Comparative physiology and transcriptional networks underlying the heat shock response in Populus trichocarpa, Arabidopsis thaliana and Glycine max.

The heat shock response continues to be layered with additional complexity as interactions and crosstalk among heat shock proteins (HSPs), the reactive oxygen network and hormonal signalling are discovered. However, comparative analyses exploring variation in each of these processes among species remain relatively unexplored. In controlled environment experiments, photosynthetic response curves were conducted from 22 to 42 °C and indicated that temperature optimum of light-saturated photosynthesis was greater for Glycine max relative to Arabidopsis thaliana or Populus trichocarpa. Transcript profiles were taken at defined states along the temperature response curves, and inferred pathway analysis revealed species-specific variation in the abiotic stress and the minor carbohydrate raffinose/galactinol pathways. A weighted gene co-expression network approach was used to group individual genes into network modules linking biochemical measures of the antioxidant system to leaf-level photosynthesis among P. trichocarpa, G. max and A. thaliana. Network-enabled results revealed an expansion in the G. max HSP17 protein family and divergence in the regulation of the antioxidant and heat shock modules relative to P. trichocarpa and A. thaliana. These results indicate that although the heat shock response is highly conserved, there is considerable species-specific variation in its regulation.

[1]  D. Oosterhuis,et al.  Genotypic differences in thermotolerance are dependent upon prestress capacity for antioxidant protection of the photosynthetic apparatus in Gossypium hirsutum. , 2010, Physiologia plantarum.

[2]  Staffan Persson,et al.  Co-expression tools for plant biology: opportunities for hypothesis generation and caveats. , 2009, Plant, cell & environment.

[3]  Mark Stitt,et al.  A guide to using MapMan to visualize and compare Omics data in plants: a case study in the crop species, Maize. , 2009, Plant, cell & environment.

[4]  M. Angilletta.  Looking for answers to questions about heat stress: researchers are getting warmer , 2009 .

[5]  K. Scharf,et al.  Functional dissection of the cytosolic chaperone network in tomato mesophyll protoplasts. , 2009, Plant, cell & environment.

[6]  Lijun Luo,et al.  Photosynthetic metabolism of C3 plants shows highly cooperative regulation under changing environments: A systems biological analysis , 2009, Proceedings of the National Academy of Sciences.

[7]  N. Smirnoff,et al.  Antioxidant status, peroxidase activity, and PR protein transcript levels in ascorbate-deficient Arabidopsis thaliana vtc mutants. , 2008, Journal of experimental botany.

[8]  D. Los,et al.  Heat stress: an overview of molecular responses in photosynthesis , 2008, Photosynthesis Research.

[9]  G. Stacey,et al.  Identification of Four Soybean Reference Genes for Gene Expression Normalization , 2008 .

[10]  S. Shigeoka,et al.  Galactinol and Raffinose Constitute a Novel Function to Protect Plants from Oxidative Damage1[W][OA] , 2008, Plant Physiology.

[11]  N. Dudai,et al.  Antioxidant activity and phenol content of plant germplasm originating in the Dead Sea area , 2008 .

[12]  Rex T. Nelson,et al.  Microsatellite discovery from BAC end sequences and genetic mapping to anchor the soybean physical and genetic maps. , 2008, Genome.

[13]  E. Vierling,et al.  Heat shock protein 101 effects in A. thaliana: genetic variation, fitness and pleiotropy in controlled temperature conditions , 2008, Molecular ecology.

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

[15]  A. Wahid,et al.  Heat tolerance in plants: An overview , 2007 .

[16]  E. Vierling,et al.  Plant Responses to High Temperature , 2007 .

[17]  R. Sage,et al.  The temperature response of C(3) and C(4) photosynthesis. , 2007, Plant, cell & environment.

[18]  D. Weston,et al.  Inhibition and acclimation of C(3) photosynthesis to moderate heat: a perspective from thermally contrasting genotypes of Acer rubrum (red maple). , 2007, Tree physiology.

[19]  M. Nei,et al.  MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. , 2007, Molecular biology and evolution.

[20]  N. Suzuki,et al.  Double Mutants Deficient in Cytosolic and Thylakoid Ascorbate Peroxidase Reveal a Complex Mode of Interaction between Reactive Oxygen Species, Plant Development, and Response to Abiotic Stresses1[W][OA] , 2007, Plant Physiology.

[21]  D. Weston,et al.  Characterization of Rubisco activase from thermally contrasting genotypes of Acer rubrum (Aceraceae). , 2007, American journal of botany.

[22]  Klaus-Dieter Scharf,et al.  Complexity of the heat stress response in plants. , 2007, Current opinion in plant biology.

[23]  E. Ainsworth,et al.  Rapid measurement of total antioxidant capacity in plants , 2007, Nature Protocols.

[24]  Yves Gibon,et al.  PageMan: An interactive ontology tool to generate, display, and annotate overview graphs for profiling experiments , 2006, BMC Bioinformatics.

[25]  William R. Swindell,et al.  The Association Among Gene Expression Responses to Nine Abiotic Stress Treatments in Arabidopsis thaliana , 2006, Genetics.

[26]  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.

[27]  R. Sairam,et al.  Protective role of antioxidant enzymes under high temperature stress. , 2006, Plant science : an international journal of experimental plant biology.

[28]  M. Gribskov,et al.  The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray) , 2006, Science.

[29]  K. Asada.  Production and Scavenging of Reactive Oxygen Species in Chloroplasts and Their Functions1 , 2006, Plant Physiology.

[30]  R. Gentleman.  Bioinformatics and Computational Biology Solutions Using R and Bioconductor , 2006 .

[31]  J. Mesirov,et al.  From the Cover: Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles , 2005 .

[32]  Joachim Selbig,et al.  Extension of the Visualization Tool MapMan to Allow Statistical Analysis of Arrays, Display of Coresponding Genes, and Comparison with Known Responses1 , 2005, Plant Physiology.

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

[34]  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.

[35]  J. Raes,et al.  Modeling gene and genome duplications in eukaryotes. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[36]  Thomas D. Sharkey,et al.  Effects of moderate heat stress on photosynthesis: importance of thylakoid reactions, rubisco deactivation, reactive oxygen species, and thermotolerance provided by isoprene , 2005 .

[37]  Darren J. Wilkinson,et al.  Modelling the actions of chaperones and their role in ageing , 2005, Mechanisms of Ageing and Development.

[38]  Karen Schlauch,et al.  Cytosolic Ascorbate Peroxidase 1 Is a Central Component of the Reactive Oxygen Gene Network of Arabidopsisw⃞ , 2005, The Plant Cell Online.

[39]  Wolfgang Busch,et al.  Identification of novel heat shock factor-dependent genes and biochemical pathways in Arabidopsis thaliana. , 2004, The Plant journal : for cell and molecular biology.

[40]  A. Wachter,et al.  Differential targeting of GSH1 and GSH2 is achieved by multiple transcription initiation: implications for the compartmentation of glutathione biosynthesis in the Brassicaceae. , 2004, The Plant journal : for cell and molecular biology.

[41]  H. Stransky,et al.  Galactinol synthase1. A Novel Heat Shock Factor Target Gene Responsible for Heat-Induced Synthesis of Raffinose Family Oligosaccharides in Arabidopsis1[w] , 2004, Plant Physiology.

[42]  R. Mittler,et al.  Reactive oxygen gene network of plants. , 2004, Trends in plant science.

[43]  Rainer Breitling,et al.  Rank products: a simple, yet powerful, new method to detect differentially regulated genes in replicated microarray experiments , 2004, FEBS letters.

[44]  A. Portis,et al.  Oxygen‐dependent H2O2 production by Rubisco , 2004, FEBS letters.

[45]  C. Weber,et al.  Role of Hsp17.4-CII as Coregulator and Cytoplasmic Retention Factor of Tomato Heat Stress Transcription Factor HsfA21 , 2004, Plant Physiology.

[46]  Stephen M. Schrader,et al.  Thylakoid membrane responses to moderately high leaf temperature in Pima cotton , 2004 .

[47]  Tania June,et al.  A simple new equation for the reversible temperature dependence of photosynthetic electron transport: a study on soybean leaf. , 2004, Functional plant biology : FPB.

[48]  S. Rhee,et al.  MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. , 2004, The Plant journal : for cell and molecular biology.

[49]  Z. Oltvai,et al.  Network biology: understanding the cell's functional organization , 2004, Nature Reviews Genetics.

[50]  S. Heckathorn,et al.  Variation in chloroplast small heat-shock protein function is a major determinant of variation in thermotolerance of photosynthetic electron transport among ecotypes of Chenopodium album. , 2003, Functional plant biology : FPB.

[51]  Y. Iwasa,et al.  Optimal choice between feedforward and feedback control in gene expression to cope with unpredictable danger. , 2003, Journal of theoretical biology.

[52]  D. Malencic,et al.  Stress Tolerance Parameters in Different Genotypes of Soybean , 2003, Biologia Plantarum.

[53]  D. Hincha,et al.  The preservation of liposomes by raffinose family oligosaccharides during drying is mediated by effects on fusion and lipid phase transitions. , 2003, Biochimica et biophysica acta.

[54]  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.

[55]  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.

[56]  Denis Loustau,et al.  Temperature response of parameters of a biochemically based model of photosynthesis. II. A review of experimental data , 2002 .

[57]  S. Heckathorn,et al.  In vivo evidence from an Agrostis stolonifera selection genotype that chloroplast small heat-shock proteins can protect photosystem II during heat stress. , 2002, Functional plant biology : FPB.

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

[59]  M. Knight,et al.  Protection against Heat Stress-Induced Oxidative Damage in Arabidopsis Involves Calcium, Abscisic Acid, Ethylene, and Salicylic Acid , 2002, Plant Physiology.

[60]  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.

[61]  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.

[62]  D. Abarca,et al.  Arabidopsis thaliana ecotype Cvi shows an increased tolerance to photo-oxidative stress and contains a new chloroplastic copper/zinc superoxide dismutase isoenzyme. , 2001, Journal of experimental botany.

[63]  G. Balogh,et al.  Synechocystis HSP17 is an amphitropic protein that stabilizes heat-stressed membranes and binds denatured proteins for subsequent chaperone-mediated refolding , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[64]  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.

[65]  S Airaksinen,et al.  Heat-shock protein expression is absent in the antarctic fish Trematomus bernacchii (family Nototheniidae). , 2000, The Journal of experimental biology.

[66]  Malik,et al.  Modified expression of a carrot small heat shock protein gene, hsp17. 7, results in increased or decreased thermotolerancedouble dagger , 1999, The Plant journal : for cell and molecular biology.

[67]  R. Morimoto.  Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. , 1998, Genes & development.

[68]  K. Hinderhofer,et al.  HSF3, a new heat shock factor from Arabidopsis thaliana, derepresses the heat shock response and confers thermotolerance when overexpressed in transgenic plants , 1998, Molecular and General Genetics MGG.

[69]  L. Jouanin,et al.  Synthesis of Glutathione in Leaves of Transgenic Poplar Overexpressing [gamma]-Glutamylcysteine Synthetase , 1996, Plant physiology.

[70]  M. Havaux,et al.  Temperature-dependent adjustment of the thermal stability of photosystem II in vivo: possible involvement of xanthophyll-cycle pigments , 1996, Planta.

[71]  J. McDowell,et al.  Strong, constitutive expression of the Arabidopsis ACT2/ACT8 actin subclass in vegetative tissues. , 1996, The Plant journal : for cell and molecular biology.

[72]  Satoshi Naito,et al.  The Arabidopsis HSP18.2 promoter/GUS gene fusion in transgenic Arabidopsis plants: a powerful tool for the isolation of regulatory mutants of the heat‐shock response , 1992 .

[73]  T. Kuo,et al.  Purification and characterization of galactinol synthase from mature zucchini squash leaves. , 1991, Plant physiology.

[74]  H. Bode,et al.  Thermotolerance and synthesis of heat shock proteins: these responses are present in Hydra attenuata but absent in Hydra oligactis. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[75]  M. A. Mansfield,et al.  Synthesis of the low molecular weight heat shock proteins in plants. , 1987, Plant physiology.

[76]  A. Necchi,et al.  Early and late heat shock proteins in wheats and other cereal species. , 1987, Plant physiology.

[77]  P. Nobel,et al.  Concomitant changes in high temperature tolerance and heat-shock proteins in desert succulents. , 1986, Plant physiology.

[78]  J. Felsenstein.  CONFIDENCE LIMITS ON PHYLOGENIES: AN APPROACH USING THE BOOTSTRAP , 1985, Evolution; international journal of organic evolution.

[79]  J. Berry,et al.  Photosynthetic Response and Adaptation to Temperature in Higher Plants , 1980 .

[80]  S. Horvath,et al.  A General Framework for Weighted Gene Co-Expression Network Analysis , 2005, Statistical applications in genetics and molecular biology.

[81]  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 .

[82]  M. Angilletta.  Thermal Adaptation: A Theoretical and Empirical Synthesis , 2009 .

[83]  E. Waters,et al.  Comparative analysis of the small heat shock proteins in three angiosperm genomes identifies new subfamilies and reveals diverse evolutionary patterns , 2008, Cell Stress and Chaperones.

[84]  N. Suzuki,et al.  Reactive oxygen species and temperature stresses: A delicate balance between signaling and destruction , 2006 .

[85]  Y. Ahn,et al.  Introduction of the carrot HSP17.7 into potato (Solanum tuberosum L.) enhances cellular membrane stability and tuberization in vitro. , 2006, Plant, cell & environment.

[86]  BMC Genomics BioMed Central , 2006 .

[87]  Gordon K. Smyth,et al.  limma: Linear Models for Microarray Data , 2005 .

[88]  Bingru Huang,et al.  Thermotolerance and antioxidant systems in Agrostis stolonifera: involvement of salicylic acid, abscisic acid, calcium, hydrogen peroxide, and ethylene. , 2004, Journal of plant physiology.

[89]  S. Long,et al.  The growth of soybean under free air [CO2] enrichment (FACE) stimulates photosynthesis while decreasing in vivo Rubisco capacity , 2004, Planta.

[90]  Yoon-Chul Choy,et al.  CADLIVE System: Map-Based Dynamic Simulation of Biochemical Networks , 2003 .

[91]  N. Mohanty,et al.  Response of seedlings to heat-stress in cultivars of wheat: Growth temperature-dependent differential modulation of photosystem 1 and 2 activity, and foliar antioxidant defense capacity , 2002 .

[92]  S. Heckathorn,et al.  The small, methionine-rich chloroplast heat-shock protein protects photosystem II electron transport during heat stress. , 1998, Plant physiology.

[93]  Xianrang Song,et al.  Maturation of a central , 1996 .

[94]  M. Havaux.  Characterization of thermal damage to the photosynthetic electron transport system in potato leaves , 1993 .

[95]  S. Lindquist.  The heat-shock response. , 1986, Annual review of biochemistry.

[96]  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.

[97]  L. Pauling,et al.  Evolutionary Divergence and Convergence in Proteins , 1965 .

[98]  Journal of Experimental Botany, Page 1 of 11 doi:10.1093/jxb/erm343 SPECIAL ISSUE REVIEW PAPER , 2022 .