Information Integration and Communication in Plant Growth Regulation

Plants are equipped with the capacity to respond to a large number of diverse signals, both internal ones and those emanating from the environment, that are critical to their survival and adaption as sessile organisms. These signals need to be integrated through highly structured intracellular networks to ensure coherent cellular responses, and in addition, spatiotemporal actions of hormones and peptides both orchestrate local cell differentiation and coordinate growth and physiology over long distances. Further, signal interactions and signaling outputs vary significantly with developmental context. This review discusses our current understanding of the integrated intracellular and intercellular signaling networks that control plant growth.

[1]  M. R. Thorpe,et al.  Jasmonic acid induces rapid changes in carbon transport and partitioning in Populus. , 2005, The New phytologist.

[2]  Eunkyoo Oh,et al.  Cell elongation is regulated through a central circuit of interacting transcription factors in the Arabidopsis hypocotyl , 2014, eLife.

[3]  Zhi-Yong Wang,et al.  The brassinosteroid signaling network-a paradigm of signal integration. , 2014, Current opinion in plant biology.

[4]  C. Ballaré,et al.  Cryptochrome 1 and phytochrome B control shade-avoidance responses in Arabidopsis via partially independent hormonal cascades , 2011, The Plant journal : for cell and molecular biology.

[5]  Jonathan Legrand,et al.  A fluorescent hormone biosensor reveals the dynamics of jasmonate signalling in plants , 2015, Nature Communications.

[6]  Xingliang Hou,et al.  DELLAs modulate jasmonate signaling via competitive binding to JAZs. , 2010, Developmental cell.

[7]  S. Prat,et al.  PIFs get BRright: PHYTOCHROME INTERACTING FACTORs as integrators of light and hormonal signals. , 2014, The New phytologist.

[8]  S. Fujiwara,et al.  A Triantagonistic Basic Helix-Loop-Helix System Regulates Cell Elongation in Arabidopsis[W][OA] , 2012, Plant Cell.

[9]  X. Deng,et al.  Plant hormone jasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade , 2012, Proceedings of the National Academy of Sciences.

[10]  X. Deng,et al.  The Photomorphogenic Repressors Cop1 and Det1: 20 Years Later , 2022 .

[11]  P. He,et al.  Inverse modulation of plant immune and brassinosteroid signaling pathways by the receptor-like cytoplasmic kinase BIK1 , 2013, Proceedings of the National Academy of Sciences.

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

[13]  T. Soyano,et al.  NODULE INCEPTION creates a long-distance negative feedback loop involved in homeostatic regulation of nodule organ production , 2014, Proceedings of the National Academy of Sciences.

[14]  Joanne Chory,et al.  Rapid Synthesis of Auxin via a New Tryptophan-Dependent Pathway Is Required for Shade Avoidance in Plants , 2008, Cell.

[15]  Zhi-Yong Wang,et al.  Brassinosteroid signal transduction from receptor kinases to transcription factors. , 2010, Annual review of plant biology.

[16]  Y. Matsubayashi,et al.  Root-derived CLE glycopeptides control nodulation by direct binding to HAR1 receptor kinase , 2013, Nature Communications.

[17]  Teva Vernoux,et al.  Comparison of plant hormone signalling systems. , 2015, Essays in biochemistry.

[18]  J. Sheen,et al.  Glucose–TOR signalling reprograms the transcriptome and activates meristems , 2013, Nature.

[19]  Robert J. Schmitz,et al.  Linking photoreceptor excitation to changes in plant architecture. , 2012, Genes & development.

[20]  C. Wasternack,et al.  Jasmonate signaling and crosstalk with gibberellin and ethylene. , 2014, Current opinion in plant biology.

[21]  Ling Zhu,et al.  SCAR Mediates Light-Induced Root Elongation in Arabidopsis through Photoreceptors and Proteasomes[W][OA] , 2011, Plant Cell.

[22]  Michael P. Pound,et al.  Systems Analysis of Auxin Transport in the Arabidopsis Root Apex[W][OPEN] , 2014, Plant Cell.

[23]  G. Jenkins,et al.  UV-B detected by the UVR8 photoreceptor antagonizes auxin signaling and plant shade avoidance , 2014, Proceedings of the National Academy of Sciences.

[24]  R. Pierik,et al.  Auxin transport through PIN-FORMED 3 (PIN3) controls shade avoidance and fitness during competition , 2010, Proceedings of the National Academy of Sciences.

[25]  Cristina N Butterfield,et al.  Development and Stem Cells Research Article , 2022 .

[26]  T. Sun,et al.  Brassinosteroid, gibberellin, and phytochrome impinge on a common transcription module in Arabidopsis , 2012, Nature Cell Biology.

[27]  Ana I. Caño-Delgado,et al.  Brassinosteroids control meristem size by promoting cell cycle progression in Arabidopsis roots , 2011, Development.

[28]  Karolina M. Pajerowska-Mukhtar,et al.  Salicylic Acid Inhibits Pathogen Growth in Plants through Repression of the Auxin Signaling Pathway , 2007, Current Biology.

[29]  Jonathan D. G. Jones,et al.  A Plant miRNA Contributes to Antibacterial Resistance by Repressing Auxin Signaling , 2006, Science.

[30]  C. Zipfel,et al.  Trade-off between growth and immunity: role of brassinosteroids. , 2015, Trends in plant science.

[31]  P. Quail,et al.  A Molecular Framework of Light-Controlled Phytohormone Action in Arabidopsis , 2012, Current Biology.

[32]  Y. Matsubayashi,et al.  Perception of root-derived peptides by shoot LRR-RKs mediates systemic N-demand signaling , 2014, Science.

[33]  Christian Fankhauser,et al.  Contrasting growth responses in lamina and petiole during neighbor detection depend on differential auxin responsiveness rather than different auxin levels. , 2015, The New phytologist.

[34]  Aditi Gupta,et al.  Interaction between Glucose and Brassinosteroid during the Regulation of Lateral Root Development in Arabidopsis1 , 2015, Plant Physiology.

[35]  C. Fankhauser,et al.  Auxin-mediated plant architectural changes in response to shade and high temperature. , 2014, Physiologia plantarum.

[36]  Eunkyoo Oh,et al.  Interaction between BZR1 and PIF4 integrates brassinosteroid and environmental responses , 2012, Nature Cell Biology.

[37]  J. Kieber,et al.  Ethylene Inhibits Cell Proliferation of the Arabidopsis Root Meristem1[OPEN] , 2015, Plant Physiology.

[38]  J. Chory,et al.  Phytochrome signaling mechanisms and the control of plant development. , 2011, Trends in cell biology.

[39]  J. Chory.  Light signal transduction: an infinite spectrum of possibilities. , 2010, The Plant journal : for cell and molecular biology.

[40]  Takashi Aoyama,et al.  A Genetic Framework for the Control of Cell Division and Differentiation in the Root Meristem , 2008, Science.

[41]  Chentao Lin,et al.  The action mechanisms of plant cryptochromes. , 2011, Trends in plant science.

[42]  Hao Wang,et al.  Antagonistic HLH/bHLH Transcription Factors Mediate Brassinosteroid Regulation of Cell Elongation and Plant Development in Rice and Arabidopsis[C][W][OA] , 2009, The Plant Cell Online.

[43]  Daniel C. Wilson,et al.  Some things get better with age: differences in salicylic acid accumulation and defense signaling in young and mature Arabidopsis , 2015, Front. Plant Sci..

[44]  Zhi-Yong Wang,et al.  Spatiotemporal Brassinosteroid Signaling and Antagonism with Auxin Pattern Stem Cell Dynamics in Arabidopsis Roots , 2015, Current Biology.

[45]  Erin E. Sparks,et al.  Spatiotemporal signalling in plant development , 2013, Nature Reviews Genetics.

[46]  K. Halliday,et al.  Molecular and genetic control of plant thermomorphogenesis , 2016, Nature Plants.

[47]  Joseph J. Kieber,et al.  Cytokinin Induces Cell Division in the Quiescent Center of the Arabidopsis Root Apical Meristem , 2013, Current Biology.

[48]  Daniel L. Mace,et al.  A High-Resolution Root Spatiotemporal Map Reveals Dominant Expression Patterns , 2007, Science.

[49]  Eunkyoo Oh,et al.  The bHLH Transcription Factor HBI1 Mediates the Trade-Off between Growth and Pathogen-Associated Molecular Pattern–Triggered Immunity in Arabidopsis[W][OPEN] , 2014, Plant Cell.

[50]  Yoselin Benitez-Alfonso,et al.  Symplastic communication in organ formation and tissue patterning. , 2016, Current opinion in plant biology.

[51]  C. Zipfel,et al.  Brassinosteroids inhibit pathogen-associated molecular pattern–triggered immune signaling independent of the receptor kinase BAK1 , 2011, Proceedings of the National Academy of Sciences.

[52]  D. Alabadí,et al.  Genomic analysis of DELLA protein activity. , 2013, Plant & cell physiology.

[53]  Patrick Achard,et al.  Integration of Plant Responses to Environmentally Activated Phytohormonal Signals , 2006, Science.

[54]  G. Krouk,et al.  A map of cell type-specific auxin responses , 2013, Molecular systems biology.

[55]  K. Nito,et al.  Spatial Regulation of the Gene Expression Response to Shade in Arabidopsis Seedlings. , 2015, Plant & cell physiology.

[56]  J. Dinneny,et al.  A Spatio-Temporal Understanding of Growth Regulation during the Salt Stress Response in Arabidopsis[W] , 2013, Plant Cell.

[57]  R. Pierik,et al.  DELLA protein function in growth responses to canopy signals. , 2007, The Plant journal : for cell and molecular biology.

[58]  M. Estelle,et al.  SCFTIR1/AFB-Based Auxin Perception: Mechanism and Role in Plant Growth and Development , 2015, Plant Cell.

[59]  J. Lohmann,et al.  Genome Wide Binding Site Analysis Reveals Transcriptional Coactivation of Cytokinin-Responsive Genes by DELLA Proteins , 2015, PLoS genetics.

[60]  Gabriel Krouk,et al.  Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. , 2010, Developmental cell.

[61]  J. Casal.  Photoreceptor signaling networks in plant responses to shade. , 2013, Annual review of plant biology.

[62]  Olivier Michielin,et al.  Inhibition of the shade avoidance response by formation of non‐DNA binding bHLH heterodimers , 2009, The EMBO journal.

[63]  P. Quail,et al.  Dynamic Antagonism between Phytochromes and PIF Family Basic Helix-Loop-Helix Factors Induces Selective Reciprocal Responses to Light and Shade in a Rapidly Responsive Transcriptional Network in Arabidopsis[C][W] , 2012, Plant Cell.

[64]  Junxian He,et al.  Brassinosteroid is required for sugar promotion of hypocotyl elongation in Arabidopsis in darkness , 2015, Planta.

[65]  J. Noel,et al.  Cryptochrome 1 interacts with PIF4 to regulate high temperature-mediated hypocotyl elongation in response to blue light , 2015, Proceedings of the National Academy of Sciences.

[66]  Jan Petrásek,et al.  Cytokinin regulates root meristem activity via modulation of the polar auxin transport , 2009, Proceedings of the National Academy of Sciences.

[67]  R. Pierik,et al.  Blue-light-mediated shade avoidance requires combined auxin and brassinosteroid action in Arabidopsis seedlings. , 2011, The Plant journal : for cell and molecular biology.

[68]  T. Sun.  Gibberellin-GID1-DELLA: A Pivotal Regulatory Module for Plant Growth and Development1 , 2010, Plant Physiology.

[69]  Eunkyoo Oh,et al.  A Triple Helix-Loop-Helix/Basic Helix-Loop-Helix Cascade Controls Cell Elongation Downstream of Multiple Hormonal and Environmental Signaling Pathways in Arabidopsis[C][W] , 2012, Plant Cell.

[70]  Hongkai Ji,et al.  Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. , 2010, Developmental cell.

[71]  J. Chory,et al.  The growth-defense pivot: crisis management in plants mediated by LRR-RK surface receptors. , 2014, Trends in biochemical sciences.

[72]  B. Moore.  Growth-Defense Tradeoffs in Plants: A Balancing Act to Optimize Fitness , 2014 .

[73]  Haiyang Wang,et al.  COP1 mediates the coordination of root and shoot growth by light through modulation of PIN1- and PIN2-dependent auxin transport in Arabidopsis , 2012, Development.

[74]  Eunkyoo Oh,et al.  Brassinosteroid signaling network and regulation of photomorphogenesis. , 2012, Annual review of genetics.

[75]  M. Strnad,et al.  Activity of the Brassinosteroid Transcription Factors BRASSINAZOLE RESISTANT1 and BRASSINOSTEROID INSENSITIVE1-ETHYL METHANESULFONATE-SUPPRESSOR1/BRASSINAZOLE RESISTANT2 Blocks Developmental Reprogramming in Response to Low Phosphate Availability1[W][OPEN] , 2014, Plant Physiology.

[76]  Yulia Fridman,et al.  Translatome analyses capture of opposing tissue-specific brassinosteroid signals orchestrating root meristem differentiation , 2015, Proceedings of the National Academy of Sciences.

[77]  J. Chory,et al.  Brassinosteroids modulate the efficiency of plant immune responses to microbe-associated molecular patterns , 2011, Proceedings of the National Academy of Sciences.

[78]  H. Yoshida,et al.  DELLA protein functions as a transcriptional activator through the DNA binding of the INDETERMINATE DOMAIN family proteins , 2014, Proceedings of the National Academy of Sciences.

[79]  W. J. Lucas,et al.  Molecular mechanisms underlying phosphate sensing, signaling, and adaptation in plants. , 2014, Journal of integrative plant biology.

[80]  C. Ballaré,et al.  To grow or defend? Low red : far-red ratios reduce jasmonate sensitivity in Arabidopsis seedlings by promoting DELLA degradation and increasing JAZ10 stability. , 2014, The New phytologist.

[81]  Zhi-Yong Wang,et al.  At the intersection of plant growth and immunity. , 2014, Cell host & microbe.

[82]  I. Xenarios,et al.  Phytochrome interacting factors 4 and 5 control seedling growth in changing light conditions by directly controlling auxin signaling. , 2012, The Plant journal : for cell and molecular biology.

[83]  S. Sabatini,et al.  Plant hormone cross-talk: the pivot of root growth. , 2015, Journal of experimental botany.

[84]  L. Strader,et al.  Abscisic Acid Regulates Root Elongation Through the Activities of Auxin and Ethylene in Arabidopsis thaliana , 2014, G3: Genes, Genomes, Genetics.

[85]  C. Fankhauser,et al.  A molecular framework for light and gibberellin control of cell elongation , 2008, Nature.

[86]  Zhaojun Ding,et al.  TAA1-Regulated Local Auxin Biosynthesis in the Root-Apex Transition Zone Mediates the Aluminum-Induced Inhibition of Root Growth in Arabidopsis[C][W][OPEN] , 2014, Plant Cell.

[87]  S. Prat,et al.  BR-dependent phosphorylation modulates PIF4 transcriptional activity and shapes diurnal hypocotyl growth , 2016 .

[88]  J. Ecker,et al.  Cryptochromes Interact Directly with PIFs to Control Plant Growth in Limiting Blue Light , 2016, Cell.

[89]  Jan Petrásek,et al.  Auxin transport routes in plant development , 2009, Development.

[90]  B. Cammue,et al.  The Plant Peptidome: An Expanding Repertoire of Structural Features and Biological Functions[OPEN] , 2015, Plant Cell.

[91]  Ana I. Caño-Delgado,et al.  Regulation of plant stem cell quiescence by a brassinosteroid signaling module. , 2014, Developmental cell.

[92]  X. Deng,et al.  Coordinated regulation of Arabidopsis thaliana development by light and gibberellins , 2008, Nature.

[93]  Murray Grant,et al.  Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. , 2011, Annual review of phytopathology.

[94]  C. Zipfel,et al.  Antagonistic Regulation of Growth and Immunity by the Arabidopsis Basic Helix-Loop-Helix Transcription Factor HOMOLOG OF BRASSINOSTEROID ENHANCED EXPRESSION2 INTERACTING WITH INCREASED LEAF INCLINATION1 BINDING bHLH11[W][OPEN] , 2014, Plant Physiology.

[95]  T. Demura,et al.  Involvement of Auxin and Brassinosteroid in the Regulation of Petiole Elongation under the Shade1[W] , 2010, Plant Physiology.

[96]  Jarkko Salojärvi,et al.  PLETHORA gradient formation mechanism separates auxin responses , 2014, Nature.

[97]  G. Coruzzi,et al.  Nitrate-responsive miR393/AFB3 regulatory module controls root system architecture in Arabidopsis thaliana , 2010, Proceedings of the National Academy of Sciences.

[98]  A. Burlingame,et al.  A mutually assured destruction mechanism attenuates light signaling in Arabidopsis , 2014, Science.

[99]  Bruno Müller,et al.  Cytokinin and auxin interaction in root stem-cell specification during early embryogenesis , 2008, Nature.

[100]  Anna N. Stepanova,et al.  TAA1-Mediated Auxin Biosynthesis Is Essential for Hormone Crosstalk and Plant Development , 2008, Cell.