What is quantitative plant biology?

Abstract Quantitative plant biology is an interdisciplinary field that builds on a long history of biomathematics and biophysics. Today, thanks to high spatiotemporal resolution tools and computational modelling, it sets a new standard in plant science. Acquired data, whether molecular, geometric or mechanical, are quantified, statistically assessed and integrated at multiple scales and across fields. They feed testable predictions that, in turn, guide further experimental tests. Quantitative features such as variability, noise, robustness, delays or feedback loops are included to account for the inner dynamics of plants and their interactions with the environment. Here, we present the main features of this ongoing revolution, through new questions around signalling networks, tissue topology, shape plasticity, biomechanics, bioenergetics, ecology and engineering. In the end, quantitative plant biology allows us to question and better understand our interactions with plants. In turn, this field opens the door to transdisciplinary projects with the society, notably through citizen science.

[1]  J. Timmer,et al.  An Integrative Model for Phytochrome B Mediated Photomorphogenesis: From Protein Dynamics to Physiology , 2010, PloS one.

[2]  J. Ortega Augmented growth equation for cell wall expansion. , 1985, Plant physiology.

[3]  Natalie M. Clark,et al.  Protein complex stoichiometry and expression dynamics of transcription factors modulate stem cell division , 2020, Proceedings of the National Academy of Sciences.

[4]  E. Schäfer,et al.  Systematic analysis of how phytochrome B dimerization determines its specificity , 2015, Nature Plants.

[5]  Bruno Moulia,et al.  Wind loads and competition for light sculpt trees into self-similar structures , 2017, Nature Communications.

[6]  René de Jesús Romero-Troncoso,et al.  Instrumentation in Developing Chlorophyll Fluorescence Biosensing: A Review , 2012, Sensors.

[7]  Andrey Alexeyenko,et al.  Spatially resolved transcriptome profiling in model plant species , 2017, Nature Plants.

[8]  O. Hamant,et al.  The contribution of mechanosensing to epidermal cell fate specification. , 2018, Current opinion in genetics & development.

[9]  A. J. Koo,et al.  Glutamate triggers long-distance, calcium-based plant defense signaling , 2018, Science.

[10]  Christian Fankhauser,et al.  Sensing the light environment in plants: photoreceptors and early signaling steps , 2015, Current Opinion in Neurobiology.

[11]  E. Scarpella,et al.  Coordination of tissue cell polarity by auxin transport and signaling , 2019, bioRxiv.

[12]  E. Menges Stochastic Modeling of Extinction in Plant Populations , 1992 .

[13]  P. B. Green,et al.  Expression of pattern in plants: combining molecular and calculus-based biophysical paradigms. , 1999, American journal of botany.

[14]  S. Schwendener,et al.  Das mechanische Princip in anatomischen Bau der Monocotylen : mit vergleichenden Ausblicken auf übrigen Pflanzenklassen / , 1874 .

[15]  G. Vinnicombe,et al.  Fundamental limits on the suppression of molecular fluctuations , 2010, Nature.

[16]  G. Lahav,et al.  Encoding and Decoding Cellular Information through Signaling Dynamics , 2013, Cell.

[17]  Bharat Bhushan,et al.  Multifunctional surface structures of plants: An inspiration for biomimetics , 2009 .

[18]  R. Terauchi,et al.  The NB‐LRR proteins RGA4 and RGA5 interact functionally and physically to confer disease resistance , 2014, The EMBO journal.

[19]  Daphne Ezer,et al.  A mass participatory experiment provides a rich temporal profile of temperature response in spring onions , 2019, Plant direct.

[20]  S. Mooney,et al.  Plant roots use a patterning mechanism to position lateral root branches toward available water , 2014, Proceedings of the National Academy of Sciences.

[21]  J. Traas,et al.  Force-Driven Polymerization and Turgor-Induced Wall Expansion. , 2016, Trends in plant science.

[22]  A J Pons,et al.  Integration of cellular signals in chattering environments. , 2011, Progress in biophysics and molecular biology.

[23]  Eric N. Cytrynbaum,et al.  Mechanisms of Self-Organization of Cortical Microtubules in Plants Revealed by Computational Simulations , 2010, Molecular biology of the cell.

[24]  C. Fleck,et al.  Shedding (far-red) light on phytochrome mechanisms and responses in land plants. , 2014, Plant science : an international journal of experimental plant biology.

[25]  Alfredo R. Huete,et al.  Leaf development and demography explain photosynthetic seasonality in Amazon evergreen forests , 2016, Science.

[26]  D. Mccloskey,et al.  The Cult of Statistical Significance: How the Standard Error Costs Us Jobs, Justice, and Lives , 2008 .

[27]  P. Wigge,et al.  Ambient temperature signalling in plants. , 2013, Current opinion in plant biology.

[28]  G. Malandain,et al.  A multiscale analysis of early flower development in Arabidopsis provides an integrated view of molecular regulation and growth control , 2020, bioRxiv.

[29]  J. Boyer,et al.  Turgor, temperature and the growth of plant cells: using Chara corallina as a model system. , 2000, Journal of experimental botany.

[30]  Siobhan M Brady,et al.  Systems approaches to identifying gene regulatory networks in plants. , 2008, Annual review of cell and developmental biology.

[31]  T. Imaizumi,et al.  Dawn and photoperiod sensing by phytochrome A , 2018, Proceedings of the National Academy of Sciences.

[32]  M. Fournier,et al.  Integrative biomechanics for tree ecology: beyond wood density and strength. , 2013, Journal of experimental botany.

[33]  J. C. Ambrose,et al.  Spatial organization of plant cortical microtubules: close encounters of the 2D kind. , 2009, Trends in cell biology.

[34]  Yuling Jiao,et al.  Epidermal restriction confers robustness to organ shapes. , 2020, Journal of integrative plant biology.

[35]  Y. Guédon,et al.  Lateral Roots: Random Diversity in Adversity. , 2019, Trends in plant science.

[36]  C. Waddington Canalization of Development and the Inheritance of Acquired Characters , 1942, Nature.

[37]  O. Hamant,et al.  Alignment between PIN1 Polarity and Microtubule Orientation in the Shoot Apical Meristem Reveals a Tight Coupling between Morphogenesis and Auxin Transport , 2010, PLoS biology.

[38]  M. S. Mukhtar,et al.  Independently Evolved Virulence Effectors Converge onto Hubs in a Plant Immune System Network , 2011, Science.

[39]  Ignazio Maria Viola,et al.  A separated vortex ring underlies the flight of the dandelion , 2018, Nature.

[40]  Dafyd J. Jenkins,et al.  Changes in Gene Expression in Space and Time Orchestrate Environmentally Mediated Shaping of Root Architecture[CC-BY] , 2017, Plant Cell.

[41]  D. R. Kaplan The Relationship of Cells to Organisms in Plants: Problem and Implications of an Organismal Perspective , 1992, International Journal of Plant Sciences.

[42]  K. C. Huang,et al.  Cell size and growth regulation in the Arabidopsis thaliana apical stem cell niche , 2016, Proceedings of the National Academy of Sciences.

[43]  Zygmunt Hejnowicz,et al.  Growth tensor of plant organs , 1984 .

[44]  K. Porter,et al.  A "MICROTUBULE" IN PLANT CELL FINE STRUCTURE , 1963, The Journal of cell biology.

[45]  Iain G. Johnston,et al.  Temperature variability is integrated by a spatially embedded decision-making center to break dormancy in Arabidopsis seeds , 2017, Proceedings of the National Academy of Sciences.

[46]  Tjelvar S. G. Olsson,et al.  A method for detecting single mRNA molecules in Arabidopsis thaliana , 2016, Plant Methods.

[47]  D. Fell,et al.  A Diel Flux Balance Model Captures Interactions between Light and Dark Metabolism during Day-Night Cycles in C3 and Crassulacean Acid Metabolism Leaves1[C][W][OPEN] , 2014, Plant Physiology.

[48]  O. Hamant,et al.  How Mechanical Forces Shape Plant Organs , 2021, Current Biology.

[49]  L. Tsimring Noise in biology , 2014, Reports on progress in physics. Physical Society.

[50]  J. Timmer,et al.  Photoconversion and Nuclear Trafficking Cycles Determine Phytochrome A's Response Profile to Far-Red Light , 2011, Cell.

[51]  Victor Thiessen Stephen T. Ziliak and Deirdre N. McCloskey, The Cult of Statistical Significance: How the Standard Error Costs us Jobs, Justice, and Lives. , 2009 .

[52]  O. Hamant,et al.  Mechanical Shielding of Rapidly Growing Cells Buffers Growth Heterogeneity and Contributes to Organ Shape Reproducibility , 2017, Current Biology.

[53]  Karl J. Niklas,et al.  Plant Biomechanics: An Engineering Approach to Plant Form and Function , 1993 .

[54]  Arezki Boudaoud,et al.  Mechanical Regulation of Auxin-Mediated Growth , 2012, Current Biology.

[55]  G. Krouk,et al.  Network Walking charts transcriptional dynamics of nitrogen signaling by integrating validated and predicted genome-wide interactions , 2019, Nature Communications.

[56]  Benoit Landrein,et al.  Mechanical Stress Acts via Katanin to Amplify Differences in Growth Rate between Adjacent Cells in Arabidopsis , 2012, Cell.

[57]  Daphne Ezer,et al.  The G-box transcriptional regulatory code in Arabidopsis , 2017, bioRxiv.

[58]  D. Bergmann,et al.  Cell-type–specific transcriptome and histone modification dynamics during cellular reprogramming in the Arabidopsis stomatal lineage , 2019, Proceedings of the National Academy of Sciences.

[59]  D. Ehrhardt,et al.  Visualization of Cellulose Synthase Demonstrates Functional Association with Microtubules , 2006, Science.

[60]  Jonathan D. G. Jones,et al.  The highly buffered Arabidopsis immune signaling network conceals the functions of its components , 2017, PLoS genetics.

[61]  Z. Hejnowicz Plants as Mechano-Osmotic Transducers , 2011 .

[62]  E. Deinum,et al.  Modelling the role of microtubules in plant cell morphology. , 2013, Current opinion in plant biology.

[63]  Haiqing Wei,et al.  Fundamental Limits of , 2010 .

[64]  J. Locke,et al.  Developmental mechanisms underlying variable, invariant and plastic phenotypes. , 2016, Annals of botany.

[65]  Daisuke Kurihara,et al.  Live-cell imaging and optical manipulation of Arabidopsis early embryogenesis. , 2015, Developmental cell.

[66]  K. Franklin Light and temperature signal crosstalk in plant development. , 2009, Current opinion in plant biology.

[67]  Rebecca A. Ayers,et al.  Structure and function of plant photoreceptors. , 2010, Annual review of plant biology.

[68]  T. J. Cooke,et al.  The genius of Wilhelm Hofmeister: the origin of causal‐analytical research in plant development , 1996 .

[69]  D. Chitwood,et al.  Evolutionary and Environmental Forces Sculpting Leaf Development , 2016, Current Biology.

[70]  E. Neumann,et al.  Arabidopsis Kinetochore Fiber-Associated MAP65-4 Cross-Links Microtubules and Promotes Microtubule Bundle Elongation[W][OA] , 2010, Plant Cell.

[71]  G. Van Isterdael,et al.  CRISPR-TSKO: A Technique for Efficient Mutagenesis in Specific Cell Types, Tissues, or Organs in Arabidopsis[OPEN] , 2019, Plant Cell.

[72]  Christophe Godin,et al.  Lateral root morphogenesis is dependent on the mechanical properties of the overlaying tissues , 2013, Proceedings of the National Academy of Sciences.

[73]  Rainer Breitling,et al.  A transatlantic perspective on 20 emerging issues in biological engineering , 2017, eLife.

[74]  R. O. Erickson Modeling of Plant Growth , 1976 .

[75]  Daphne Ezer,et al.  NITPicker: selecting time points for follow-up experiments , 2019, BMC Bioinformatics.

[76]  Daniel J. Kliebenstein,et al.  Genomic Analysis of QTLs and Genes Altering Natural Variation in Stochastic Noise , 2011, PLoS genetics.

[77]  Yosef Yarden,et al.  Feedback regulation of EGFR signalling: decision making by early and delayed loops , 2011, Nature Reviews Molecular Cell Biology.

[78]  J. Ioannidis Why Most Published Research Findings Are False , 2005, PLoS medicine.

[79]  L. Mahadevan,et al.  How the Venus flytrap snaps , 2005, Nature.

[80]  Ulrich Kutschera,et al.  Tissue stresses in growing plant organs , 1989 .

[81]  Christian Rogers,et al.  Standards for plant synthetic biology: a common syntax for exchange of DNA parts. , 2015, The New phytologist.

[82]  Coordination of tissue cell polarity by auxin transport and signaling , 2019, eLife.

[83]  Zygmunt Hejnowicz,et al.  Tissue stresses in organs of herbaceous plants III. Elastic properties of the tissues of sunflowers hypocotyl and origin of tissue stresses , 1996 .

[84]  James C. W. Locke,et al.  Light inputs shape the Arabidopsis circadian system. , 2011, The Plant journal : for cell and molecular biology.

[85]  Li Yang,et al.  Convergent targeting of a common host protein-network by pathogen effectors from three kingdoms of life. , 2014, Cell host & microbe.

[86]  Peng Wang,et al.  Finding the genes to build C4 rice. , 2016, Current opinion in plant biology.

[87]  Stéphane Douady,et al.  Fluttering of growing leaves as a way to reach flatness: experimental evidence on Persea americana , 2018, Journal of The Royal Society Interface.

[88]  P B Green Transductions to generate plant form and pattern: an essay on cause and effect. , 1997, Gravitational and space biology bulletin : publication of the American Society for Gravitational and Space Biology.

[89]  Katja E. Jaeger,et al.  The G-Box Transcriptional Regulatory Code in Arabidopsis1[OPEN] , 2017, Plant Physiology.

[90]  From plasmodesma geometry to effective symplasmic permeability through biophysical modelling , 2019, eLife.

[91]  Douglas G. Scofield,et al.  The Norway spruce genome sequence and conifer genome evolution , 2013, Nature.

[92]  Gabriel Krouk,et al.  Reverse engineering highlights potential principles of large gene regulatory network design and learning , 2017, npj Systems Biology and Applications.

[93]  R. Furbank,et al.  Explainable machine learning models of major crop traits from satellite-monitored continent-wide field trial data , 2021, Nature Plants.

[94]  Guillaume Cerutti,et al.  Temporal integration of auxin information for the regulation of patterning , 2020, eLife.

[95]  Eberhard Schäfer,et al.  A new approach to explain the “high irradiance responses” of photomorphogenesis on the basis of phytochrome , 1975 .

[96]  Malia A. Gehan,et al.  Temporal network analysis identifies early physiological and transcriptomic indicators of mild drought in Brassica rapa , 2017, eLife.

[97]  Przemyslaw Prusinkiewicz,et al.  Lindenmayer Systems, Fractals, and Plants , 1989, Lecture Notes in Biomathematics.

[98]  T. Dresselhaus,et al.  Does Early Embryogenesis in Eudicots and Monocots Involve the Same Mechanism and Molecular Players?1[OPEN] , 2016, Plant Physiology.

[99]  T. Bohr,et al.  Unifying model of shoot gravitropism reveals proprioception as a central feature of posture control in plants , 2012, Proceedings of the National Academy of Sciences.

[100]  Emma M. Keizer,et al.  Stochastic gene expression in Arabidopsis thaliana , 2017, Nature Communications.

[101]  J. Berry,et al.  A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species , 1980, Planta.

[102]  P. J. Andralojc,et al.  Rubisco activity and regulation as targets for crop improvement. , 2013, Journal of experimental botany.

[103]  Philippe Andrey,et al.  Cell geometry determines symmetric and asymmetric division plane selection in Arabidopsis early embryos , 2019, PLoS Comput. Biol..

[104]  Michele Meroni,et al.  Estimating and understanding crop yields with explainable deep learning in the Indian Wheat Belt , 2020, Environmental Research Letters.

[105]  J. Napier,et al.  Understanding and manipulating plant lipid composition: Metabolic engineering leads the way , 2014, Current opinion in plant biology.

[106]  J. Lockhart An analysis of irreversible plant cell elongation. , 1965, Journal of theoretical biology.

[107]  B. Scheres,et al.  Geometric cues forecast the switch from two‐ to three‐dimensional growth in Physcomitrella patens , 2019, The New phytologist.

[108]  Ari Pekka Mähönen,et al.  An inducible genome editing system for plants , 2019, bioRxiv.

[109]  Liping Gao,et al.  The long-term maintenance of a resistance polymorphism through diffuse interactions , 2014, Nature.

[110]  R. Steuer,et al.  Elucidating temporal resource allocation and diurnal dynamics in phototrophic metabolism using conditional FBA , 2015, Scientific Reports.

[111]  H. Leitte,et al.  Rules and Self-Organizing Properties of Post-embryonic Plant Organ Cell Division Patterns , 2016, Current Biology.

[112]  Stefano Ermon,et al.  Deep Transfer Learning for Crop Yield Prediction with Remote Sensing Data , 2018, COMPASS.

[113]  P. Koumoutsakos,et al.  MorphoGraphX: A platform for quantifying morphogenesis in 4D , 2015, eLife.

[114]  Bandan Chakrabortty,et al.  A Plausible Microtubule-Based Mechanism for Cell Division Orientation in Plant Embryogenesis , 2018, Current Biology.

[115]  C. Godin,et al.  Microtubule-Mediated Wall Anisotropy Contributes to Leaf Blade Flattening , 2020, Current Biology.

[116]  Y. Couder,et al.  Developmental Patterning by Mechanical Signals in Arabidopsis , 2009 .

[117]  Natalie M. Clark,et al.  Tracking transcription factor mobility and interaction in Arabidopsis roots with fluorescence correlation spectroscopy , 2016, eLife.

[118]  Iain G. Johnston,et al.  Identification of a bet-hedging network motif generating noise in hormone concentrations and germination propensity in Arabidopsis , 2018, Journal of The Royal Society Interface.

[119]  E Prabhu,et al.  Deep Learning and IoT for Smart Agriculture Using WSN , 2017, 2017 IEEE International Conference on Computational Intelligence and Computing Research (ICCIC).

[120]  Yasmine Meroz,et al.  Stochastic processes in gravitropism , 2014, Front. Plant Sci..

[121]  J. Hillston,et al.  Stochastic properties of the plant circadian clock , 2012, Journal of The Royal Society Interface.

[122]  Karsten M. Borgwardt,et al.  1,135 Genomes Reveal the Global Pattern of Polymorphism in Arabidopsis thaliana , 2016, Cell.

[123]  P. Lintilhac,et al.  Mechanical signals in plant development: a new method for single cell studies. , 1997, Developmental biology.

[124]  W. Silk,et al.  Quantitative Descriptions of Development , 1984 .

[125]  Ari Löytynoja,et al.  An inducible genome editing system for plants , 2020, Nature Plants.

[126]  Enrique Castano,et al.  Transcriptomics and co-expression networks reveal tissue-specific responses and regulatory hubs under mild and severe drought in papaya (Carica papaya L.) , 2018, Scientific Reports.

[127]  Klaus Palme,et al.  Mechanical induction of lateral root initiation in Arabidopsis thaliana , 2008, Proceedings of the National Academy of Sciences.

[128]  Emma Saxon Beyond bar charts , 2015, BMC Biology.

[129]  Fred A. Hamprecht,et al.  Accurate and versatile 3D segmentation of plant tissues at cellular resolution , 2020, bioRxiv.

[130]  O. Hamant,et al.  Heterogeneity and Robustness in Plant Morphogenesis: From Cells to Organs. , 2018, Annual review of plant biology.

[131]  A. Trewavas Information, Noise and Communication: Thresholds as Controlling Elements in Development , 2012 .

[132]  E. Schäfer,et al.  Phytochrome B integrates light and temperature signals in Arabidopsis , 2016, Science.

[133]  Z. Jeffrey Chen,et al.  Stochastic and Epigenetic Changes of Gene Expression in Arabidopsis Polyploids , 2004, Genetics.

[134]  E. Stelzer,et al.  A Spatial Accommodation by Neighboring Cells Is Required for Organ Initiation in Arabidopsis , 2014, Science.

[135]  Barbara Mazzolai,et al.  Taking inspiration from climbing plants: methodologies and benchmarks—a review , 2020, Bioinspiration & biomimetics.

[136]  George W Bassel,et al.  Information Processing and Distributed Computation in Plant Organs. , 2018, Trends in plant science.

[137]  P. Prusinkiewicz,et al.  Genetic control of plant development by overriding a geometric division rule. , 2014, Developmental cell.

[138]  O. Hamant,et al.  Variable Cell Growth Yields Reproducible OrganDevelopment through Spatiotemporal Averaging. , 2016, Developmental cell.

[139]  T. Higashiyama,et al.  Polar vacuolar distribution is essential for accurate asymmetric division of Arabidopsis zygotes , 2019, Proceedings of the National Academy of Sciences.

[140]  Meng Chen,et al.  Light signal transduction in higher plants. , 2004, Annual review of genetics.

[141]  Boris N. Kholodenko,et al.  Signalling ballet in space and time , 2010, Nature Reviews Molecular Cell Biology.

[142]  Stefano Chessa,et al.  Bayesian Sigmoid-Type Time Series Forecasting with Missing Data for Greenhouse Crops , 2020, Sensors.

[143]  Hugh C. Woolfenden,et al.  A computational approach for inferring the cell wall properties that govern guard cell dynamics , 2017, The Plant journal : for cell and molecular biology.

[144]  Zygmunt Hejnowicz,et al.  Plant Structure: Function and Development , 2004 .

[145]  V. Walbot,et al.  Defining the developmental program leading to meiosis in maize , 2018, Science.

[146]  Martin Bringmann,et al.  Tissue-wide Mechanical Forces Influence the Polarity of Stomatal Stem Cells in Arabidopsis , 2017, Current Biology.

[147]  Amilcare Porporato,et al.  Stochastic Dynamics of Plant-Water Interactions , 2007 .

[148]  Paul T. Tarr,et al.  An epidermis-driven mechanism positions and scales stem cell niches in plants , 2016, Science Advances.

[149]  F. Katagiri,et al.  Comparing signaling mechanisms engaged in pattern-triggered and effector-triggered immunity. , 2010, Current opinion in plant biology.

[150]  C. Fankhauser,et al.  Light-regulated plant growth and development. , 2010, Current topics in developmental biology.

[151]  K. T. ten Tusscher,et al.  Modeling of Root Nitrate Responses Suggests Preferential Foraging Arises From the Integration of Demand, Supply and Local Presence Signals , 2019, bioRxiv.

[152]  Allen L. King,et al.  A Mechanism for the Origin of Specifically Oriented Textures in Development with Special Reference to Nitella Wall Texture , 1966 .

[153]  Evolution: Tooth structure re-engineered , 2014, Nature.

[154]  Sascha Ott,et al.  Wigwams: identifying gene modules co-regulated across multiple biological conditions , 2013, Bioinform..

[155]  S. Kamoun,et al.  NLR singletons, pairs, and networks: evolution, assembly, and regulation of the intracellular immunoreceptor circuitry of plants. , 2019, Current opinion in plant biology.

[156]  Drew Endy,et al.  Opening options for material transfer , 2018, Nature Biotechnology.

[157]  E. Huq,et al.  Plant photoreceptors: Multi-functional sensory proteins and their signaling networks. , 2019, Seminars in cell & developmental biology.

[158]  James C. W. Locke,et al.  Fluctuations of the transcription factor ATML1 generate the pattern of giant cells in the Arabidopsis sepal , 2017, eLife.

[159]  She Chen,et al.  The Decoy Substrate of a Pathogen Effector and a Pseudokinase Specify Pathogen-Induced Modified-Self Recognition and Immunity in Plants. , 2015, Cell host & microbe.

[160]  R. Satija,et al.  Root Regeneration Triggers an Embryo-like Sequence Guided by Hormonal Interactions , 2016, Cell.

[161]  Guillaume Lobet,et al.  GLO-Roots: an imaging platform enabling multidimensional characterization of soil-grown root systems , 2015, bioRxiv.

[162]  K. Oparka,et al.  Controlling intercellular flow through mechanosensitive plasmodesmata nanopores , 2019, Nature Communications.

[163]  R. Morris,et al.  A ROS-Assisted Calcium Wave Dependent on the AtRBOHD NADPH Oxidase and TPC1 Cation Channel Propagates the Systemic Response to Salt Stress1[OPEN] , 2016, Plant Physiology.

[164]  Ruben Garrido-Oter,et al.  Interplay Between Innate Immunity and the Plant Microbiota. , 2017, Annual review of phytopathology.

[165]  Yoselin Benitez-Alfonso,et al.  From plasmodesma geometry to effective symplasmic permeability through biophysical modelling , 2019, bioRxiv.

[166]  Jonathan D. G. Jones,et al.  Structural Basis for Assembly and Function of a Heterodimeric Plant Immune Receptor , 2014, Science.

[167]  P B Green,et al.  Mechanism for Plant Cellular Morphogenesis , 1962, Science.

[168]  Przemyslaw Prusinkiewicz,et al.  MAppleT: simulation of apple tree development using mixed stochastic and biomechanical models. , 2008, Functional plant biology : FPB.

[169]  M. Kellner,et al.  MicroRNA Dynamics and Functions During Arabidopsis Embryogenesis , 2019, Plant Cell.

[170]  G. Bassel,et al.  Global Topological Order Emerges through Local Mechanical Control of Cell Divisions in the Arabidopsis Shoot Apical Meristem , 2019, Cell systems.

[171]  James C. W. Locke,et al.  Phytochromes function as thermosensors in Arabidopsis , 2016, Science.

[172]  D. Bouchez,et al.  Normal differentiation patterns in plants lacking microtubular preprophase bands , 1995, Nature.

[173]  EVOLUTION IN THE REAL WORLD: STOCHASTIC VARIATION AND THE DETERMINANTS OF FITNESS IN CARLINA VULGARIS , 2002, Evolution; international journal of organic evolution.

[174]  Ari Pekka Mähönen,et al.  ELIMÄKI Locus Is Required for Vertical Proprioceptive Response in Birch Trees , 2020, Current Biology.

[175]  Nathaniel K. Newlands,et al.  An integrated, probabilistic model for improved seasonal forecasting of agricultural crop yield under environmental uncertainty , 2014, Front. Environ. Sci..

[176]  J Dumais,et al.  The Fern Sporangium: A Unique Catapult , 2012, Science.

[177]  Keara A Franklin,et al.  Phytochrome A is an irradiance-dependent red light sensor. , 2007, The Plant journal : for cell and molecular biology.

[178]  James A.H. Murray,et al.  A Bistable Circuit Involving SCARECROW-RETINOBLASTOMA Integrates Cues to Inform Asymmetric Stem Cell Division , 2012, Cell.

[179]  Sandra Pelletier,et al.  A Receptor-like Kinase Mediates the Response of Arabidopsis Cells to the Inhibition of Cellulose Synthesis , 2007, Current Biology.