Transcriptional profiling of Arabidopsis heat shock proteins and transcription factors reveals extensive overlap between heat and non-heat stress response pathways

BackgroundThe heat shock response of Arabidopsis thaliana is dependent upon a complex regulatory network involving twenty-one known transcription factors and four heat shock protein families. It is known that heat shock proteins (Hsps) and transcription factors (Hsfs) are involved in cellular response to various forms of stress besides heat. However, the role of Hsps and Hsfs under cold and non-thermal stress conditions is not well understood, and it is unclear which types of stress interact least and most strongly with Hsp and Hsf response pathways. To address this issue, we have analyzed transcriptional response profiles of Arabidopsis Hsfs and Hsps to a range of abiotic and biotic stress treatments (heat, cold, osmotic stress, salt, drought, genotoxic stress, ultraviolet light, oxidative stress, wounding, and pathogen infection) in both above and below-ground plant tissues.ResultsAll stress treatments interact with Hsf and Hsp response pathways to varying extents, suggesting considerable cross-talk between heat and non-heat stress regulatory networks. In general, Hsf and Hsp expression was strongly induced by heat, cold, salt, and osmotic stress, while other types of stress exhibited family or tissue-specific response patterns. With respect to the Hsp20 protein family, for instance, large expression responses occurred under all types of stress, with striking similarity among expression response profiles. Several genes belonging to the Hsp20, Hsp70 and Hsp100 families were specifically upregulated twelve hours after wounding in root tissue, and exhibited a parallel expression response pattern during recovery from heat stress. Among all Hsf and Hsp families, large expression responses occurred under ultraviolet-B light stress in aerial tissue (shoots) but not subterranean tissue (roots).ConclusionOur findings show that Hsf and Hsp family member genes represent an interaction point between multiple stress response pathways, and therefore warrant functional analysis under conditions apart from heat shock treatment. In addition, our analysis revealed several family and tissue-specific heat shock gene expression patterns that have not been previously described. These results have implications regarding the molecular basis of cross-tolerance in plant species, and raise new questions to be pursued in future experimental studies of the Arabidopsis heat shock response network.

[1]  A. Hoffmann,et al.  Evolutionary Genetics and Environmental Stress , 1991 .

[2]  J. Keller,et al.  Proteasome inhibition in oxidative stress neurotoxicity: implications for heat shock proteins , 2001, Journal of neurochemistry.

[3]  Cornelia Göbel,et al.  Rapid Induction of Distinct Stress Responses after the Release of Singlet Oxygen in Arabidopsis Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.014662. , 2003, The Plant Cell Online.

[4]  N. Banzet,et al.  Accumulation of small heat shock proteins, including mitochondrial HSP22, induced by oxidative stress and adaptive response in tomato cells. , 1998, The Plant journal : for cell and molecular biology.

[5]  D. Inzé,et al.  Transcriptomic Footprints Disclose Specificity of Reactive Oxygen Species Signaling in Arabidopsis1[W] , 2006, Plant Physiology.

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

[7]  Stefan R. Henz,et al.  A gene expression map of Arabidopsis thaliana development , 2005, Nature Genetics.

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

[9]  H. Bohnert,et al.  Dissecting salt stress pathways. , 2006, Journal of experimental botany.

[10]  L. Young,et al.  Ethanol treatment triggers a heat shock‐like response but no thermotolerance in soybean (Glycine max cv. Kaohsiung No.8) seedlings , 2000 .

[11]  K. Yeh,et al.  Isolation and characterization of tomato Hsa32 encoding a novel heat-shock protein , 2006 .

[12]  T. Thomas,et al.  Differential regulation of small heat-shock genes in plants: analysis of a water-stress-inducible and developmentally activated sunflower promoter , 1996, Plant Molecular Biology.

[13]  M. Agarwal,et al.  Arabidopsis thaliana Hsp100 proteins: kith and kin , 2001, Cell stress & chaperones.

[14]  Garrett J. Lee,et al.  A small heat shock protein cooperates with heat shock protein 70 systems to reactivate a heat-denatured protein. , 2000, Plant physiology.

[15]  B. Thomas,et al.  Ultraviolet‐B‐induced stress and changes in gene expression in Arabidopsis thaliana: role of signalling pathways controlled by jasmonic acid, ethylene and reactive oxygen species , 1999 .

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

[17]  Rafael A. Irizarry,et al.  Bioinformatics and Computational Biology Solutions using R and Bioconductor , 2005 .

[18]  R. Mittler,et al.  Growth suppression, altered stomatal responses, and augmented induction of heat shock proteins in cytosolic ascorbate peroxidase (Apx1)-deficient Arabidopsis plants. , 2003, The Plant journal : for cell and molecular biology.

[19]  M. Van Montagu,et al.  Small heat shock proteins and stress tolerance in plants. , 2002, Biochimica et biophysica acta.

[20]  K. Scharf,et al.  Formation of cytoplasmic heat shock granules in tomato cell cultures and leaves , 1983, Molecular and cellular biology.

[21]  Kil-Jae Lee,et al.  Acquired tolerance to temperature extremes. , 2003, Trends in plant science.

[22]  A. Weber,et al.  Plastic and adaptive gene expression patterns associated with temperature stress in Arabidopsis thaliana , 2007, Heredity.

[23]  Yuxiang Cheng,et al.  rHsp90 gene expression in response to several environmental stresses in rice (Oryza sativa L.). , 2006, Plant physiology and biochemistry : PPB.

[24]  T. Murphy,et al.  A comparison of the effects of a fungal elicitor and ultraviolet radiation on ion transport and hydrogen peroxide synthesis by rose cells , 1991 .

[25]  R. Mittler,et al.  Could heat shock transcription factors function as hydrogen peroxide sensors in plants? , 2006, Annals of botany.

[26]  S. Chaufour,et al.  Mammalian small stress proteins protect against oxidative stress through their ability to increase glucose-6-phosphate dehydrogenase activity and by maintaining optimal cellular detoxifying machinery. , 1999, Experimental cell research.

[27]  Y. Hihara,et al.  DNA Microarray Analysis of Cyanobacterial Gene Expression during Acclimation to High Light , 2001, Plant Cell.

[28]  Jianhua Zhu,et al.  Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. , 2006, The Plant journal : for cell and molecular biology.

[29]  M. Delseny,et al.  Genomic analysis of the Hsp70 superfamily in Arabidopsis thaliana , 2001, Cell stress & chaperones.

[30]  J. Jo,et al.  Expression of the chloroplast-localized small heat shock protein by oxidative stress in rice. , 2000, Gene.

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

[32]  Jia Liu,et al.  Gene expression profiling of potato responses to cold, heat, and salt stress , 2005, Functional & Integrative Genomics.

[33]  N. Holbrook,et al.  Cellular response to oxidative stress: Signaling for suicide and survival * , 2002, Journal of cellular physiology.

[34]  K. Kregel,et al.  Heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance. , 2002, Journal of applied physiology.

[35]  C. Almoguera,et al.  Tissue-specific expression of sunflower heat shock proteins in response to water stress , 1993 .

[36]  Yoav Benjamini,et al.  Identifying differentially expressed genes using false discovery rate controlling procedures , 2003, Bioinform..

[37]  Y. Charng,et al.  Arabidopsis Hsa32, a Novel Heat Shock Protein, Is Essential for Acquired Thermotolerance during Long Recovery after Acclimation1[W] , 2006, Plant Physiology.

[38]  Tal Isaacson,et al.  Dual Role for Tomato Heat Shock Protein 21: Protecting Photosystem II from Oxidative Stress and Promoting Color Changes during Fruit Maturation , 2005, The Plant Cell Online.

[39]  G. Pastori,et al.  Common Components, Networks, and Pathways of Cross-Tolerance to Stress. The Central Role of “Redox” and Abscisic Acid-Mediated Controls1 , 2002, Plant Physiology.

[40]  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.

[41]  G. Gloor,et al.  The Hsp90 family of proteins in Arabidopsis thaliana , 2001, Cell stress & chaperones.

[42]  P. Mullineaux,et al.  A mutation affecting ASCORBATE PEROXIDASE 2 gene expression reveals a link between responses to high light and drought tolerance. , 2006, Plant, cell & environment.

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

[44]  K. Scharf,et al.  Arabidopsis and the heat stress transcription factor world: how many heat stress transcription factors do we need? , 2001, Cell stress & chaperones.

[45]  E. Vierling,et al.  The expression of small heat shock proteins in seeds responds to discrete developmental signals and suggests a general protective role in desiccation tolerance. , 2000, Plant physiology.

[46]  Jiahn-Chou Guan,et al.  Characterization of the genomic structures and selective expression profiles of nine class I small heat shock protein genes clustered on two chromosomes in rice (Oryza sativa L.) , 2004, Plant Molecular Biology.

[47]  K. Morris,et al.  Ultraviolet-B exposure leads to up-regulation of senescence-associated genes in Arabidopsis thaliana. , 2001, Journal of experimental botany.

[48]  R. Fluhr,et al.  The role of calcium and activated oxygens as signals for controlling cross-tolerance. , 2000, Trends in plant science.

[49]  E. Vierling,et al.  The expanding family of Arabidopsis thaliana small heat stress proteins and a new family of proteins containing α-crystallin domains (Acd proteins) , 2001, Cell stress & chaperones.

[50]  R. Mittler,et al.  The Zinc-Finger Protein Zat12 Plays a Central Role in Reactive Oxygen and Abiotic Stress Signaling in Arabidopsis1[w] , 2005, Plant Physiology.

[51]  A. Reindl,et al.  Update on Signal Transduction Regulation of the Heat-Shock Response , 1998 .

[52]  R. Volkov,et al.  Heat stress-induced H2O2 is required for effective expression of heat shock genes in Arabidopsis , 2006, Plant Molecular Biology.

[53]  L. Hennig,et al.  Arabidopsis transcript profiling on Affymetrix GeneChip arrays , 2003, Plant Molecular Biology.

[54]  P. Mehlen,et al.  Analysis of the resistance to heat and hydrogen peroxide stresses in COS cells transiently expressing wild type or deletion mutants of the Drosophila 27-kDa heat-shock protein. , 1993, European journal of biochemistry.

[55]  J. Sánchez-Serrano,et al.  Wound signalling in plants. , 2001, Journal of experimental botany.

[56]  Katherine S. Pollard,et al.  Cluster Analysis of Genomic Data , 2005 .

[57]  Erik T. Bieschke,et al.  Muscle-specific expression of Drosophila hsp70 in response to aging and oxidative stress. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[58]  I. Horváth,et al.  Small heat-shock proteins regulate membrane lipid polymorphism , 2002, Proceedings of the National Academy of Sciences of the United States of America.

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

[60]  Mark J. van der Laan,et al.  Hybrid Clustering of Gene Expression Data with Visualization and the Bootstrap , 2001 .

[61]  D. Weiss,et al.  Expression of small heat-shock proteins at low temperatures. A possible role in protecting against chilling injuries. , 1998, Plant physiology.

[62]  J. K. Roberts,et al.  Acquisition of Thermotolerance in Soybean Seedlings : Synthesis and Accumulation of Heat Shock Proteins and their Cellular Localization. , 1984, Plant physiology.

[63]  C. Laloi,et al.  Reactive oxygen signalling: the latest news. , 2004, Current opinion in plant biology.

[64]  Rafael A. Irizarry,et al.  A Model-Based Background Adjustment for Oligonucleotide Expression Arrays , 2004 .

[65]  Tse-Min Lee,et al.  Journal of Experimental Botany Advance Access published September 12, 2005 Journal of Experimental Botany, Page 1 of 15 , 2005 .

[66]  B. Pogson,et al.  Global Changes in Gene Expression in Response to High Light in Arabidopsis1,212 , 2002, Plant Physiology.

[67]  M. Van Montagu,et al.  At-HSP17.6A, encoding a small heat-shock protein in Arabidopsis, can enhance osmotolerance upon overexpression. , 2001, The Plant journal : for cell and molecular biology.

[68]  L. Nover,et al.  Cytosolic heat-stress proteins Hsp17.7 class I and Hsp17.3 class II of tomato act as molecular chaperones in vivo , 2000, Planta.

[69]  Garrett J. Lee,et al.  A small heat shock protein stably binds heat‐denatured model substrates and can maintain a substrate in a folding‐competent state , 1997, The EMBO journal.

[70]  R. Volkov,et al.  Heat Stress- and Heat Shock Transcription Factor-Dependent Expression and Activity of Ascorbate Peroxidase in Arabidopsis1 , 2002, Plant Physiology.

[71]  Mark J. van der Laan,et al.  A new algorithm for hybrid hierarchical clustering with visualization and the bootstrap , 2003 .

[72]  J. Hancock,et al.  Regulation of the Arabidopsis transcriptome by oxidative stress. , 2001, Plant physiology.

[73]  A. Niedzwiecki,et al.  Role of oxidative stress in Drosophila aging. , 1992, Mutation research.

[74]  Gordon K Smyth,et al.  Statistical Applications in Genetics and Molecular Biology Linear Models and Empirical Bayes Methods for Assessing Differential Expression in Microarray Experiments , 2011 .

[75]  H. Hirt,et al.  Alfalfa heat shock genes are differentially expressed during somatic embryogenesis , 1991, Plant Molecular Biology.

[76]  Dan Nettleton,et al.  A Discussion of Statistical Methods for Design and Analysis of Microarray Experiments for Plant Scientists , 2006, The Plant Cell Online.

[77]  R. Fluhr,et al.  UV-B-Induced PR-1 Accumulation Is Mediated by Active Oxygen Species. , 1995, The Plant cell.

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

[79]  J. Bornman,et al.  The chloroplast small heat shock protein undergoes oxidation-dependent conformational changes and may protect plants from oxidative stress. , 1999, Cell stress & chaperones.