreach programs. We also anticipate that this document will guide the formation of community partnerships to scale up currently successful outreach programs, and lead to the design of future programs that effectively engage with a more diverse student body and citizenry.

  View details for DOI 10.1002/pld3.316

  View details for PubMedID 33870032

• Characterization of CYCLOPHILLIN38 shows that a photosynthesis-derived systemic signal controls lateral root emergence. Plant physiology Duan, L. n., Pérez-Ruiz, J. M., Cejudo, F. J., Dinneny, J. R. 2021; 185 (2): 503–18

  Abstract

  Photosynthesis in leaves generates fixed-carbon resources and essential metabolites that support sink tissues, such as roots. Two of these metabolites, sucrose and auxin, promote growth in root systems, but the explicit connection between photosynthetic activity and control of root architecture has not been explored. Through a mutant screen to identify pathways regulating root system architecture, we identified a mutation in the Arabidopsis thaliana CYCLOPHILIN 38 (CYP38) gene, which causes accumulation of pre-emergent stage lateral roots. CYP38 was previously reported to stabilize photosystem II (PSII) in chloroplasts. CYP38 expression is enriched in shoots, and grafting experiments show that the gene acts non-cell-autonomously to promote lateral root emergence. Growth of wild-type plants under low-light conditions phenocopies the cyp38 lateral root emergence defect, as does the inhibition of PSII-dependent electron transport or Nicotinamide adenine dinucleotide phosphate (NADPH) production. Importantly, these perturbations to photosynthetic activity rapidly suppress lateral root emergence, which is separate from their effects on shoot size. Supplementary exogenous sucrose largely rescued primary root (PR) growth in cyp38, but not lateral root growth. Auxin (indole-3-acetic acid (IAA)) biosynthesis from tryptophan is dependent on reductant generated during photosynthesis. Consistently, we found that wild-type seedlings grown under low light and cyp38 mutants have highly diminished levels of IAA in root tissues. IAA treatment rescued the cyp38 lateral root defect, revealing that photosynthesis promotes lateral root emergence partly through IAA biosynthesis. These data directly confirm the importance of CYP38-dependent photosynthetic activity in supporting root growth, and define the specific contributions of two metabolites in refining root architecture under light-limited conditions.

  View details for DOI 10.1093/plphys/kiaa032

  View details for PubMedID 33721893

• Mechanobiology: Plant Cells Face Pressure from Neighbors. Current biology : CB Dinneny, J. R. 2020; 30 (8): R344–R346

  Abstract

  Plant cell growth is constrained by the rate of water uptake and wallextensibility. New research reveals that the topology and geometry of cells in a tissue predicts the pressures that ultimately determine growth.

  View details for DOI 10.1016/j.cub.2020.02.025

  View details for PubMedID 32315631

• A Wall with Integrity: Surveillance and Maintenance of the Plant Cell Wall Under Stress. The New phytologist Rui, Y., Dinneny, J. R. 2019

  Abstract

  The structural and functional integrity of the wall needs to be constantly monitored and fine-tuned to allow for growth while preventing mechanical failure. Many studies have advanced our understanding of the pathways contributing to cell wall biosynthesis and how these pathways are regulated by external and internal cues. Recent evidence also supports a model in which certain aspects of the wall itself may act as growth-regulating signals. Molecular components of the signaling pathways that sense and maintain cell wall integrity have begun to be revealed, including signals arising in the wall, sensors that detect changes at the cell surface, and downstream signal transduction modules. Abiotic and biotic stress conditions set new contexts to study cell wall integrity, but the nature and consequences of wall disruptions by various stressors require further investigations. A deeper understanding of cell wall signaling will provide insights into the growth regulatory mechanisms that allow plants to survive in a changing environment. This article is protected by copyright. All rights reserved.

  View details for DOI 10.1111/nph.16166

  View details for PubMedID 31486535

• Cytokinin functions as an asymmetric and anti-gravitropic signal in lateral roots. Nature communications Waidmann, S., Ruiz Rosquete, M., Scholler, M., Sarkel, E., Lindner, H., LaRue, T., Petrik, I., Dunser, K., Martopawiro, S., Sasidharan, R., Novak, O., Wabnik, K., Dinneny, J. R., Kleine-Vehn, J. 2019; 10 (1): 3540

  Abstract

  Directional organ growth allows the plant root system to strategically cover its surroundings. Intercellular auxin transport is aligned with the gravity vector in the primary root tips, facilitating downward organ bending at the lower root flank. Here we show that cytokinin signaling functions as a lateral root specific anti-gravitropic component, promoting the radial distribution of the root system. We performed a genome-wide association study and reveal that signal peptide processing of Cytokinin Oxidase 2 (CKX2) affects its enzymatic activity and, thereby, determines the degradation of cytokinins in natural Arabidopsis thaliana accessions. Cytokinin signaling interferes with growth at the upper lateral root flank and thereby prevents downward bending. Our interdisciplinary approach proposes that two phytohormonal cues at opposite organ flanks counterbalance each other's negative impact on growth, suppressing organ growth towards gravity and allow for radial expansion of the root system.

  View details for DOI 10.1038/s41467-019-11483-4

  View details for PubMedID 31387989

• Developmental Responses to Water and Salinity in Root Systems. Annual review of cell and developmental biology Dinneny, J. R. 2019

  Abstract

  Roots provide the primary mechanism that plants use to absorb water and nutrients from their environment. These functions are dependent on developmental mechanisms that direct root growth and branching into regions of soil where these resources are relatively abundant. Water is the most limiting factor for plant growth, and its availability is determined by the weather, soil structure, and salinity. In this review, we define the developmental pathways that regulate the direction of growth and branching pattern of the root system, which together determine the expanse of soil from which a plant can access water. The ability of plants to regulate development in response to the spatial distribution of water is a focus of many recent studies and provides a model for understanding how biological systems utilize positional cues to affect signaling and morphogenesis. A better understanding of these processes will inform approaches to improve crop water use efficiency to more sustainably feed a growing population. Expected final online publication date for the Annual Review of Cell and Developmental Biology, Volume 35 is October 7, 2019. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

  View details for DOI 10.1146/annurev-cellbio-100617-062949

  View details for PubMedID 31382759

• EcoFABs: advancing microbiome science through standardized fabricated ecosystems. Nature methods Zengler, K., Hofmockel, K., Baliga, N. S., Behie, S. W., Bernstein, H. C., Brown, J. B., Dinneny, J. R., Floge, S. A., Forry, S. P., Hess, M., Jackson, S. A., Jansson, C., Lindemann, S. R., Pett-Ridge, J., Maranas, C., Venturelli, O. S., Wallenstein, M. D., Shank, E. A., Northen, T. R. 2019

  View details for DOI 10.1038/s41592-019-0465-0

  View details for PubMedID 31227812

• beta-Cyclocitral is a conserved root growth regulator PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA Dickinson, A. J., Lehner, K., Mi, J., Jia, K., Mijar, M., Dinneny, J., Al-Babili, S., Benfey, P. N. 2019; 116 (21): 10563–67

  View details for DOI 10.1073/pnas.1821445116

  View details for Web of Science ID 000468403400061

• Environmental Stress: Salinity Ruins a Plant's Day inthe Sun. Current biology : CB Magallon, K. J., Dinneny, J. R. 2019; 29 (10): R360–R362

  Abstract

  New research reveals how low levels of salinity in soil inhibit a plant's ability to respond to shade through a signaling mechanism involving the plant stress hormone abscisic acid.

  View details for DOI 10.1016/j.cub.2019.04.006

  View details for PubMedID 31112684

• Water transport, perception, and response in plants JOURNAL OF PLANT RESEARCH Scharwies, J., Dinneny, J. R. 2019; 132 (3): 311–24

  View details for DOI 10.1007/s10265-019-01089-8

  View details for Web of Science ID 000467486400003

• Directions for research and training in plant omics: Big Questions and Big Data. Plant direct Argueso, C. T., Assmann, S. M., Birnbaum, K. D., Chen, S., Dinneny, J. R., Doherty, C. J., Eveland, A. L., Friesner, J., Greenlee, V. R., Law, J. A., Marshall-Colon, A., Mason, G. A., O'Lexy, R., Peck, S. C., Schmitz, R. J., Song, L., Stern, D., Varagona, M. J., Walley, J. W., Williams, C. M. 2019; 3 (4): e00133

  Abstract

  A key remit of the NSF-funded "Arabidopsis Research and Training for the 21st Century" (ART-21) Research Coordination Network has been to convene a series of workshops with community members to explore issues concerning research and training in plant biology, including the role that research using Arabidopsis thaliana can play in addressing those issues. A first workshop focused on training needs for bioinformatic and computational approaches in plant biology was held in 2016, and recommendations from that workshop have been published (Friesner etal., Plant Physiology, 175, 2017, 1499). In this white paper, we provide a summary of the discussions and insights arising from the second ART-21 workshop. The second workshop focused on experimental aspects of omics data acquisition and analysis and involved a broad spectrum of participants from academics and industry, ranging from graduate students through post-doctorates, early career and established investigators. Our hope is that this article will inspire beginning and established scientists, corporations, and funding agencies to pursue directions in research and training identified by this workshop, capitalizing on the reference species Arabidopsis thaliana and other valuable plant systems.

  View details for DOI 10.1002/pld3.133

  View details for PubMedID 31245771

• Non-Contact Thermoacoustic Sensing and Characterization of Plant Root Traits Singhvi, A., Ma, B., Scharwies, J., Dinneny, J. R., Khuri-Yakub, B. T., Arbabian, A., IEEE IEEE. 2019: 1992–95

  View details for Web of Science ID 000510220100511

• Root branching toward water involves posttranslational modification of transcription factor ARF7. Science (New York, N.Y.) Orosa-Puente, B., Leftley, N., von Wangenheim, D., Banda, J., Srivastava, A. K., Hill, K., Truskina, J., Bhosale, R., Morris, E., Srivastava, M., Kumpers, B., Goh, T., Fukaki, H., Vermeer, J. E., Vernoux, T., Dinneny, J. R., French, A. P., Bishopp, A., Sadanandom, A., Bennett, M. J. 2018; 362 (6421): 1407–10

  Abstract

  Plants adapt to heterogeneous soil conditions by altering their root architecture. For example, roots branch when in contact with water by using the hydropatterning response. We report that hydropatterning is dependent on auxin response factor ARF7. This transcription factor induces asymmetric expression of its target gene LBD16 in lateral root founder cells. This differential expression pattern is regulated by posttranslational modification of ARF7 with the small ubiquitin-like modifier (SUMO) protein. SUMOylation negatively regulates ARF7 DNA binding activity. ARF7 SUMOylation is required to recruit the Aux/IAA (indole-3-acetic acid) repressor protein IAA3. Blocking ARF7 SUMOylation disrupts IAA3 recruitment and hydropatterning. We conclude that SUMO-dependent regulation of auxin response controls root branching pattern in response to water availability.

  View details for PubMedID 30573626

• Suppression of Arabidopsis GGLT1 affects growth by reducing the L-galactose content and borate cross-linking of rhamnogalacturonan-II PLANT JOURNAL Sechet, J., Htwe, S., Urbanowicz, B., Agyeman, A., Feng, W., Ishikawa, T., Colomes, M., Kumar, K., Kawai-Yamada, M., Dinneny, J. R., O'Neill, M. A., Mortimer, J. C. 2018; 96 (5): 1036–50

  Abstract

  Boron is a micronutrient that is required for the normal growth and development of vascular plants, but its precise functions remain a subject of debate. One established role for boron is in the cell wall where it forms a diester cross-link between two monomers of the low-abundance pectic polysaccharide rhamnogalacturonan-II (RG-II). The inability of RG-II to properly assemble into a dimer results in the formation of cell walls with abnormal biochemical and biomechanical properties and has a severe impact on plant productivity. Here we describe the effects on RG-II structure and cross-linking and on the growth of plants in which the expression of a GDP-sugar transporter (GONST3/GGLT1) has been reduced. In the GGLT1-silenced plants the amount of L-galactose in side-chain A of RG-II is reduced by up to 50%. This leads to a reduction in the extent of RG-II cross-linking in the cell walls as well as a reduction in the stability of the dimer in the presence of calcium chelators. The silenced plants have a dwarf phenotype, which is rescued by growth in the presence of increased amounts of boric acid. Similar to the mur1 mutant, which also disrupts RG-II cross-linking, GGLT1-silenced plants display a loss of cell wall integrity under salt stress. We conclude that GGLT1 is probably the primary Golgi GDP-L-galactose transporter, and provides GDP-L-galactose for RG-II biosynthesis. We propose that the L-galactose residue is critical for RG-II dimerization and for the stability of the borate cross-link.

  View details for PubMedID 30203879

  View details for PubMedCentralID PMC6263843

• Organization out of disorder: liquid-liquid phase separation in plants CURRENT OPINION IN PLANT BIOLOGY Cuevas-Velazquez, C. L., Dinneny, J. R. 2018; 45: 68–74

  View details for DOI 10.1016/j.pbi.2018.05.005

  View details for Web of Science ID 000451490600008

• Seeds of Science Why We Got It So Wrong on GMOs (Book Review) SCIENCE Book Review Authored by: Dinneny, J. R. 2018; 360 (6396): 1407

  View details for DOI 10.1126/science.aat8772

  View details for Web of Science ID 000436598000029

• Organization out of disorder: liquid-liquid phase separation in plants. Current opinion in plant biology Cuevas-Velazquez, C. L., Dinneny, J. R. 2018; 45 (Pt A): 68–74

  Abstract

  Membraneless compartments are formed from the dynamic physical association of proteins and RNAs through liquid-liquid phase separation, and have recently emerged as an exciting new mechanism to explain the dynamic organization of biochemical processes in the cell. In this review, we provide an overview of the current knowledge of the process of phase separation in plants and other eukaryotes. We discuss specific examples of liquid-like membraneless compartments found in green plants, their composition, and the intriguing prevalence of proteins with intrinsically disordered domains. Finally, we speculate on the function of disordered proteins in regulating the formation of membraneless compartments and how their conformational flexibility may be important for molecular memory and for sensing perturbations in the physicochemical environment of the cell, particularly important processes in sessile organisms.

  View details for PubMedID 29859470

• Q&A: How do gene regulatory networks control environmental responses in plants? BMC BIOLOGY Sun, Y., Dinneny, J. R. 2018; 16: 38

  Abstract

  A gene regulatory network (GRN) describes the hierarchical relationship between transcription factors, associated proteins, and their target genes. Studying GRNs allows us to understand how a plant's genotype and environment are integrated to regulate downstream physiological responses. Current efforts in plants have focused on defining the GRNs that regulate functions such as development and stress response and have been performed primarily in genetically tractable model plant species such as Arabidopsis thaliana. Future studies will likely focus on how GRNs function in non-model plants and change over evolutionary time to allow for adaptation to extreme environments. This broader understanding will inform efforts to engineer GRNs to create tailored crop traits.

  View details for PubMedID 29642893

• Growth is required for perception of water availability to pattern root branches in plants. Proceedings of the National Academy of Sciences of the United States of America Robbins, N. E., Dinneny, J. R. 2018

  Abstract

  Water availability is a potent regulator of plant development and induces root branching through a process termed hydropatterning. Hydropatterning enables roots to position lateral branches toward regions of high water availability, such as wet soil or agar media, while preventing their emergence where water is less available, such as in air. The mechanism by which roots perceive the spatial distribution of water during hydropatterning is unknown. Using primary roots of Zea mays (maize) we reveal that developmental competence for hydropatterning is limited to the growth zone of the root tip. Past work has shown that growth generates gradients in water potential across an organ when asymmetries exist in the distribution of available water. Using mathematical modeling, we predict that substantial growth-sustained water potential gradients are also generated in the hydropatterning competent zone and that such biophysical cues inform the patterning of lateral roots. Using diverse chemical and environmental treatments we experimentally demonstrate that growth is necessary for normal hydropatterning of lateral roots. Transcriptomic characterization of the local response of tissues to a moist surface or air revealed extensive regulation of signaling and physiological pathways, some of which we show are growth-dependent. Our work supports a "sense-by-growth" mechanism governing hydropatterning, by which water availability cues are rendered interpretable through growth-sustained water movement.

  View details for PubMedID 29317538

• The 6xABRE synthetic promoter enables the spatiotemporal analysis of ABA-mediated transcriptional regulation. Plant physiology Wu, R. n., Duan, L. n., Pruneda-Paz, J. n., Oh, D. H., Pound, M. P., Kay, S. A., Dinneny, J. R. 2018

  Abstract

  The water stress-associated hormone abscisic acid (ABA) acts through a well-defined signal transduction cascade to mediate downstream transcriptional events important for acclimation to stress. Although ABA signaling is known to function in specific tissues to regulate root growth, little is understood regarding the spatial pattern of ABA-mediated transcriptional regulation. Here we describe the construction and evaluation of an ABSCISIC ACID RESPONSIVE ELEMENT (ABRE)-based synthetic promoter reporter that reveals the transcriptional response of tissues to different levels of exogenous ABA and stresses. Genome-scale yeast-one-hybrid screens complemented these approaches and revealed how promoter sequence and architecture affect the recruitment of diverse transcription factors (TFs) to the ABRE. Our analysis also revealed ABA-independent activity of the ABRE-reporter under non-stress conditions, with activity being enriched at the quiescent center and stem cell niche. We show that the WUSCHEL RELATED HOMEOBOX 5 and NAC DOMAIN PROTEIN 13 TFs regulate QC/SCN expression of the ABRE-reporter, which highlights the convergence of developmental and DNA-damage signaling pathways onto this cis-element in the absence of water stress. This work establishes a tool to study the spatial pattern of ABA-mediated transcriptional regulation and a repertoire of TF-ABRE interactions that contribute to the developmental and environmental control of gene expression in roots.

  View details for PubMedID 29884679

• The FERONIA Receptor Kinase Maintains Cell-Wall Integrity during Salt Stress through Ca2+Signaling. Current biology : CB Feng, W. n., Kita, D. n., Peaucelle, A. n., Cartwright, H. N., Doan, V. n., Duan, Q. n., Liu, M. C., Maman, J. n., Steinhorst, L. n., Schmitz-Thom, I. n., Yvon, R. n., Kudla, J. n., Wu, H. M., Cheung, A. Y., Dinneny, J. R. 2018

  Abstract

  Cells maintain integrity despite changes in their mechanical properties elicited during growth and environmental stress. How cells sense their physical state and compensate for cell-wall damage is poorly understood, particularly in plants. Here we report that FERONIA (FER), a plasma-membrane-localized receptor kinase from Arabidopsis, is necessary for the recovery of root growth after exposure to high salinity, a widespread soil stress. The extracellular domain of FER displays tandem regions of homology with malectin, an animal protein known to bind di-glucose in vitro and important for protein quality control in the endoplasmic reticulum. The presence of malectin-like domains in FER and related receptor kinases has led to widespread speculation that they interact with cell-wall polysaccharides and can potentially serve a wall-sensing function. Results reported here show that salinity causes softening of the cell wall and that FER is necessary to sense these defects. When this function is disrupted in the fer mutant, root cells explode dramatically during growth recovery. Similar defects are observed in the mur1 mutant, which disrupts pectin cross-linking. Furthermore, fer cell-wall integrity defects can be rescued by treatment with calcium and borate, which also facilitate pectin cross-linking. Sensing of these salinity-induced wall defects might therefore be a direct consequence of physical interaction between the extracellular domain of FER and pectin. FER-dependent signaling elicits cell-specific calcium transients that maintain cell-wall integrity during salt stress. These results reveal a novel extracellular toxicity of salinity, and identify FER as a sensor of damage to the pectin-associated wall.

  View details for PubMedID 29456142

• Time dependent genetic analysis links field and controlled environment phenotypes in the model C4 grass Setaria. PLoS genetics Feldman, M. J., Paul, R. E., Banan, D., Barrett, J. F., Sebastian, J., Yee, M. C., Jiang, H., Lipka, A. E., Brutnell, T. P., Dinneny, J. R., Leakey, A. D., Baxter, I. 2017; 13 (6): e1006841

  Abstract

  Vertical growth of plants is a dynamic process that is influenced by genetic and environmental factors and has a pronounced effect on overall plant architecture and biomass composition. We have performed six controlled growth trials of an interspecific Setaria italica x Setaria viridis recombinant inbred line population to assess how the genetic architecture of plant height is influenced by developmental queues, water availability and planting density. The non-destructive nature of plant height measurements has enabled us to monitor height throughout the plant life cycle in both field and controlled environments. We find that plant height is reduced under water limitation and high density planting and affected by growth environment (field vs. growth chamber). The results support a model where plant height is a heritable, polygenic trait and that the major genetic loci that influence plant height function independent of growth environment. The identity and contribution of loci that influence height changes dynamically throughout development and the reduction of growth observed in water limited environments is a consequence of delayed progression through the genetic program which establishes plant height in Setaria. In this population, alleles inherited from the weedy S. viridis parent act to increase plant height early, whereas a larger number of small effect alleles inherited from the domesticated S. italica parent collectively act to increase plant height later in development.

  View details for DOI 10.1371/journal.pgen.1006841

  View details for PubMedID 28644860

  View details for PubMedCentralID PMC5507400

• A microbially derived tyrosine-sulfated peptide mimics a plant peptide hormone. New phytologist Pruitt, R. N., Joe, A., Zhang, W., Feng, W., Stewart, V., Schwessinger, B., Dinneny, J. R., Ronald, P. C. 2017

  Abstract

  The biotrophic pathogen Xanthomonas oryzae pv. oryzae (Xoo) produces a sulfated peptide named RaxX, which shares similarity to peptides in the PSY (plant peptide containing sulfated tyrosine) family. We hypothesize that RaxX mimics the growth-stimulating activity of PSY peptides. Root length was measured in Arabidopsis and rice treated with synthetic RaxX peptides. We also used comparative genomic analyses and reactive oxygen species burst assays to evaluate the activity of RaxX and PSY peptides. Here we found that a synthetic sulfated RaxX derivative comprising 13 residues (RaxX13-sY), highly conserved between RaxX and PSY, induces root growth in Arabidopsis and rice in a manner similar to that triggered by PSY. We identified residues that are required for activation of immunity mediated by the rice XA21 receptor but that are not essential for root growth induced by PSY. Finally, we showed that a Xanthomonas strain lacking raxX is impaired in virulence. These findings suggest that RaxX serves as a molecular mimic of PSY peptides to facilitate Xoo infection and that XA21 has evolved the ability to recognize and respond specifically to the microbial form of the peptide.

  View details for DOI 10.1111/nph.14609

  View details for PubMedID 28556915

• Root hydrotropism is controlled via a cortex-specific growth mechanism. Nature plants Dietrich, D., Pang, L., Kobayashi, A., Fozard, J. A., Boudolf, V., Bhosale, R., Antoni, R., Nguyen, T., Hiratsuka, S., Fujii, N., Miyazawa, Y., Bae, T., Wells, D. M., Owen, M. R., Band, L. R., Dyson, R. J., Jensen, O. E., King, J. R., Tracy, S. R., Sturrock, C. J., Mooney, S. J., Roberts, J. A., Bhalerao, R. P., Dinneny, J. R., Rodriguez, P. L., Nagatani, A., Hosokawa, Y., Baskin, T. I., Pridmore, T. P., De Veylder, L., Takahashi, H., Bennett, M. J. 2017; 3: 17057-?

  Abstract

  Plants can acclimate by using tropisms to link the direction of growth to environmental conditions. Hydrotropism allows roots to forage for water, a process known to depend on abscisic acid (ABA) but whose molecular and cellular basis remains unclear. Here we show that hydrotropism still occurs in roots after laser ablation removed the meristem and root cap. Additionally, targeted expression studies reveal that hydrotropism depends on the ABA signalling kinase SnRK2.2 and the hydrotropism-specific MIZ1, both acting specifically in elongation zone cortical cells. Conversely, hydrotropism, but not gravitropism, is inhibited by preventing differential cell-length increases in the cortex, but not in other cell types. We conclude that root tropic responses to gravity and water are driven by distinct tissue-based mechanisms. In addition, unlike its role in root gravitropism, the elongation zone performs a dual function during a hydrotropic response, both sensing a water potential gradient and subsequently undergoing differential growth.

  View details for DOI 10.1038/nplants.2017.57

  View details for PubMedID 28481327

• Understanding and engineering plant form. Seminars in cell & developmental biology Brophy, J. A., LaRue, T. n., Dinneny, J. R. 2017

  Abstract

  A plant's form is an important determinant of its fitness and economic value. Here, we review strategies for producing plants with altered forms. Historically, the process of changing a plant's form has been slow in agriculture, requiring iterative rounds of growth and selection. We discuss modern techniques for identifying genes involved in the development of plant form and tools that will be needed to effectively design and engineer plants with altered forms. Synthetic genetic circuits are highlighted for their potential to generate novel plant forms. We emphasize understanding development as a prerequisite to engineering and discuss the potential role of computer models in translating knowledge about single genes or pathways into a more comprehensive understanding of development.

  View details for PubMedID 28864344

• Setaria viridis: A Model for Understanding Panicoid Grass Root Systems GENETICS AND GENOMICS OF SETARIA Sebastian, J., Dinneny, J. R., Doust, A., Diao 2017; 19: 177–93

  View details for DOI 10.1007/978-3-319-45105-3_11

  View details for Web of Science ID 000415645300012

• The Next Generation of Training for Arabidopsis Researchers: Bioinformatics and Quantitative Biology. Plant physiology Friesner, J. n., Assmann, S. M., Bastow, R. n., Bailey-Serres, J. n., Beynon, J. n., Brendel, V. n., Buell, C. R., Bucksch, A. n., Busch, W. n., Demura, T. n., Dinneny, J. R., Doherty, C. J., Eveland, A. L., Falter-Braun, P. n., Gehan, M. A., Gonzales, M. n., Grotewold, E. n., Gutierrez, R. n., Kramer, U. n., Krouk, G. n., Ma, S. n., Markelz, R. J., Megraw, M. n., Meyers, B. C., Murray, J. A., Provart, N. J., Rhee, S. n., Smith, R. n., Spalding, E. P., Taylor, C. n., Teal, T. K., Torii, K. U., Town, C. n., Vaughn, M. n., Vierstra, R. n., Ware, D. n., Wilkins, O. n., Williams, C. n., Brady, S. M. 2017; 175 (4): 1499–1509

  View details for PubMedID 29208732

• Grasses suppress shoot-borne roots to conserve water during drought PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA Sebastian, J., Yee, M., Viana, W. G., Rellan-Alvarez, R., Feldman, M., Priest, H. D., Trontin, C., Lee, T., Jiang, H., Baxter, I., Mockler, T. C., Hochholdinger, F., Brutnell, T. P., Dinneny, J. R. 2016; 113 (31): 8861-8866

  Abstract

  Many important crops are members of the Poaceae family, which develop root systems characterized by a high degree of root initiation from the belowground basal nodes of the shoot, termed the crown. Although this postembryonic shoot-borne root system represents the major conduit for water uptake, little is known about the effect of water availability on its development. Here we demonstrate that in the model C4 grass Setaria viridis, the crown locally senses water availability and suppresses postemergence crown root growth under a water deficit. This response was observed in field and growth room environments and in all grass species tested. Luminescence-based imaging of root systems grown in soil-like media revealed a shift in root growth from crown-derived to primary root-derived branches, suggesting that primary root-dominated architecture can be induced in S. viridis under certain stress conditions. Crown roots of Zea mays and Setaria italica, domesticated relatives of teosinte and S. viridis, respectively, show reduced sensitivity to water deficit, suggesting that this response might have been influenced by human selection. Enhanced water status of maize mutants lacking crown roots suggests that under a water deficit, stronger suppression of crown roots actually may benefit crop productivity.

  View details for DOI 10.1073/pnas.1604021113

  View details for Web of Science ID 000380586600078

  View details for PubMedCentralID PMC4978293

• Growing Out of Stress: The Role of Cell- and Organ-Scale Growth Control in Plant Water-Stress Responses. Plant cell Feng, W., Lindner, H., Robbins, N. E., Dinneny, J. R. 2016; 28 (8): 1769-1782

  Abstract

  Water is the most limiting resource on land for plant growth, and its uptake by plants is affected by many abiotic stresses, such as salinity, cold, heat, and drought. While much research has focused on exploring the molecular mechanisms underlying the cellular signaling events governing water-stress responses, it is also important to consider the role organismal structure plays as a context for such responses. The regulation of growth in plants occurs at two spatial scales: the cell and the organ. In this review, we focus on how the regulation of growth at these different spatial scales enables plants to acclimate to water-deficit stress. The cell wall is discussed with respect to how the physical properties of this structure affect water loss and how regulatory mechanisms that affect wall extensibility maintain growth under water deficit. At a higher spatial scale, the architecture of the root system represents a highly dynamic physical network that facilitates access of the plant to a heterogeneous distribution of water in soil. We discuss the role differential growth plays in shaping the structure of this system and the physiological implications of such changes.

  View details for DOI 10.1105/tpc.16.00182

  View details for PubMedID 27503468

  View details for PubMedCentralID PMC5006702

• Environmental Control of Root System Biology ANNUAL REVIEW OF PLANT BIOLOGY, VOL 67 Rellan-Alvarez, R., Lobet, G., Dinneny, J. R. 2016; 67: 619-642

  Abstract

  The plant root system traverses one of the most complex environments on earth. Understanding how roots support plant life on land requires knowing how soil properties affect the availability of nutrients and water and how roots manipulate the soil environment to optimize acquisition of these resources. Imaging of roots in soil allows the integrated analysis and modeling of environmental interactions occurring at micro- to macroscales. Advances in phenotyping of root systems is driving innovation in cross-platform-compatible methods for data analysis. Root systems acclimate to the environment through architectural changes that act at the root-type level as well as through tissue-specific changes that affect the metabolic needs of the root and the efficiency of nutrient uptake. A molecular understanding of the signaling mechanisms that guide local and systemic signaling is providing insight into the regulatory logic of environmental responses and has identified points where crosstalk between pathways occurs.

  View details for DOI 10.1146/annurev-arplant-043015-111848

  View details for Web of Science ID 000375803200025

  View details for PubMedID 26905656

• GLO-Roots: an imaging platform enabling multidimensional characterization of soil-grown root systems ELIFE Rellan-Alvarez, R., Lobet, G., Lindner, H., Pradier, P., Sebastian, J., Yee, M., Geng, Y., Trontin, C., LaRue, T., Schrager-Lavelle, A., Haney, C. H., Nieu, R., Maloof, J., Vogel, J. P., Dinneny, J. R. 2015; 4

  Abstract

  Root systems develop different root types that individually sense cues from their local environment and integrate this information with systemic signals. This complex multi-dimensional amalgam of inputs enables continuous adjustment of root growth rates, direction, and metabolic activity that define a dynamic physical network. Current methods for analyzing root biology balance physiological relevance with imaging capability. To bridge this divide, we developed an integrated-imaging system called Growth and Luminescence Observatory for Roots (GLO-Roots) that uses luminescence-based reporters to enable studies of root architecture and gene expression patterns in soil-grown, light-shielded roots. We have developed image analysis algorithms that allow the spatial integration of soil properties, gene expression, and root system architecture traits. We propose GLO-Roots as a system that has great utility in presenting environmental stimuli to roots in ways that evoke natural adaptive responses and in providing tools for studying the multi-dimensional nature of such processes.

  View details for DOI 10.7554/eLife.07597

  View details for Web of Science ID 000373814300001

  View details for PubMedID 26287479

  View details for PubMedCentralID PMC4589753

• Low Sugar Is Not Always Good: Impact of Specific O-Glycan Defects on Tip Growth in Arabidopsis PLANT PHYSIOLOGY Velasquez, S. M., Marzol, E., Borassi, C., Pol-Fachin, L., Ricardi, M. M., Mangano, S., Denita Juarez, S. P., Salgado Salter, J. D., Gloazzo Dorosz, J., Marcus, S. E., Knox, J. P., Dinneny, J. R., Iusem, N. D., Verli, H., Estevez, J. M. 2015; 168 (3): 808-U918

  View details for DOI 10.1104/pp.114.255521

  View details for Web of Science ID 000359307600007

  View details for PubMedID 25944827

  View details for PubMedCentralID PMC4741341

• The divining root: moisture-driven responses of roots at the micro- and macro-scale JOURNAL OF EXPERIMENTAL BOTANY Robbins, N. E., Dinneny, J. R. 2015; 66 (8): 2145-2154

  Abstract

  Water is fundamental to plant life, but the mechanisms by which plant roots sense and respond to variations in water availability in the soil are poorly understood. Many studies of responses to water deficit have focused on large-scale effects of this stress, but have overlooked responses at the sub-organ or cellular level that give rise to emergent whole-plant phenotypes. We have recently discovered hydropatterning, an adaptive environmental response in which roots position new lateral branches according to the spatial distribution of available water across the circumferential axis. This discovery illustrates that roots are capable of sensing and responding to water availability at spatial scales far lower than those normally studied for such processes. This review will explore how roots respond to water availability with an emphasis on what is currently known at different spatial scales. Beginning at the micro-scale, there is a discussion of water physiology at the cellular level and proposed sensory mechanisms cells use to detect osmotic status. The implications of these principles are then explored in the context of cell and organ growth under non-stress and water-deficit conditions. Following this, several adaptive responses employed by roots to tailor their functionality to the local moisture environment are discussed, including patterning of lateral root development and generation of hydraulic barriers to limit water loss. We speculate that these micro-scale responses are necessary for optimal functionality of the root system in a heterogeneous moisture environment, allowing for efficient water uptake with minimal water loss during periods of drought.

  View details for DOI 10.1093/jxb/eru496

  View details for Web of Science ID 000353895000004

  View details for PubMedID 25617469

• Traversing organizational scales in plant salt-stress responses CURRENT OPINION IN PLANT BIOLOGY Dinneny, J. R. 2015; 23: 70-75

  Abstract

  Modern society has developed in large part due to our ability to reliably grow plants for food and renewable resources. Predicted increases in environmental variability will impact agricultural productivity and may have extensive secondary effects on the stability of our society. Thus, a concerted effort to understand plant response strategies to stress is needed. High salinity is an agriculturally important environmental stress and generates complex effects on the physiology of the plant. The abiotic-stress-associated hormone, abscisic acid (ABA), mediates a major component of this response. I highlight recent work studying salt-stress responses at different spatial and organizational scales from the action of ABA in specific cell types to global networks of proteins that predict critical regulatory events during acclimation.

  View details for DOI 10.1016/j.pbi.2014.10.009

  View details for Web of Science ID 000349880900011

  View details for PubMedID 25449729

• Salt-stress regulation of root system growth and architecture in Arabidopsis seedlings. Methods in molecular biology (Clifton, N.J.) Duan, L., Sebastian, J., Dinneny, J. R. 2015; 1242: 105-122

  Abstract

  In order to acclimate to the soil environment, plants need to constantly optimize their root system architecture for efficient resource uptake. Roots are highly sensitive to changes in their surrounding environment and root system responses to a stress such as salinity and drought can be very dynamic and complex in nature. These responses can be manifested differentially at the cellular, tissue, or organ level and between the types of roots in a root system. Therefore, various approaches must be taken to quantify and characterize these responses. In this chapter, we review methods to study basic root growth traits, such as root length, cell cycle activity and meristem size, cell shape and size that form the basis for the emergent properties of the root system. Methods for the detailed analysis of lateral root initiation and postemergence growth are described. Finally, several live-imaging systems, which allow for dynamic imaging of the root, will be explored. Together these tools provide insight into the regulatory steps that sculpt the root system upon environmental change and can be used as the basis for the evaluation of genetic variation affecting these pathways.

  View details for DOI 10.1007/978-1-4939-1902-4_10

  View details for PubMedID 25408448

• Beyond the Barrier: Communication in the Root through the Endodermis PLANT PHYSIOLOGY Robbins, N. E., Trontin, C., Duan, L., Dinneny, J. R. 2014; 166 (2): 551-559

  Abstract

  The root endodermis is characterized by the Casparian strip and by the suberin lamellae, two hydrophobic barriers that restrict the free diffusion of molecules between the inner cell layers of the root and the outer environment. The presence of these barriers and the position of the endodermis between the inner and outer parts of the root require that communication between these two domains acts through the endodermis. Recent work on hormone signaling, propagation of calcium waves, and plant-fungal symbiosis has provided evidence in support of the hypothesis that the endodermis acts as a signaling center. The endodermis is also a unique mechanical barrier to organogenesis, which must be overcome through chemical and mechanical cross talk between cell layers to allow for development of new lateral organs while maintaining its barrier functions. In this review, we discuss recent findings regarding these two important aspects of the endodermis.

  View details for DOI 10.1104/pp.114.244871

  View details for Web of Science ID 000345071500010

  View details for PubMedCentralID PMC4213087

• Beyond the barrier: communication in the root through the endodermis. Plant physiology Robbins, N. E., Trontin, C., Duan, L., Dinneny, J. R. 2014; 166 (2): 551-559

  Abstract

  The root endodermis is characterized by the Casparian strip and by the suberin lamellae, two hydrophobic barriers that restrict the free diffusion of molecules between the inner cell layers of the root and the outer environment. The presence of these barriers and the position of the endodermis between the inner and outer parts of the root require that communication between these two domains acts through the endodermis. Recent work on hormone signaling, propagation of calcium waves, and plant-fungal symbiosis has provided evidence in support of the hypothesis that the endodermis acts as a signaling center. The endodermis is also a unique mechanical barrier to organogenesis, which must be overcome through chemical and mechanical cross talk between cell layers to allow for development of new lateral organs while maintaining its barrier functions. In this review, we discuss recent findings regarding these two important aspects of the endodermis.

  View details for DOI 10.1104/pp.114.244871

  View details for PubMedID 25125504

• Plant roots use a patterning mechanism to position lateral root branches toward available water PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA Bao, Y., Aggarwal, P., Robbins, N. E., Sturrock, C. J., Thompson, M. C., Tan, H. Q., Tham, C., Duan, L., Rodriguez, P. L., Vernoux, T., Mooney, S. J., Bennett, M. J., Dinneny, J. R. 2014; 111 (25): 9319-9324

  Abstract

  The architecture of the branched root system of plants is a major determinant of vigor. Water availability is known to impact root physiology and growth; however, the spatial scale at which this stimulus influences root architecture is poorly understood. Here we reveal that differences in the availability of water across the circumferential axis of the root create spatial cues that determine the position of lateral root branches. We show that roots of several plant species can distinguish between a wet surface and air environments and that this also impacts the patterning of root hairs, anthocyanins, and aerenchyma in a phenomenon we describe as hydropatterning. This environmental response is distinct from a touch response and requires available water to induce lateral roots along a contacted surface. X-ray microscale computed tomography and 3D reconstruction of soil-grown root systems demonstrate that such responses also occur under physiologically relevant conditions. Using early-stage lateral root markers, we show that hydropatterning acts before the initiation stage and likely determines the circumferential position at which lateral root founder cells are specified. Hydropatterning is independent of endogenous abscisic acid signaling, distinguishing it from a classic water-stress response. Higher water availability induces the biosynthesis and transport of the lateral root-inductive signal auxin through local regulation of tryptophan aminotransferase of Arabidopsis 1 and PIN-formed 3, both of which are necessary for normal hydropatterning. Our work suggests that water availability is sensed and interpreted at the suborgan level and locally patterns a wide variety of developmental processes in the root.

  View details for DOI 10.1073/pnas.1400966111

  View details for Web of Science ID 000337760600071

  View details for PubMedCentralID PMC4078807

• Plant roots use a patterning mechanism to position lateral root branches toward available water. Proceedings of the National Academy of Sciences of the United States of America Bao, Y., Aggarwal, P., Robbins, N. E., Sturrock, C. J., Thompson, M. C., Tan, H. Q., Tham, C., Duan, L., Rodriguez, P. L., Vernoux, T., Mooney, S. J., Bennett, M. J., Dinneny, J. R. 2014; 111 (25): 9319-9324

  Abstract

  The architecture of the branched root system of plants is a major determinant of vigor. Water availability is known to impact root physiology and growth; however, the spatial scale at which this stimulus influences root architecture is poorly understood. Here we reveal that differences in the availability of water across the circumferential axis of the root create spatial cues that determine the position of lateral root branches. We show that roots of several plant species can distinguish between a wet surface and air environments and that this also impacts the patterning of root hairs, anthocyanins, and aerenchyma in a phenomenon we describe as hydropatterning. This environmental response is distinct from a touch response and requires available water to induce lateral roots along a contacted surface. X-ray microscale computed tomography and 3D reconstruction of soil-grown root systems demonstrate that such responses also occur under physiologically relevant conditions. Using early-stage lateral root markers, we show that hydropatterning acts before the initiation stage and likely determines the circumferential position at which lateral root founder cells are specified. Hydropatterning is independent of endogenous abscisic acid signaling, distinguishing it from a classic water-stress response. Higher water availability induces the biosynthesis and transport of the lateral root-inductive signal auxin through local regulation of tryptophan aminotransferase of Arabidopsis 1 and PIN-formed 3, both of which are necessary for normal hydropatterning. Our work suggests that water availability is sensed and interpreted at the suborgan level and locally patterns a wide variety of developmental processes in the root.

  View details for DOI 10.1073/pnas.1400966111

  View details for PubMedID 24927545

• Methods to Promote Germination of Dormant Setaria viridis Seeds PLOS ONE Sebastian, J., Wong, M. K., Tang, E., Dinneny, J. R. 2014; 9 (4)

  Abstract

  Setaria viridis has recently emerged as a promising genetic model system to study diverse aspects of monocot biology. While the post-germination life cycle of S. viridis is approximately 8 weeks long, the prolonged dormancy of freshly harvested seeds can more than double the total time required between successive generations. Here we describe methods that promote seed germination in S. viridis. Our results demonstrate that treating S. viridis seeds with liquid smoke or a GA3 and KNO3 solution improves germination rates to 90% or higher even in seeds that are 6 days post-harvest with similar results obtained whether seeds are planted in soil or on gel-based media. Importantly, we show that these treatments have no significant effect on the growth of the adult plant. We have tested these treatments on diverse S. viridis accessions and show variation in their response. The methods described here will help advance research using this model grass species by increasing the pace at which successive generations of plants can be analyzed.

  View details for DOI 10.1371/journal.pone.0095109

  View details for Web of Science ID 000335226500058

  View details for PubMedID 24748008

  View details for PubMedCentralID PMC3991590

• Circular RNA is expressed across the eukaryotic tree of life. PloS one Wang, P. L., Bao, Y., Yee, M., Barrett, S. P., Hogan, G. J., Olsen, M. N., Dinneny, J. R., Brown, P. O., Salzman, J. 2014; 9 (6)

  Abstract

  An unexpectedly large fraction of genes in metazoans (human, mouse, zebrafish, worm, fruit fly) express high levels of circularized RNAs containing canonical exons. Here we report that circular RNA isoforms are found in diverse species whose most recent common ancestor existed more than one billion years ago: fungi (Schizosaccharomyces pombe and Saccharomyces cerevisiae), a plant (Arabidopsis thaliana), and protists (Plasmodium falciparum and Dictyostelium discoideum). For all species studied to date, including those in this report, only a small fraction of the theoretically possible circular RNA isoforms from a given gene are actually observed. Unlike metazoans, Arabidopsis, D. discoideum, P. falciparum, S. cerevisiae, and S. pombe have very short introns (∼ 100 nucleotides or shorter), yet they still produce circular RNAs. A minority of genes in S. pombe and P. falciparum have documented examples of canonical alternative splicing, making it unlikely that all circular RNAs are by-products of alternative splicing or 'piggyback' on signals used in alternative RNA processing. In S. pombe, the relative abundance of circular to linear transcript isoforms changed in a gene-specific pattern during nitrogen starvation. Circular RNA may be an ancient, conserved feature of eukaryotic gene expression programs.

  View details for DOI 10.1371/journal.pone.0090859

  View details for PubMedID 24609083

  View details for PubMedCentralID PMC3946582

• A gateway with a guard: How the endodermis regulates growth through hormone signaling PLANT SCIENCE Dinneny, J. R. 2014; 214: 14-19

  Abstract

  The endodermis is a defining feature of plant roots and is most widely studied as a differentially permeable barrier limiting solute uptake from the soil into the vascular stream. Recent work has revealed that this inner cell layer is also an important signaling center for hormone-mediated control of growth. Auxin, gibberellic acid, abscisic acid and strigalactones all appear to depend on the endodermis to regulate root biology and point to this cell type as having important inter-cell layer regulatory activity, as well. In this review I discuss recent work detailing the importance of the endodermis in growth control and how this function is affected during responses to the environment.

  View details for DOI 10.1016/j.plantsci.2013.09.009

  View details for Web of Science ID 000328725700003

  View details for PubMedID 24268159

• Circular RNA Is Expressed across the Eukaryotic Tree of Life. PloS one Wang, P. L., Bao, Y., Yee, M., Barrett, S. P., Hogan, G. J., Olsen, M. N., Dinneny, J. R., Brown, P. O., Salzman, J. 2014; 9 (3)

  Abstract

  An unexpectedly large fraction of genes in metazoans (human, mouse, zebrafish, worm, fruit fly) express high levels of circularized RNAs containing canonical exons. Here we report that circular RNA isoforms are found in diverse species whose most recent common ancestor existed more than one billion years ago: fungi (Schizosaccharomyces pombe and Saccharomyces cerevisiae), a plant (Arabidopsis thaliana), and protists (Plasmodium falciparum and Dictyostelium discoideum). For all species studied to date, including those in this report, only a small fraction of the theoretically possible circular RNA isoforms from a given gene are actually observed. Unlike metazoans, Arabidopsis, D. discoideum, P. falciparum, S. cerevisiae, and S. pombe have very short introns (∼ 100 nucleotides or shorter), yet they still produce circular RNAs. A minority of genes in S. pombe and P. falciparum have documented examples of canonical alternative splicing, making it unlikely that all circular RNAs are by-products of alternative splicing or 'piggyback' on signals used in alternative RNA processing. In S. pombe, the relative abundance of circular to linear transcript isoforms changed in a gene-specific pattern during nitrogen starvation. Circular RNA may be an ancient, conserved feature of eukaryotic gene expression programs.

  View details for DOI 10.1371/journal.pone.0090859

  View details for PubMedID 24609083

  View details for PubMedCentralID PMC3946582

• A robust family of Golden Gate Agrobacterium vectors for plant synthetic biology FRONTIERS IN PLANT SCIENCE Emami, S., Yee, M., Dinneny, J. R. 2013; 4

  Abstract

  Tools that allow for rapid, accurate and inexpensive assembly of multi-component combinatorial libraries of DNA for transformation into plants will accelerate the progress of synthetic biology research. Recent innovations in molecular cloning methods has vastly expanded the repertoire with which plant biologists can engineer a transgene. Here we describe a new set of binary vectors for use in Agrobacterium-mediated plant transformation that utilizes the Golden-Gate Cloning approach. Our optimized protocol facilitates the rapid and inexpensive generation of multi-component transgenes for later introduction into plants.

  View details for DOI 10.3389/fpls.2013.00339

  View details for Web of Science ID 000331109300001

  View details for PubMedID 24032037

  View details for PubMedCentralID PMC3759027

• A Spatio-Temporal Understanding of Growth Regulation during the Salt Stress Response in Arabidopsis PLANT CELL Geng, Y., Wu, R., Wee, C. W., Xie, F., Wei, X., Chan, P. M., Tham, C., Duan, L., Dinneny, J. R. 2013; 25 (6): 2132-2154

  Abstract

  Plant environmental responses involve dynamic changes in growth and signaling, yet little is understood as to how progress through these events is regulated. Here, we explored the phenotypic and transcriptional events involved in the acclimation of the Arabidopsis thaliana seedling root to a rapid change in salinity. Using live-imaging analysis, we show that growth is dynamically regulated with a period of quiescence followed by recovery then homeostasis. Through the use of a new high-resolution spatio-temporal transcriptional map, we identify the key hormone signaling pathways that regulate specific transcriptional programs, predict their spatial domain of action, and link the activity of these pathways to the regulation of specific phases of growth. We use tissue-specific approaches to suppress the abscisic acid (ABA) signaling pathway and demonstrate that ABA likely acts in select tissue layers to regulate spatially localized transcriptional programs and promote growth recovery. Finally, we show that salt also regulates many tissue-specific and time point-specific transcriptional responses that are expected to modify water transport, Casparian strip formation, and protein translation. Together, our data reveal a sophisticated assortment of regulatory programs acting together to coordinate spatially patterned biological changes involved in the immediate and long-term response to a stressful shift in environment.

  View details for DOI 10.1105/tpc.113.112896

  View details for Web of Science ID 000322371500020

  View details for PubMedID 23898029

  View details for PubMedCentralID PMC3723617

• Endodermal ABA Signaling Promotes Lateral Root Quiescence during Salt Stress in Arabidopsis Seedlings PLANT CELL Duan, L., Dietrich, D., Ng, C. H., Chan, P. M., Bhalerao, R., Bennett, M. J., Dinneny, J. R. 2013; 25 (1): 324-341

  Abstract

  The endodermal tissue layer is found in the roots of vascular plants and functions as a semipermeable barrier, regulating the transport of solutes from the soil into the vascular stream. As a gateway for solutes, the endodermis may also serve as an important site for sensing and responding to useful or toxic substances in the environment. Here, we show that high salinity, an environmental stress widely impacting agricultural land, regulates growth of the seedling root system through a signaling network operating primarily in the endodermis. We report that salt stress induces an extended quiescent phase in postemergence lateral roots (LRs) whereby the rate of growth is suppressed for several days before recovery begins. Quiescence is correlated with sustained abscisic acid (ABA) response in LRs and is dependent upon genes necessary for ABA biosynthesis, signaling, and transcriptional regulation. We use a tissue-specific strategy to identify the key cell layers where ABA signaling acts to regulate growth. In the endodermis, misexpression of the ABA insensitive1-1 mutant protein, which dominantly inhibits ABA signaling, leads to a substantial recovery in LR growth under salt stress conditions. Gibberellic acid signaling, which antagonizes the ABA pathway, also acts primarily in the endodermis, and we define the crosstalk between these two hormones. Our results identify the endodermis as a gateway with an ABA-dependent guard, which prevents root growth into saline environments.

  View details for DOI 10.1105/tpc.112.107227

  View details for Web of Science ID 000315572400025

  View details for PubMedID 23341337

  View details for PubMedCentralID PMC3584545