Research on plant abiotic stress responses in the post-genome era: past, present and future.

Understanding abiotic stress responses in plants is an important and challenging topic in plant research. Physiological and molecular biological analyses have allowed us to draw a picture of abiotic stress responses in various plants, and determination of the Arabidopsis genome sequence has had a great impact on this research field. The availability of the complete genome sequence has facilitated access to essential information for all genes, e.g. gene products and their function, transcript levels, putative cis-regulatory elements, and alternative splicing patterns. These data have been obtained from comprehensive transcriptome analyses and studies using full-length cDNA collections and T-DNA- or transposon-tagged mutant lines, which were also enhanced by genome sequence information. Moreover, studies on novel regulatory mechanisms involving use of small RNA molecules, chromatin modulation and genomic DNA modification have enabled us to recognize that plants have evolved complicated and sophisticated systems in response to complex abiotic stresses. Integrated data obtained with various 'omics' approaches have provided a more comprehensive picture of abiotic stress responses. In addition, research on stress responses in various plant species other than Arabidopsis has increased our knowledge regarding the mechanisms of plant stress tolerance in nature. Based on this progress, improvements in crop stress tolerance have been attempted by means of gene transfer and marker-assisted breeding. In this review, we summarize recent progress in abiotic stress studies, especially in the post-genomic era, and offer new perspectives on research directions for the next decade.

[1]  Adam Round,et al.  The abscisic acid receptor PYR1 in complex with abscisic acid , 2009, Nature.

[2]  D. Lisch.  Epigenetic regulation of transposable elements in plants. , 2009, Annual review of plant biology.

[3]  Joseph M. Dale,et al.  Empirical Analysis of Transcriptional Activity in the Arabidopsis Genome , 2003, Science.

[4]  Kazuo Shinozaki,et al.  Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) Function as Transcriptional Activators in Abscisic Acid Signaling Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.006130. , 2003, The Plant Cell Online.

[5]  Oliver Fiehn,et al.  A prominent role for the CBF cold response pathway in configuring the low-temperature metabolome of Arabidopsis. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[6]  M. Hirai,et al.  Decoding genes with coexpression networks and metabolomics - 'majority report by precogs'. , 2008, Trends in plant science.

[7]  Jian-Kang Zhu,et al.  Arabidopsis mutant deficient in 3 abscisic acid-activated protein kinases reveals critical roles in growth, reproduction, and stress , 2009, Proceedings of the National Academy of Sciences.

[8]  J. Nap,et al.  The SWI/SNF chromatin-remodeling gene AtCHR12 mediates temporary growth arrest in Arabidopsis thaliana upon perceiving environmental stress. , 2007, The Plant journal : for cell and molecular biology.

[9]  K. Shinozaki,et al.  The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis. , 2004, Molecular cell.

[10]  Fan Jiang,et al.  Activation of Glucosidase via Stress-Induced Polymerization Rapidly Increases Active Pools of Abscisic Acid , 2006, Cell.

[11]  T. Flowers.  Improving crop salt tolerance. , 2004, Journal of experimental botany.

[12]  M. Thomashow,et al.  Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis. , 2004, The Plant journal : for cell and molecular biology.

[13]  E. Nambara,et al.  Abscisic acid biosynthesis and catabolism. , 2005, Annual review of plant biology.

[14]  S. Berger.  The complex language of chromatin regulation during transcription , 2007, Nature.

[15]  R. Sunkar,et al.  Drought and Salt Tolerance in Plants , 2005 .

[16]  I. Hwang,et al.  Arabidopsis Calcium-Dependent Protein Kinase AtCPK32 Interacts with ABF4, a Transcriptional Regulator of Abscisic Acid-Responsive Gene Expression, and Modulates Its Activity1 , 2005, Plant Physiology.

[17]  I. Kovalchuk,et al.  Epigenetic control of plant stress response , 2008, Environmental and molecular mutagenesis.

[18]  K. Shinozaki,et al.  Arabidopsis plasma membrane protein crucial for Ca2+ influx and touch sensing in roots , 2007, Proceedings of the National Academy of Sciences.

[19]  K. Shinozaki,et al.  Antagonistic Interaction between Systemic Acquired Resistance and the Abscisic Acid–Mediated Abiotic Stress Response in Arabidopsis[W] , 2008, The Plant Cell Online.

[20]  Kazuo Shinozaki,et al.  Phenome analysis in plant species using loss-of-function and gain-of-function mutants. , 2009, Plant & cell physiology.

[21]  R. Fluhr,et al.  Rapid Transcriptome Changes Induced by Cytosolic Ca2+ Transients Reveal ABRE-Related Sequences as Ca2+-Responsive cis Elements in Arabidopsis[W] , 2006, The Plant Cell Online.

[22]  Mikiko C. Siomi,et al.  The Discovery of Rna Interference (rnai) Biogenesis of Small Rnas on the Road to Reading the Rna-interference Code Insight Review , 2022 .

[23]  N. Tsutsumi,et al.  Dynamic and reversible changes in histone H3-Lys4 methylation and H3 acetylation occurring at submergence-inducible genes in rice. , 2006, Plant & cell physiology.

[24]  D. Tollervey,et al.  The Many Pathways of RNA Degradation , 2009, Cell.

[25]  Murray Grant,et al.  Pseudomonas syringae pv. tomato hijacks the Arabidopsis abscisic acid signalling pathway to cause disease , 2007, The EMBO journal.

[26]  Kazuo Shinozaki,et al.  Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. , 2006, Annual review of plant biology.

[27]  Marjori Matzke,et al.  Targets of RNA-directed DNA methylation. , 2007, Current opinion in plant biology.

[28]  R. Sunkar,et al.  Novel and Stress-Regulated MicroRNAs and Other Small RNAs from Arabidopsis , 2004, The Plant Cell Online.

[29]  Yiyue Zhang,et al.  The negative regulator of plant cold responses, HOS1, is a RING E3 ligase that mediates the ubiquitination and degradation of ICE1. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[30]  Américo Rodrigues,et al.  HAB1–SWI3B Interaction Reveals a Link between Abscisic Acid Signaling and Putative SWI/SNF Chromatin-Remodeling Complexes in Arabidopsis[C][W] , 2008, The Plant Cell Online.

[31]  Jian-Kang Zhu,et al.  Epigenetic regulation of stress responses in plants. , 2009, Current opinion in plant biology.

[32]  A. Reddy.  Alternative splicing of pre-messenger RNAs in plants in the genomic era. , 2007, Annual review of plant biology.

[33]  N. Tuteja,et al.  Calcium- and salt-stress signaling in plants: shedding light on SOS pathway. , 2008, Archives of biochemistry and biophysics.

[34]  S. Cutler,et al.  A Gate-Latch-Lock Mechanism for Hormone Signaling by Abscisic Acid Receptors , 2009, Nature.

[35]  Andrea Pitzschke,et al.  Emerging MAP kinase pathways in plant stress signalling. , 2005, Trends in plant science.

[36]  V. Brendel,et al.  Genomewide comparative analysis of alternative splicing in plants. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[37]  Américo Rodrigues,et al.  Protein Phosphatases 2C Regulate the Activation of the Snf1-Related Kinase OST1 by Abscisic Acid in Arabidopsis[W] , 2009, The Plant Cell Online.

[38]  M. Sussman,et al.  Analysis of the Arabidopsis Histidine Kinase ATHK1 Reveals a Connection between Vegetative Osmotic Stress Sensing and Seed Maturation[W][OA] , 2008, The Plant Cell Online.

[39]  H. Bohnert,et al.  Involvement of Arabidopsis HOS15 in histone deacetylation and cold tolerance , 2008, Proceedings of the National Academy of Sciences.

[40]  K. Shinozaki,et al.  Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[41]  T. Flowers,et al.  Salinity tolerance in halophytes. , 2008, The New phytologist.

[42]  Jian-Kang Zhu,et al.  Screening for Gene Regulation Mutants by Bioluminescence Imaging , 2002, Science's STKE.

[43]  M. Hirai,et al.  Omics-based identification of Arabidopsis Myb transcription factors regulating aliphatic glucosinolate biosynthesis , 2007, Proceedings of the National Academy of Sciences.

[44]  Gunnar Rätsch,et al.  Stress-induced changes in the Arabidopsis thaliana transcriptome analyzed using whole-genome tiling arrays. , 2009, The Plant journal : for cell and molecular biology.

[45]  Peter Doerner,et al.  Abscisic Acid Has a Key Role in Modulating Diverse Plant-Pathogen Interactions1[C][W][OA] , 2009, Plant Physiology.

[46]  Kazuo Shinozaki,et al.  Isolation and Functional Analysis of Arabidopsis Stress-Inducible NAC Transcription Factors That Bind to a Drought-Responsive cis-Element in the early responsive to dehydration stress 1 Promoterw⃞ , 2004, The Plant Cell Online.

[47]  K. Shinozaki,et al.  Three Arabidopsis SnRK2 protein kinases, SRK2D/SnRK2.2, SRK2E/SnRK2.6/OST1 and SRK2I/SnRK2.3, involved in ABA signaling are essential for the control of seed development and dormancy. , 2009, Plant & cell physiology.

[48]  Daniel L. Mace,et al.  Cell Identity Mediates the Response of Arabidopsis Roots to Abiotic Stress , 2008, Science.

[49]  T. Sakurai,et al.  Comparative Genomics in Salt Tolerance between Arabidopsis and Arabidopsis-Related Halophyte Salt Cress Using Arabidopsis Microarray1 , 2004, Plant Physiology.

[50]  Masakazu Satou,et al.  Genome-wide analysis of alternative pre-mRNA splicing in Arabidopsis thaliana based on full-length cDNA sequences. , 2004, Nucleic acids research.

[51]  D. Bartel,et al.  MicroRNAS and their regulatory roles in plants. , 2006, Annual review of plant biology.

[52]  Jian-Kang Zhu,et al.  ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. , 2003, Genes & development.

[53]  Colleen J. Doherty,et al.  Roles for Arabidopsis CAMTA Transcription Factors in Cold-Regulated Gene Expression and Freezing Tolerance[W][OA] , 2009, The Plant Cell Online.

[54]  Kazuo Shinozaki,et al.  Mitogen-activated protein kinase cascades in plants: a new nomenclature. , 2002, Trends in plant science.

[55]  Olivier Voinnet,et al.  The diversity of RNA silencing pathways in plants. , 2006, Trends in genetics : TIG.

[56]  K. Shinozaki,et al.  Co-expression of the stress-inducible zinc finger homeodomain ZFHD1 and NAC transcription factors enhances expression of the ERD1 gene in Arabidopsis. , 2006, The Plant Journal.

[57]  H. Bohnert,et al.  Salinity stress adaptation competence in the extremophile Thellungiella halophila in comparison with its relative Arabidopsis thaliana. , 2005, The Plant journal : for cell and molecular biology.

[58]  C. Xiang,et al.  Functional gene-mining for salt-tolerance genes with the power of Arabidopsis. , 2008, The Plant journal : for cell and molecular biology.

[59]  K. Shinozaki,et al.  Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. , 2006, Current opinion in plant biology.

[60]  M. Estelle,et al.  Recent advances and emerging trends in plant hormone signalling , 2009, Nature.

[61]  Ramanjulu Sunkar,et al.  Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. , 2007, Trends in plant science.

[62]  K. Shinozaki,et al.  Alterations of lysine modifications on the histone H3 N-tail under drought stress conditions in Arabidopsis thaliana. , 2008, Plant & cell physiology.

[63]  E. Bornberg-Bauer,et al.  The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. , 2007, The Plant journal : for cell and molecular biology.

[64]  N. Fedoroff.  Cross-Talk in Abscisic Acid Signaling , 2002, Science's STKE.

[65]  Kazuo Shinozaki,et al.  Arabidopsis DREB2A-Interacting Proteins Function as RING E3 Ligases and Negatively Regulate Plant Drought Stress–Responsive Gene Expression[W] , 2008, The Plant Cell Online.

[66]  K. Shinozaki,et al.  Abscisic acid-dependent multisite phosphorylation regulates the activity of a transcription activator AREB1. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[67]  Alistair Rogers,et al.  Connecting genes, coexpression modules, and molecular signatures to environmental stress phenotypes in plants , 2008, BMC Systems Biology.

[68]  S. Assmann,et al.  Two Novel GPCR-Type G Proteins Are Abscisic Acid Receptors in Arabidopsis , 2009, Cell.

[69]  G. Owttrim.  RNA helicases and abiotic stress , 2006, Nucleic acids research.

[70]  Kenichi Hitomi,et al.  Structural Mechanism of Abscisic Acid Binding and Signaling by Dimeric PYR1 , 2009, Science.

[71]  E. Grill,et al.  Regulators of PP2C Phosphatase Activity Function as Abscisic Acid Sensors , 2009, Science.

[72]  N. Fedoroff.  RNA-binding proteins in plants: the tip of an iceberg? , 2002, Current opinion in plant biology.

[73]  Charles L. Guy,et al.  Exploring the Temperature-Stress Metabolome of Arabidopsis1[w] , 2004, Plant Physiology.

[74]  Da-Peng Zhang,et al.  Two Calcium-Dependent Protein Kinases, CPK4 and CPK11, Regulate Abscisic Acid Signal Transduction in Arabidopsis[W] , 2007, The Plant Cell Online.

[75]  K. Torii,et al.  SCREAM/ICE1 and SCREAM2 Specify Three Cell-State Transitional Steps Leading to Arabidopsis Stomatal Differentiation[W][OA] , 2008, The Plant Cell Online.

[76]  Alisdair R Fernie,et al.  Plant metabolomics: towards biological function and mechanism. , 2006, Trends in plant science.

[77]  S. Luan,et al.  A rice quantitative trait locus for salt tolerance encodes a sodium transporter , 2005, Nature Genetics.

[78]  C. Valon,et al.  An Update on Abscisic Acid Signaling in Plants and More , 2022 .

[79]  Peter McCourt,et al.  Cross-talk in plant hormone signalling: what Arabidopsis mutants are telling us. , 2003, Annals of botany.

[80]  K. Shinozaki,et al.  Gene networks involved in drought stress response and tolerance. , 2006, Journal of experimental botany.

[81]  K. Miura,et al.  Sumoylation, a post-translational regulatory process in plants. , 2007, Current opinion in plant biology.

[82]  S. Cutler,et al.  In vitro Reconstitution of an ABA Signaling Pathway , 2009, Nature.

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

[84]  J. Ecker,et al.  CDPKs CPK6 and CPK3 Function in ABA Regulation of Guard Cell S-Type Anion- and Ca2+- Permeable Channels and Stomatal Closure , 2006, PLoS biology.

[85]  R. Mittler,et al.  Abiotic stress, the field environment and stress combination. , 2006, Trends in plant science.

[86]  Y. Fujita,et al.  Structural basis of abscisic acid signalling , 2009, Nature.

[87]  E. Vierling,et al.  Heat Stress Phenotypes of Arabidopsis Mutants Implicate Multiple Signaling Pathways in the Acquisition of Thermotolerance1[w] , 2005, Plant Physiology.

[88]  K. Shinozaki,et al.  Functional analysis of AHK1/ATHK1 and cytokinin receptor histidine kinases in response to abscisic acid, drought, and salt stress in Arabidopsis , 2007, Proceedings of the National Academy of Sciences.

[89]  Sheng Yang He,et al.  Plant Stomata Function in Innate Immunity against Bacterial Invasion , 2006, Cell.

[90]  Jonathan D. G. Jones,et al.  Hormone (Dis)harmony Moulds Plant Health and Disease , 2009, Science.

[91]  Ghislain Breton,et al.  Decoding Ca(2+) signals through plant protein kinases. , 2004, Annual review of plant biology.

[92]  Jonathan D. G. Jones,et al.  CDPK-mediated signalling pathways: specificity and cross-talk. , 2004, Journal of experimental botany.

[93]  T. Zhu,et al.  Networks of transcription factors with roles in environmental stress response. , 2004, Trends in plant science.

[94]  Filip Rolland,et al.  A central integrator of transcription networks in plant stress and energy signalling , 2007, Nature.

[95]  J. Schroeder,et al.  Impacts of altered RNA metabolism on abscisic acid signaling. , 2003, Current opinion in plant biology.

[96]  M. Matsuoka,et al.  Genetic approaches to crop improvement: responding to environmental and population changes , 2008, Nature Reviews Genetics.

[97]  H. Bohnert,et al.  Integration of Arabidopsis thaliana stress-related transcript profiles, promoter structures, and cell-specific expression , 2007, Genome Biology.

[98]  B. Asselbergh,et al.  Global switches and fine-tuning-ABA modulates plant pathogen defense. , 2008, Molecular plant-microbe interactions : MPMI.

[99]  F. Myouga,et al.  Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis , 2009, Proceedings of the National Academy of Sciences.

[100]  K. Shinozaki,et al.  Regulatory network of gene expression in the drought and cold stress responses. , 2003, Current opinion in plant biology.

[101]  R. Vierstra.  The ubiquitin–26S proteasome system at the nexus of plant biology , 2009, Nature Reviews Molecular Cell Biology.

[102]  S. Luan.  The CBL-CIPK network in plant calcium signaling. , 2009, Trends in plant science.

[103]  Masakazu Satou,et al.  Arabidopsis transcriptome analysis under drought, cold, high-salinity and ABA treatment conditions using a tiling array. , 2008, Plant & cell physiology.

[104]  K. Shinozaki,et al.  Perception and transduction of abscisic acid signals: keys to the function of the versatile plant hormone ABA. , 2007, Trends in plant science.

[105]  M. Thomashow.  So what's new in the field of plant cold acclimation? Lots! , 2001, Plant physiology.

[106]  Shuhei Yamamoto,et al.  Abscisic acid-activated SNRK2 protein kinases function in the gene-regulation pathway of ABA signal transduction by phosphorylating ABA response element-binding factors. , 2005, The Plant journal : for cell and molecular biology.

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

[108]  K. Shinozaki,et al.  Engineering drought tolerance in plants: discovering and tailoring genes to unlock the future. , 2006, Current opinion in biotechnology.

[109]  P. Ciais,et al.  Europe-wide reduction in primary productivity caused by the heat and drought in 2003 , 2005, Nature.

[110]  Marie Boudsocq,et al.  Identification of Nine Sucrose Nonfermenting 1-related Protein Kinases 2 Activated by Hyperosmotic and Saline Stresses in Arabidopsis thaliana* , 2004, Journal of Biological Chemistry.

[111]  C. Pieterse,et al.  Networking by small-molecule hormones in plant immunity. , 2009, Nature chemical biology.

[112]  M. Hirai,et al.  Widely Targeted Metabolomics Based on Large-Scale MS/MS Data for Elucidating Metabolite Accumulation Patterns in Plants , 2008, Plant & cell physiology.

[113]  M. Gribskov,et al.  The Arabidopsis CDPK-SnRK Superfamily of Protein Kinases , 2003, Plant Physiology.

[114]  R. Lister,et al.  Next is now: new technologies for sequencing of genomes, transcriptomes, and beyond. , 2009, Current opinion in plant biology.

[115]  M. Hirai,et al.  Elucidation of Gene-to-Gene and Metabolite-to-Gene Networks in Arabidopsis by Integration of Metabolomics and Transcriptomics* , 2005, Journal of Biological Chemistry.

[116]  R. Solano,et al.  Molecular players regulating the jasmonate signalling network. , 2005, Current opinion in plant biology.

[117]  Qingqiu Gong,et al.  An Arabidopsis gene network based on the graphical Gaussian model. , 2007, Genome research.

[118]  K. Shinozaki,et al.  CYP707A3, a major ABA 8'-hydroxylase involved in dehydration and rehydration response in Arabidopsis thaliana. , 2006, The Plant journal : for cell and molecular biology.

[119]  O. Borsani,et al.  Endogenous siRNAs Derived from a Pair of Natural cis-Antisense Transcripts Regulate Salt Tolerance in Arabidopsis , 2005, Cell.

[120]  S. Kim,et al.  ABFs, a Family of ABA-responsive Element Binding Factors* , 2000, The Journal of Biological Chemistry.

[121]  D. Galbraith,et al.  Salt Cress. A Halophyte and Cryophyte Arabidopsis Relative Model System and Its Applicability to Molecular Genetic Analyses of Growth and Development of Extremophiles1 , 2004, Plant Physiology.