Short-term and continuing stresses differentially interplay with multiple hormones to regulate plant survival and growth.

The stress phytohormone, abscisic acid (ABA), plays important roles in facilitating plants to survive and grow well under a wide range of stress conditions. Previous gene expression studies mainly focused on plant responses to short-term ABA treatment, but the effect of sustained ABA treatment and their difference are poorly studied. Here, we treated plants with ABA for 1 h or 9 d, and our genome-wide analysis indicated the differentially regulated genes under the two conditions were tremendously different. We analyzed other hormones' signaling changes by using their whole sets of known responsive genes as reporters and integrating feedback regulation of their biosynthesis. We found that, under short-term ABA treatment, signaling outputs of growth-promoting hormones, brassinosteroids and gibberellins, and a biotic stress-responsive hormone, jasmonic acid, were significantly inhibited, while auxin and ethylene signaling outputs were promoted. However, sustained ABA treatment repressed cytokinin and gibberellin signaling, but stimulated auxin signaling. Using several sets of hormone-related mutants, we found candidates in corresponding hormonal signaling pathways, including receptors or transcription regulators, are essential in responding to ABA. Our findings indicate interactions of ABA-dependent stress signals with hormones at different levels are involved in plants to survive under transient stress and to adapt to continuing stressful environments.

[1]  P. Ronald,et al.  Recent advances in dissecting stress-regulatory crosstalk in rice. , 2013, Molecular plant.

[2]  K. Shinozaki,et al.  Cytokinins: metabolism and function in plant adaptation to environmental stresses. , 2012, Trends in plant science.

[3]  R. Vaňková,et al.  Recovery from drought stress in tobacco , 2012, Plant signaling & behavior.

[4]  Minyoung Lee,et al.  Activation of a flavin monooxygenase gene YUCCA7 enhances drought resistance in Arabidopsis , 2011, Planta.

[5]  K. Shinozaki,et al.  Analysis of Cytokinin Mutants and Regulation of Cytokinin Metabolic Genes Reveals Important Regulatory Roles of Cytokinins in Drought, Salt and Abscisic Acid Responses, and Abscisic Acid Biosynthesis[C][W] , 2011, Plant Cell.

[6]  S. Cutler,et al.  Abscisic acid: emergence of a core signaling network. , 2010, Annual review of plant biology.

[7]  J. Ton,et al.  The multifaceted role of ABA in disease resistance. , 2009, Trends in plant science.

[8]  Xuelu Wang,et al.  The primary signaling outputs of brassinosteroids are regulated by abscisic acid signaling , 2009, Proceedings of the National Academy of Sciences.

[9]  H. Fukaki,et al.  Hormone interactions during lateral root formation , 2009, Plant Molecular Biology.

[10]  R. Solano,et al.  JAZ repressors set the rhythm in jasmonate signaling. , 2008, Current opinion in plant biology.

[11]  Kazuo Shinozaki,et al.  The AtGenExpress hormone and chemical treatment data set: experimental design, data evaluation, model data analysis and data access. , 2008, The Plant journal : for cell and molecular biology.

[12]  Marta Godoy,et al.  ABA Is an Essential Signal for Plant Resistance to Pathogens Affecting JA Biosynthesis and the Activation of Defenses in Arabidopsis[W] , 2007, The Plant Cell Online.

[13]  Jennifer L. Nemhauser,et al.  Different Plant Hormones Regulate Similar Processes through Largely Nonoverlapping Transcriptional Responses , 2006, Cell.

[14]  B. P. Hall,et al.  Progress report: ethylene signaling and responses , 2006, Planta.

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

[16]  Zhi-Liang Zheng,et al.  Transcriptome Analysis Reveals Specific Modulation of Abscisic Acid Signaling by ROP10 Small GTPase in Arabidopsis1[w] , 2005, Plant Physiology.

[17]  J. Chory,et al.  A New Class of Transcription Factors Mediates Brassinosteroid-Regulated Gene Expression in Arabidopsis , 2005, Cell.

[18]  Paul R. Ebert,et al.  Antagonistic Interaction between Abscisic Acid and Jasmonate-Ethylene Signaling Pathways Modulates Defense Gene Expression and Disease Resistance in Arabidopsis , 2004, The Plant Cell Online.

[19]  K. Roberts,et al.  The expression patterns of arabinogalactan-protein AtAGP30 and GLABRA2 reveal a role for abscisic acid in the early stages of root epidermal patterning. , 2004, The Plant journal : for cell and molecular biology.

[20]  D. Inzé,et al.  Cell Cycle Modulation in the Response of the Primary Root of Arabidopsis to Salt Stress1 , 2004, Plant Physiology.

[21]  Christopher D Town,et al.  Development and evaluation of an Arabidopsis whole genome Affymetrix probe array. , 2004, The Plant journal : for cell and molecular biology.

[22]  N. Chua,et al.  ABA activates ADPR cyclase and cADPR induces a subset of ABA-responsive genes in Arabidopsis. , 2004, The Plant journal : for cell and molecular biology.

[23]  Hur-Song Chang,et al.  Transcriptome Changes for Arabidopsis in Response to Salt, Osmotic, and Cold Stress1,212 , 2002, Plant Physiology.

[24]  K. Akiyama,et al.  Monitoring the expression pattern of around 7,000 Arabidopsis genes under ABA treatments using a full-length cDNA microarray , 2002, Functional & Integrative Genomics.

[25]  G. Hagen,et al.  Auxin-responsive gene expression: genes, promoters and regulatory factors , 2002, Plant Molecular Biology.

[26]  Margaret Werner-Washburne,et al.  The genomics of yeast responses to environmental stress and starvation , 2002, Functional & Integrative Genomics.

[27]  J. Chory,et al.  BES1 Accumulates in the Nucleus in Response to Brassinosteroids to Regulate Gene Expression and Promote Stem Elongation , 2002, Cell.

[28]  R. Munns.  Comparative physiology of salt and water stress. , 2002, Plant, cell & environment.

[29]  K. Ljung,et al.  Sites and homeostatic control of auxin biosynthesis in Arabidopsis during vegetative growth. , 2002, The Plant journal : for cell and molecular biology.

[30]  A. Thompson,et al.  Control of abscisic acid synthesis. , 2000, Journal of experimental botany.

[31]  R. Kaldenhoff,et al.  Light-induced stomatal movement of selected Arabidopsis thaliana mutants. , 2000, Journal of experimental botany.

[32]  P. McCourt,et al.  Regulation of Abscisic Acid Signaling by the Ethylene Response Pathway in Arabidopsis , 2000, Plant Cell.

[33]  I. Coraggio,et al.  Ethylene promotes ethylene biosynthesis during pea seed germination by positive feedback regulation of 1-aminocyclo-propane-1-carboxylic acid oxidase , 2000, Planta.

[34]  M. Ashburner,et al.  Gene Ontology: tool for the unification of biology , 2000, Nature Genetics.

[35]  H. Bohnert,et al.  Genomic approaches to plant stress tolerance. , 2000, Current opinion in plant biology.

[36]  A. Cutler,et al.  Formation and breakdown of ABA. , 1999, Trends in plant science.

[37]  H. Lichtenthaler,et al.  The Stress Concept in Plants: An Introduction , 1998, Annals of the New York Academy of Sciences.

[38]  S. Clouse,et al.  BRASSINOSTEROIDS: Essential Regulators of Plant Growth and Development. , 1998, Annual review of plant physiology and plant molecular biology.

[39]  Malcolm C. Drew,et al.  Ethylene and plant responses to stress , 1997 .

[40]  F. B. Pickett,et al.  Mutations in the AXR3 gene of Arabidopsis result in altered auxin response including ectopic expression from the SAUR-AC1 promoter. , 1996, The Plant journal : for cell and molecular biology.

[41]  F. Tardieu,et al.  Expansion of pea leaves subjected to short water deficit: cell number and cell size are sensitive to stress at different periods of leaf development , 1995 .

[42]  K. Skriver,et al.  cis-acting DNA elements responsive to gibberellin and its antagonist abscisic acid. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[43]  J. Ecker,et al.  Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. , 1990, The Plant cell.

[44]  P. Kramer,et al.  Responses of Plants to Environmental Stresses , 1973 .

[45]  Jianhua Zhang,et al.  Abscisic acid accumulation modulates auxin transport in the root tip to enhance proton secretion for maintaining root growth under moderate water stress. , 2013, The New phytologist.

[46]  L. Xiong,et al.  A GH 3 family m mber , OsGH 3-2 , modulates auxin and abscisic acid levels and differentially affects drought and cold tolerance in rice , 2012 .

[47]  Jian-Kang Zhu,et al.  Salt and drought stress signal transduction in plants. , 2002, Annual review of plant biology.

[48]  M. Evans,et al.  The action of auxin on plant cell elongation. , 1985, Critical reviews in plant sciences.

[49]  V. Petersen.  Effect of Energy-Requiring Defense Reactions on Yield and Grain Quality in a Powdery Mildew-Resistant Barley Cultivar , 1981 .