A step towards understanding plant responses to multiple environmental stresses: a genome-wide study.

In natural habitats, especially in arid areas, plants are often simultaneously exposed to multiple abiotic stresses, such as salt, osmotic and heat stresses. However, most analyses of gene expression in stress responses examine individual stresses. In this report, we compare gene expression in individual and combined stresses. We show that combined stress treatments with salt, mannitol and heat induce a unique pattern of gene expression that is not a simple merge of the individual stress responses. Under multiple stress conditions, expression of most heat and salt stress-responsive genes increased to levels similar to or higher than those measured in single stress conditions, but osmotic stress-responsive genes increased to lower levels. Genes up-regulated to higher levels under multiple stress condition than single stress conditions include genes for heat shock proteins, heat shock regulators and late embryogenesis abundant proteins (LEAs), which protect other proteins from damage caused by stresses, suggesting their importance in multiple stress condition. Based on this analysis, we identify candidate genes for engineering crop plants tolerant to multiple stresses.

[1]  E. T. Palva,et al.  The expression of a rab-related gene, rab18, is induced by abscisic acid during the cold acclimation process of Arabidopsis thaliana (L.) Heynh , 1992, Plant Molecular Biology.

[2]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[3]  Satoru Miyano,et al.  Open source clustering software , 2004 .

[4]  P. Verslues,et al.  Essential Role of Tissue-Specific Proline Synthesis and Catabolism in Growth and Redox Balance at Low Water Potential1[W][OA] , 2011, Plant Physiology.

[5]  M. Wise,et al.  The continuing conundrum of the LEA proteins , 2007, Naturwissenschaften.

[6]  Jianhua Zhu,et al.  The Plant Cuticle Is Required for Osmotic Stress Regulation of Abscisic Acid Biosynthesis and Osmotic Stress Tolerance in Arabidopsis[W] , 2011, Plant Cell.

[7]  Jian-Kang Zhu,et al.  Responses to Abiotic Stress , 2002 .

[8]  R. Mittler,et al.  The Combined Effect of Drought Stress and Heat Shock on Gene Expression in Tobacco1 , 2002, Plant Physiology.

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

[10]  N. Kav,et al.  Functional characterization of four APETALA2-family genes (RAP2.6, RAP2.6L, DREB19 and DREB26) in Arabidopsis , 2010, Plant Molecular Biology.

[11]  E. Vierling.  The Roles of Heat Shock Proteins in Plants , 1991 .

[12]  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.

[13]  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.

[14]  S. Somerville,et al.  Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[15]  K. Shinozaki,et al.  Two Transcription Factors, DREB1 and DREB2, with an EREBP/AP2 DNA Binding Domain Separate Two Cellular Signal Transduction Pathways in Drought- and Low-Temperature-Responsive Gene Expression, Respectively, in Arabidopsis , 1998, Plant Cell.

[16]  D. Hincha,et al.  A mitochondrial late embryogenesis abundant protein stabilizes model membranes in the dry state. , 2010, Biochimica et biophysica acta.

[17]  Nobutaka Mitsuda,et al.  Arabidopsis HsfB1 and HsfB2b Act as Repressors of the Expression of Heat-Inducible Hsfs But Positively Regulate the Acquired Thermotolerance1[C][W][OA] , 2011, Plant Physiology.

[18]  V. Shulaev,et al.  When Defense Pathways Collide. The Response of Arabidopsis to a Combination of Drought and Heat Stress1[w] , 2004, Plant Physiology.

[19]  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.

[20]  M. Feder,et al.  Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. , 1999, Annual review of physiology.

[21]  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.

[22]  Jianhua Zhu,et al.  An Arabidopsis homeodomain transcription factor gene, HOS9, mediates cold tolerance through a CBF-independent pathway. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[23]  U. Sonnewald,et al.  Simultaneous Application of Heat, Drought, and Virus to Arabidopsis Plants Reveals Significant Shifts in Signaling Networks1[W][OPEN] , 2013, Plant Physiology.

[24]  Hur-Song Chang,et al.  Transcriptional Profiling Reveals Novel Interactions between Wounding, Pathogen, Abiotic Stress, and Hormonal Responses in Arabidopsis1,212 , 2002, Plant Physiology.

[25]  Z. Hong,et al.  Overexpression of [delta]-Pyrroline-5-Carboxylate Synthetase Increases Proline Production and Confers Osmotolerance in Transgenic Plants , 1995, Plant physiology.

[26]  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.

[27]  P. Wigge,et al.  H2A.Z-Containing Nucleosomes Mediate the Thermosensory Response in Arabidopsis , 2010, Cell.

[28]  Nobutaka Mitsuda,et al.  Arabidopsis HsfB 1 and HsfB 2 b Act as Repressors of the Expression of Heat-Inducible Hsfs But Positively Regulate the Acquired Thermotolerance 1 [ C ] [ W ] [ OA ] , 2011 .

[29]  M. Bevan,et al.  The function of plant heat shock promoter elements in the regulated expression of chimaeric genes in transgenic tobacco , 1989, Molecular and General Genetics MGG.

[30]  Y. Sun,et al.  Small heat shock proteins: molecular structure and chaperone function , 2005, Cellular and Molecular Life Sciences CMLS.

[31]  S. Shigeoka,et al.  Arabidopsis heat shock transcription factor A2 as a key regulator in response to several types of environmental stress. , 2006, The Plant journal : for cell and molecular biology.

[32]  P. Verslues,et al.  Mechanisms independent of abscisic acid (ABA) or proline feedback have a predominant role in transcriptional regulation of proline metabolism during low water potential and stress recovery. , 2010, Plant, cell & environment.

[33]  S. Rasmussen,et al.  Transcriptome Responses to Combinations of Stresses in Arabidopsis1[W][OA] , 2013, Plant Physiology.

[34]  Patrick Minnis,et al.  Dust aerosol effect on semi-arid climate over Northwest China detected from A-Train satellite measurements , 2010 .

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

[36]  M. Ishitani,et al.  Interaction of osmotic stress, temperature, and abscisic acid in the regulation of gene expression in Arabidopsis. , 1999, Plant physiology.

[37]  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.

[38]  L. Rensing,et al.  Heat shock effects on cell cycle progression , 2000, Cellular and Molecular Life Sciences CMLS.

[39]  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.

[40]  K. Akiyama,et al.  Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. , 2002, The Plant journal : for cell and molecular biology.

[41]  B. Mueller‐Roeber,et al.  Arabidopsis NAC transcription factor JUNGBRUNNEN1 affects thermomemory-associated genes and enhances heat stress tolerance in primed and unprimed conditions , 2012, Plant signaling & behavior.

[42]  Akira Oikawa,et al.  Pause-and-Stop: The Effects of Osmotic Stress on Cell Proliferation during Early Leaf Development in Arabidopsis and a Role for Ethylene Signaling in Cell Cycle Arrest[W] , 2011, Plant Cell.

[43]  S. Potter,et al.  Acquired resistance in Arabidopsis. , 1992, The Plant cell.

[44]  Johan Trygg,et al.  Consensus by Democracy. Using Meta-Analyses of Microarray and Genomic Data to Model the Cold Acclimation Signaling Pathway in Arabidopsis1[W] , 2006, Plant Physiology.

[45]  A. Tunnacliffe,et al.  LEA proteins prevent protein aggregation due to water stress. , 2005, The Biochemical journal.

[46]  Q. Lu,et al.  Chloroplast Small Heat Shock Protein HSP21 Interacts with Plastid Nucleoid Protein pTAC5 and Is Essential for Chloroplast Development in Arabidopsis under Heat Stress[W] , 2013, Plant Cell.

[47]  I. Hwang,et al.  A Vacuolar β-Glucosidase Homolog That Possesses Glucose-Conjugated Abscisic Acid Hydrolyzing Activity Plays an Important Role in Osmotic Stress Responses in Arabidopsis[W] , 2012, Plant Cell.

[48]  K. Shinozaki,et al.  A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. , 1994, The Plant cell.

[49]  E. Vierling,et al.  Core Genome Responses Involved in Acclimation to High Temperature1[C][W][OA] , 2007, Plant Physiology.

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

[51]  Xiaoyan Zhang,et al.  Lipid transfer protein 3 as a target of MYB96 mediates freezing and drought stress in Arabidopsis , 2013, Journal of experimental botany.