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Coexpression network analysis associated with call of rice seedlings for encountering heat stress

Plant Molecular Biology volume 84, pages 125–143 (2014)Cite this article

Abstract

Coexpression network analysis is useful tool for identification of functional association of coexpressed genes. We developed a coexpression network of rice from heat stress transcriptome data. Global transcriptome of rice leaf tissues was performed by microarray at three time points—post 10 and 60 min heat stress at 42 °C and 30 min recovery at 26 °C following 60 min 42 °C heat stress to investigate specifically the early events in the heat stress and recovery response. The transcriptome profile was significantly modulated within 10 min of heat stress. Strikingly, the number of up-regulated genes was higher than the number of down-regulated genes in 10 min of heat stress. The enrichment of GO terms protein kinase activity/protein serine threonine kinase activity, response to heat and reactive oxygen species in up-regulated genes after 10 min signifies the role of signal transduction events and reactive oxygen species during early heat stress. The enrichment of transcription factor (TF) binding sites for heat shock factors, bZIPs and DREBs coupled with up-regulation of TFs of different families suggests that the heat stress response in rice involves integration of various regulatory networks. The interpretation of microarray data in the context of coexpression network analysis identified several functionally correlated genes consisting of previously documented heat upregulated genes as well as new genes that can be implicated in heat stress. Based on the findings on parallel analysis of growth of seedlings, associated changes in transcripts of selected Hsps, genome-wide microarray profiling and the coexpression network analysis, this study is a step forward in understanding heat response of rice, the world’s most important food crop.

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References

  • Agarwal M, Sahi C, Katiyar-Agarwal S, Agarwal S, Young T, Gallie DR, Sharma VM, Ganesan K, Grover A (2003) Molecular characterization of rice hsp101: complementation of yeast hsp104 mutation by disaggregation of protein granules and differential expression in indica and japonica rice types. Plant Mol Biol 51:543–553

    PubMed  Article  CAS  Google Scholar 

  • Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G (2000) Gene ontology: tool for the unification of biology. The gene ontology consortium. Nat Genet 25:25–29

    PubMed  Article  CAS  Google Scholar 

  • Aviezer-Hagai K, Skovorodnikova J, Galigniana M, Farchi-Pisanty O, Maayan E, Bocovza S, Efrat Y, von Koskull-Doring P, Ohad N, Breiman A (2007) Arabidopsis immunophilins ROF1 (AtFKBP62) and ROF2 (AtFKBP65) exhibit tissue specificity, are heat-stress induced, and bind HSP90. Plant Mol Biol 63:237–255

    PubMed  Article  CAS  Google Scholar 

  • Busch W, Wunderlich M, Schoffl F (2005) Identification of novel heat shock factor-dependent genes and biochemical pathways in Arabidopsis thaliana. Plant J 41:1–14

    PubMed  Article  CAS  Google Scholar 

  • Charng YY, Liu HC, Liu NY, Hsu FC, Ko SS (2006) Arabidopsis Hsa32, a novel heat shock protein, is essential for acquired thermotolerance during long recovery after acclimation. Plant Physiol 140:1297–1305

    PubMed  Article  CAS  Google Scholar 

  • Chen H, Hwang JE, Lim CJ, Kim DY, Lee SY, Lim CO (2010) Arabidopsis DREB2C functions as a transcriptional activator of HsfA3 during the heat stress response. Biochem Biophys Res Commun 401:238–244

    PubMed  Article  CAS  Google Scholar 

  • Cheng C, Yun KY, Ressom HW, Mohanty B, Bajic VB, Jia Y, Yun SJ, de los Reyes BG (2007) An early response regulatory cluster induced by low temperature and hydrogen peroxide in seedlings of chilling-tolerant japonica rice. BMC Genomics 8:175

    PubMed  Article  Google Scholar 

  • Evrard A, Kumar M, Lecourieux D, Lucks J, von Koskull-Doring P, Hirt H (2013) Regulation of the heat stress response in Arabidopsis by MPK6-targeted phosphorylation of the heat stress factor HsfA2. PeerJ 1:e59

    PubMed  Article  Google Scholar 

  • Fernandes J, Morrow DJ, Casati P, Walbot V (2008) Distinctive transcriptome responses to adverse environmental conditions in Zea mays L. Plant Biotechnol J 6:782–798

    PubMed  Article  CAS  Google Scholar 

  • Ficklin SP, Luo F, Feltus FA (2010) The association of multiple interacting genes with specific phenotypes in rice using gene coexpression networks. Plant Physiol 154:13–24

    PubMed  Article  CAS  Google Scholar 

  • Gammulla CG, Pascovici D, Atwell BJ, Haynes PA (2010) Differential metabolic response of cultured rice (Oryza sativa) cells exposed to high- and low-temperature stress. Proteomics 10:3001–3019

    PubMed  Article  CAS  Google Scholar 

  • Gao H, Brandizzi F, Benning C, Larkin RM (2008) A membrane-tethered transcription factor defines a branch of the heat stress response in Arabidopsis thaliana. Proc Natl Acad Sci USA 105:16398–16403

    PubMed  Article  CAS  Google Scholar 

  • Garg AK, Kim JK, Owens TG, Ranwala AP, Choi YD, Kochian LV, Wu RJ (2002) Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proc Natl Acad Sci USA 99:15898–15903

    PubMed  Article  CAS  Google Scholar 

  • Guertin MJ, Lis JT (2010) Chromatin landscape dictates HSF binding to target DNA elements. PLoS Genet 6:e1001114

    Google Scholar 

  • Hahn JS, Hu Z, Thiele DJ, Iyer VR (2004) Genome-wide analysis of the biology of stress responses through heat shock transcription factor. Mol Cell Biol 24:5249–5256

    PubMed  Article  CAS  Google Scholar 

  • Hahn A, Bublak D, Schleiff E, Scharf KD (2011) Crosstalk between Hsp90 and Hsp70 chaperones and heat stress transcription factors in tomato. Plant Cell 23:741–755

    PubMed  Article  CAS  Google Scholar 

  • Hayashi S, Wakasa Y, Takahashi H, Kawakatsu T, Takaiwa F (2011) Signal transduction by IRE1-mediated splicing of bZIP50 and other stress sensors in the endoplasmic reticulum stress response of rice. Plant J 69:946–956

    PubMed  Article  Google Scholar 

  • Hu W, Hu G, Han B (2009) Genome-wide survey and expression profiling of heat shock proteins and heat shock factors revealed overlapped and stress specific response under abiotic stresses in rice. Plant Sci 176:583–590

    Article  CAS  Google Scholar 

  • Jung K-H, Ko H-J, Nguyen MX, Kim S-R, Ronald P, An G (2012) Genome-wide identification and analysis of early heat stress responsive genes in rice. J Plant Biol 55:458–468

    Article  CAS  Google Scholar 

  • Kanchiswamy CN, Muroi A, Maffei ME, Yoshioka H, Sawasaki T, Arimura G (2010) Ca2+ dependent protein kinases and their substrate HsfB2a are differently involved in the heat response signaling pathway in Arabidopsis. Plant Biotechnol 27:470–473

    Google Scholar 

  • Katiyar-Agarwal S, Agarwal M, Grover A (2003) Heat-tolerant basmati rice engineered by over-expression of hsp101. Plant Mol Biol 51:677–686

    PubMed  Article  CAS  Google Scholar 

  • Keunen E, Peshev D, Vangronsveld J, W VDE, Cuypers A (2013) Plant sugars are crucial players in the oxidative challenge during abiotic stress: extending the traditional concept. Plant Cell Environ 36:1242–1255

    Google Scholar 

  • Kobayashi M, Ohura I, Kawakita K, Yokota N, Fujiwara M, Shimamoto K, Doke N, Yoshioka H (2007) Calcium-dependent protein kinases regulate the production of reactive oxygen species by potato NADPH oxidase. Plant Cell 19:1065–1080

    PubMed  Article  CAS  Google Scholar 

  • Kovacs D, Kalmar E, Torok Z, Tompa P (2008) Chaperone activity of ERD10 and ERD14, two disordered stress-related plant proteins. Plant Physiol 147:381–390

    PubMed  Article  CAS  Google Scholar 

  • Kovtun Y, Chiu WL, Tena G, Sheen J (2000) Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc Natl Acad Sci USA 97:2940–2945

    PubMed  Article  CAS  Google Scholar 

  • Larkindale J, Vierling E (2008) Core genome responses involved in acclimation to high temperature. Plant Physiol 146:748–761

    PubMed  Article  CAS  Google Scholar 

  • Lee TH, Kim YK, Pham TT, Song SI, Kim JK, Kang KY, An G, Jung KH, Galbraith DW, Kim M, Yoon UH, Nahm BH (2009) RiceArrayNet: a database for correlating gene expression from transcriptome profiling, and its application to the analysis of coexpressed genes in rice. Plant Physiol 151:16–33

    PubMed  Article  CAS  Google Scholar 

  • Lee I, Seo YS, Coltrane D, Hwang S, Oh T, Marcotte EM, Ronald PC (2011) Genetic dissection of the biotic stress response using a genome-scale gene network for rice. Proc Natl Acad Sci USA 108:18548–18553

    PubMed  Article  CAS  Google Scholar 

  • Lenka SK, Katiyar A, Chinnusamy V, Bansal KC (2010) Comparative analysis of drought-responsive transcriptome in Indica rice genotypes with contrasting drought tolerance. Plant Biotechnol J 9:315–327

    PubMed  Article  Google Scholar 

  • Less H, Galili G (2008) Principal transcriptional programs regulating plant amino acid metabolism in response to abiotic stresses. Plant Physiol 147:316–330

    PubMed  Article  CAS  Google Scholar 

  • Li B, Liu HT, Sun DY, Zhou RG (2004) Ca2+ and calmodulin modulate DNA-binding activity of maize heat shock transcription factor in vitro. Plant Cell Physiol 45:627–634

    PubMed  Article  CAS  Google Scholar 

  • Li S, Zhou X, Chen L, Huang W, Yu D (2010) Functional characterization of Arabidopsis thaliana WRKY39 in heat stress. Mol Cells 29:475–483

    PubMed  Article  CAS  Google Scholar 

  • Li S, Fu Q, Chen L, Huang W, Yu D (2011) Arabidopsis thaliana WRKY25, WRKY26, and WRKY33 coordinate induction of plant thermotolerance. Planta 233:1237–1252

    PubMed  Article  CAS  Google Scholar 

  • Li CR, Liang DD, Li J, Duan YB, Li H, Yang YC, Qin RY, Li L, Wei PC, Yang JB (2013) Unravelling mitochondrial retrograde regulation in the abiotic stress induction of rice alternative oxidase 1 genes. Plant, Cell Environ 36:775–788

    Article  CAS  Google Scholar 

  • Liu HT, Li GL, Chang H, Sun DY, Zhou RG, Li B (2007a) Calmodulin-binding protein phosphatase PP7 is involved in thermotolerance in Arabidopsis. Plant, Cell Environ 30:156–164

    Article  CAS  Google Scholar 

  • Liu JX, Srivastava R, Che P, Howell SH (2007b) An endoplasmic reticulum stress response in Arabidopsis is mediated by proteolytic processing and nuclear relocation of a membrane-associated transcription factor, bZIP28. Plant Cell 19:4111–4119

    PubMed  Article  CAS  Google Scholar 

  • Liu HT, Gao F, Li GL, Han JL, Liu DL, Sun DY, Zhou RG (2008) The calmodulin-binding protein kinase 3 is part of heat-shock signal transduction in Arabidopsis thaliana. Plant J 55:760–773

    PubMed  Article  CAS  Google Scholar 

  • Liu J, Sun N, Liu M, Du B, Wang X, Qi X (2013) An autoregulatory loop controlling Arabidopsis HsfA2 expression: role of heat shock-induced alternative splicing. Plant Physiol 162:512–521

    PubMed  Article  CAS  Google Scholar 

  • Lu SJ, Yang ZT, Sun L, Song ZT, Liu JX (2012) Conservation of IRE1-regulated bZIP74 mRNA unconventional splicing in rice (Oryza sativa L.) involved in ER stress responses. Mol Plant 212:504–514

    Article  Google Scholar 

  • Matsukura S, Mizoi J, Yoshida T, Todaka D, Ito Y, Maruyama K, Shinozaki K, Yamaguchi-Shinozaki K (2010) Comprehensive analysis of rice DREB2-type genes that encode transcription factors involved in the expression of abiotic stress-responsive genes. Mol Genet Genomics 283:185–196

    PubMed  Article  CAS  Google Scholar 

  • Matsuura H, Ishibashi Y, Shinmyo A, Kanaya S, Kato K (2010) Genome-wide analyses of early translational responses to elevated temperature and high salinity in Arabidopsis thaliana. Plant Cell Physiol 51:448–462

    PubMed  Article  CAS  Google Scholar 

  • Meiri D, Breiman A (2009) Arabidopsis ROF1 (FKBP62) modulates thermotolerance by interacting with HSP90.1 and affecting the accumulation of HsfA2-regulated sHSPs. Plant J 59:387–399

    PubMed  Article  CAS  Google Scholar 

  • Miller G, Mittler R (2006) Could heat shock transcription factors function as hydrogen peroxide sensors in plants? Ann Bot 98:279–288

    PubMed  Article  CAS  Google Scholar 

  • Mishkind M, Vermeer JE, Darwish E, Munnik T (2009) Heat stress activates phospholipase D and triggers PIP accumulation at the plasma membrane and nucleus. Plant J 60:10–21

    PubMed  Article  CAS  Google Scholar 

  • Mittal D, Madhyastha DA, Grover A (2012) Genome-wide transcriptional profiles during temperature and oxidative stress reveal coordinated expression patterns and overlapping regulons in rice. PLoS ONE 7:e40899

    PubMed  Article  CAS  Google Scholar 

  • Morris RT, O’Connor TR, Wyrick JJ (2008) Osiris: an integrated promoter database for Oryza sativa L. Bioinformatics 24:2915–2917

    PubMed  Article  CAS  Google Scholar 

  • Murakami Y, Toriyama K (2008) Enhanced high temperature tolerance in transgenic rice seedlings with elevated levels of alternative oxidase, OsAOX1a. Plant Biotechnol 25:361–364

    Article  CAS  Google Scholar 

  • Mutwil M, Klie S, Tohge T, Giorgi FM, Wilkins O, Campbell MM, Fernie AR, Usadel B, Nikoloski Z, Persson S (2011) PlaNet: combined sequence and expression comparisons across plant networks derived from seven species. Plant Cell 23:895–910

    PubMed  Article  CAS  Google Scholar 

  • Ning J, Liu S, Hu H, Xiong L (2008) Systematic analysis of NPK1-like genes in rice reveals a stress-inducible gene cluster co-localized with a quantitative trait locus of drought resistance. Mol Genet Genomics 280:535–546

    PubMed  Article  CAS  Google Scholar 

  • Oh SJ, Song SI, Kim YS, Jang HJ, Kim SY, Kim M, Kim YK, Nahm BH, Kim JK (2005) Arabidopsis CBF3/DREB1A and ABF3 in transgenic rice increased tolerance to abiotic stress without stunting growth. Plant Physiol 138:341–351

    PubMed  Article  CAS  Google Scholar 

  • Park SH, Chung PJ, Juntawong P, Bailey-Serres J, Kim YS, Jung H, Bang SW, Kim YK, Do Choi Y, Kim JK (2012) Posttranscriptional control of photosynthetic mRNA decay under stress conditions requires 3′ and 5′ untranslated regions and correlates with differential polysome association in rice. Plant Physiol 159:1111–1124

    PubMed  Article  CAS  Google Scholar 

  • Peng S, Huang J, Sheehy JE, Laza RC, Visperas RM, Zhong X, Centeno GS, Khush GS, Cassman KG (2004) Rice yields decline with higher night temperature from global warming. Proc Natl Acad Sci USA 101:9971–9975

    PubMed  Article  CAS  Google Scholar 

  • Qin F, Kakimoto M, Sakuma Y, Maruyama K, Osakabe Y, Tran LS, Shinozaki K, Yamaguchi-Shinozaki K (2007) Regulation and functional analysis of ZmDREB2A in response to drought and heat stresses in Zea mays L. Plant J 50:54–69

    PubMed  Article  CAS  Google Scholar 

  • Qin D, Wu H, Peng H, Yao Y, Ni Z, Li Z, Zhou C, Sun Q (2008) Heat stress-responsive transcriptome analysis in heat susceptible and tolerant wheat (Triticum aestivum L.) by using Wheat Genome Array. BMC Genomics 9:432

    PubMed  Article  Google Scholar 

  • Rabbani MA, Maruyama K, Abe H, Khan MA, Katsura K, Ito Y, Yoshiwara K, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Monitoring expression profiles of rice genes under cold, drought, and high-salinity stresses and abscisic acid application using cDNA microarray and RNA gel-blot analyses. Plant Physiol 133:1755–1767

    PubMed  Article  CAS  Google Scholar 

  • Reddy AS, Shad Ali G (2011) Plant serine/arginine-rich proteins: roles in precursor messenger RNA splicing, plant development, and stress responses. Wiley Interdiscip Rev RNA 2:875–889

    PubMed  Article  CAS  Google Scholar 

  • Saidi Y, Finka A, Muriset M, Bromberg Z, Weiss YG, Maathuis FJ, Goloubinoff P (2009) The heat shock response in moss plants is regulated by specific calcium-permeable channels in the plasma membrane. Plant Cell 21:2829–2843

    PubMed  Article  CAS  Google Scholar 

  • Sakuma Y, Maruyama K, Qin F, Osakabe Y, Shinozaki K, Yamaguchi-Shinozaki K (2006) Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stress-responsive gene expression. Proc Natl Acad Sci USA 103:18822–18827

    PubMed  Article  CAS  Google Scholar 

  • Sarkar NK, Kim YK, Grover A (2009) Rice sHsp genes: genomic organization and expression profiling under stress and development. BMC Genomics 10:393

    PubMed  Article  Google Scholar 

  • Sarkar NK, Kundnani P, Grover A (2013a) Functional analysis of Hsp70 superfamily proteins of rice (Oryza sativa). Cell Stress Chaperones 18:427–437

    Google Scholar 

  • Sarkar NK, Thapar U, Kundnani P, Panwar P, Grover A (2013b) Functional relevance of J-protein family of rice (Oryza sativa). Cell Stress Chaperones 18:321–331

    PubMed  Article  CAS  Google Scholar 

  • Sato Y, Namiki N, Takehisa H, Kamatsuki K, Minami H, Ikawa H, Ohyanagi H, Sugimoto K, Itoh J, Antonio BA, Nagamura Y (2013) RiceFREND: a platform for retrieving coexpressed gene networks in rice. Nucleic Acids Res 41:D1214–D1221

    PubMed  Article  CAS  Google Scholar 

  • Schramm F, Larkindale J, Kiehlmann E, Ganguli A, Englich G, Vierling E, von Koskull-Doring P (2008) A cascade of transcription factor DREB2A and heat stress transcription factor HsfA3 regulates the heat stress response of Arabidopsis. Plant J 53:264–274

    PubMed  Article  CAS  Google Scholar 

  • Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504

    PubMed  Article  CAS  Google Scholar 

  • Shi W, Muthurajan R, Rahman H, Selvam J, Peng S, Zou Y, Jagadish KS (2013) Source-sink dynamics and proteomic reprogramming under elevated night temperature and their impact on rice yield and grain quality. New Phytol 197:825–837

    PubMed  Article  CAS  Google Scholar 

  • Shim D, Hwang JU, Lee J, Lee S, Choi Y, An G, Martinoia E, Lee Y (2009) Orthologs of the class A4 heat shock transcription factor HsfA4a confer cadmium tolerance in wheat and rice. Plant Cell 21:4031–4043

    PubMed  Article  CAS  Google Scholar 

  • Singh A, Singh U, Mittal D, Grover A (2010) Genome-wide analysis of rice ClpB/HSP100, ClpC and ClpD genes. BMC Genomics 11:95

    PubMed  Article  Google Scholar 

  • Smyth GK (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3:Article3

    Google Scholar 

  • Sugio A, Dreos R, Aparicio F, Maule AJ (2009) The cytosolic protein response as a subcomponent of the wider heat shock response in Arabidopsis. Plant Cell 21:642–654

    PubMed  Article  CAS  Google Scholar 

  • Suri SS, Dhindsa RS (2008) A heat-activated MAP kinase (HAMK) as a mediator of heat shock response in tobacco cells. Plant, Cell Environ 31:218–226

    Article  CAS  Google Scholar 

  • Suzuki N, Bajad S, Shuman J, Shulaev V, Mittler R (2008) The transcriptional co-activator MBF1c is a key regulator of thermotolerance in Arabidopsis thaliana. J Biol Chem 283:9269–9275

    PubMed  Article  CAS  Google Scholar 

  • Suzuki N, Sejima H, Tam R, Schlauch K, Mittler R (2011) Identification of the MBF1 heat-response regulon of Arabidopsis thaliana. Plant J 66:844–851

    PubMed  Article  CAS  Google Scholar 

  • Takahashi H, Kawakatsu T, Wakasa Y, Hayashi S, Takaiwa F (2012) A rice transmembrane bZIP transcription factor, OsbZIP39, regulates the endoplasmic reticulum stress response. Plant Cell Physiol 53:144–153

    PubMed  Article  CAS  Google Scholar 

  • Ueda K, Matsuura H, Yamaguchi M, Demura T, Kato K (2012) Genome-wide analyses of changes in translation state caused by elevated temperature in Oryza sativa. Plant Cell Physiol 53:1481–1491

    PubMed  Article  CAS  Google Scholar 

  • Volkov RA, Panchuk II, Mullineaux PM, Schoffl F (2006) Heat stress-induced H2O2 is required for effective expression of heat shock genes in Arabidopsis. Plant Mol Biol 61:733–746

    PubMed  Article  CAS  Google Scholar 

  • Wang D, Pan Y, Zhao X, Zhu L, Fu B, Li Z (2011) Genome-wide temporal-spatial gene expression profiling of drought responsiveness in rice. BMC Genomics 12:149

    PubMed  Article  Google Scholar 

  • Wu WS, Li WH (2008) Identifying gene regulatory modules of heat shock response in yeast. BMC Genomics 9:439

    PubMed  Article  CAS  Google Scholar 

  • Wu X, Shiroto Y, Kishitani S, Ito Y, Toriyama K (2009) Enhanced heat and drought tolerance in transgenic rice seedlings overexpressing OsWRKY11 under the control of HSP101 promoter. Plant Cell Rep 28:21–30

    PubMed  Article  CAS  Google Scholar 

  • Yamakawa H, Hakata M (2010) Atlas of rice grain filling-related metabolism under high temperature: joint analysis of metabolome and transcriptome demonstrated inhibition of starch accumulation and induction of amino acid accumulation. Plant Cell Physiol 51:795–809

    PubMed  Article  CAS  Google Scholar 

  • Yan JJ, Zhang YB, Ding Y (2012) Binding mechanism between Hsp90 and Sgt1 explored by homology modeling and molecular dynamics simulations in rice. J Mol Model 18:4665–4673

    PubMed  Article  CAS  Google Scholar 

  • Yang YH, Dudoit S, Luu P, Lin DM, Peng V, Ngai J, Speed TP (2002) Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res 30:e15

    PubMed  Article  Google Scholar 

  • Yin Y, Li S, Liao W, Lu Q, Wen X, Lu C (2010) Photosystem II photochemistry, photoinhibition, and the xanthophyll cycle in heat-stressed rice leaves. J Plant Physiol 167:959–966

    PubMed  Article  CAS  Google Scholar 

  • Yokotani N, Ichikawa T, Kondou Y, Matsui M, Hirochika H, Iwabuchi M, Oda K (2008) Expression of rice heat stress transcription factor OsHsfA2e enhances tolerance to environmental stresses in transgenic Arabidopsis. Planta 227:957–967

    PubMed  Article  CAS  Google Scholar 

  • You J, Zong W, Li X, Ning J, Hu H, Xiao J, Xiong L (2013) The SNAC1-targeted gene OsSRO1c modulates stomatal closure and oxidative stress tolerance by regulating hydrogen peroxide in rice. J Exp Bot 64:569–583

    PubMed  Article  CAS  Google Scholar 

  • Yun KY, Park MR, Mohanty B, Herath V, Xu F, Mauleon R, Wijaya E, Bajic VB, Bruskiewich R, de Los Reyes BG (2010) Transcriptional regulatory network triggered by oxidative signals configures the early response mechanisms of japonica rice to chilling stress. BMC Plant Biol 10:16

    PubMed  Article  Google Scholar 

  • Zeeberg BR, Feng W, Wang G, Wang MD, Fojo AT, Sunshine M, Narasimhan S, Kane DW, Reinhold WC, Lababidi S, Bussey KJ, Riss J, Barrett JC, Weinstein JN (2003) GoMiner: a resource for biological interpretation of genomic and proteomic data. Genome Biol 4:R28

    PubMed  Article  Google Scholar 

  • Zhang X, Li J, Liu A, Zou J, Zhou X, Xiang J, Rerksiri W, Peng Y, Xiong X, Chen X (2012) Expression profile in rice panicle: insights into heat response mechanism at reproductive stage. PLoS ONE 7:e49652

    PubMed  Article  CAS  Google Scholar 

  • Zou J, Liu C, Chen X (2011) Proteomics of rice in response to heat stress and advances in genetic engineering for heat tolerance in rice. Plant Cell Rep 30:2155–2165

    PubMed  Article  CAS  Google Scholar 

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Acknowledgments

This work was supported by funding from Centre for Plant Molecular Biology and Centre for Advanced Research and Innovation on Plant Stress and Developmental Biology, Department of Biotechnology, Government of India. AG is thankful to Department of Science and Technology, Government of India for the J.C. Bose fellowship award. We thank Prof. Sang Bong Choi, Myongji University, South Korea for helpful discussions. We thank John Wyrick, Washington State University, USA for help with Osiris database.

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  1. Department of Plant Molecular Biology, University of Delhi South Campus, New Delhi, 110021, India

    Neelam K. Sarkar & Anil Grover

  2. Genomics and Genetics Institute, GreenGene Biotech, Myongji University, 38-2 Namdong, Yongin, Kyonggido, Korea

    Yeon-Ki Kim

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  1. Neelam K. Sarkar
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Correspondence to Anil Grover.

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Supplementary material 1 (XLSX 12 kb)

Supplementary material 2 (XLSX 690 kb)

Supplementary material 3 (XLSX 24 kb)

11103_2013_123_MOESM4_ESM.pptx

Supplementary Fig. 1. Functional categories of genes. Pie diagrams represent the various functional categories by COG (http://www.ncbi.nlm.nih.gov/COG/old/) analysis of up-regulated and down-regulated genes in three stress treatments. (PPTX 803 kb)

11103_2013_123_MOESM5_ESM.pptx

Supplementary Fig. 2. Hierarchical clustering of genes during heat stress and recovery. Microarray analysis of leaf tissue was performed as mentioned in the text. Twofold up- or down-regulated genes in at least one of the treatments in microarray were analyzed for hierarchical clustering. A-D are the clusters described in the text. (PPTX 56 kb)

11103_2013_123_MOESM6_ESM.pptx

Supplementary Fig. 3. Semi-quantitative RT-PCR analysis of selected genes. RT-PCR was performed in duplicate and the results of one set are presented. Details of primers and the number of cycles are listed in Supplementary Table 1 (PPTX 6670 kb)

Supplementary Fig. 4. Interactome analysis of Os03g12820 and Os03g60080 genes in STRING database. (PPTX 737 kb)

Supplementary Fig. 5. Expression analysis of coexpression network genes in genevestigator. (PNG 63 kb)

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Sarkar, N.K., Kim, YK. & Grover, A. Coexpression network analysis associated with call of rice seedlings for encountering heat stress. Plant Mol Biol 84, 125–143 (2014). https://doi.org/10.1007/s11103-013-0123-3

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  • DOI: https://doi.org/10.1007/s11103-013-0123-3

Keywords

  • Coexpression network
  • Early events
  • Heat stress
  • Microarray
  • Recovery
  • Rice