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Application of MapMan and RiceNet drives systematic analyses of the early heat stress transcriptome in rice seedlings

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Abstract

High-throughput transcriptome analyses such as oligonucleotide microarray technology are powerful tools for identifying an entire set of transcripts under given experimental conditions. However, it is not a simple process to interpret which information is important from those large gene sets. Using oligonucleotide arrays, more than 3000 rice microarray data have been produced; all are available for public users from the NCBI gene expression omnibus (GEO; http://www.ncbi.nlm.nih.gov/geo/). In this study, we employed MapMan and RiceNet tools to drive systematic analyses of the early heat stress transcriptome in rice seedlings. We generated transcriptome data to identify 589 genes that respond to early during heat stress, and uploaded the list to various overviews installed in the MapMan tool. In the cellular-response overview, this investigation revealed that the heat stress MapMan term is the most dominant, fitting well to the purpose of transcriptome analysis for examining the early heat stress response. When we applied the regulation overview, we learned that genes associated with transcription factors, protein modification, and calcium regulation are more significantly coupled with early heat stress in rice seedlings. This suggests that essential components, comprising signaling pathways, are mediated by such stress. We also used RiceNet to determine the functional gene network mediated by this stress. This network development was based on genes with enriched MapMan terms, i.e., heat stress, transcription factors, protein modification, and calcium regulation. We expect that applications of MapMan and RiceNet to genome-wide transcriptome data will guide users to identify key elements for further analyses.

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References

  • Affymetrix (2001) Affymetrix Microarray Suite User Guide, Ed, Vol version 5 edition. Affymetrix

  • AL-Quraan NA, Locy RD, Singh NK (2012) Heat and cold stresses phenotypes of Arabidopsis thaliana calmodulin mutants: regulation of gamma-aminobutyric acid shunt pathway under temperature stress. Int J Plant Biol 3:10.4081/pb.2012.e4082

  • Chauhan H, Khurana N, Agarwal P, Khurana P (2011) Heat shock factors in rice (Oryza sativa L.): genome-wide expression analysis during reproductive development and abiotic stress. Mol Genet Genomics 286:171–187

    Article  PubMed  CAS  Google Scholar 

  • Chen YJ, Inouye M (2008) The intramolecular chaperone-mediated protein folding. Curr Opin Struc Biol 18:765–770

    Article  CAS  Google Scholar 

  • Ciftci-Yilmaz S, Morsy MR, Song LH, Coutu A, Krizek BA, Lewis MW, Warren D, Cushman J, Connolly EL, Mittler R (2007) The EAR-motif of the Cys2/His2-type zinc finger protein Zat7 plays a key role in the defense response of Arabidopsis to salinity stress. J Biol Chem 282:9260–9268

    Article  PubMed  CAS  Google Scholar 

  • Coghlin C, Carpenter B, Dundas SR, Lawrie LC, Telfer C, Murray GI (2006) Characterization and over-expression of chaperonin tcomplex proteins in colorectal cancer. J Pathol 210:351–357

    Article  PubMed  CAS  Google Scholar 

  • Coppolino MG, Dedhar S (1998) Calreticulin. Int J Biochem Cell Biol 30:553–558

    Article  PubMed  CAS  Google Scholar 

  • Cuellar J, Martin-Benito J, Scheres SH, Sousa R, Moro F, Lopez-Vinas E, Gomez-Puertas P, Muga A, Carrascosa JL, Valpuesta JM (2008) The structure of CCT-Hsc70 NBD suggests a mechanism for Hsp70 delivery of substrates to the chaperonin. Nat Struct Mol Biol 15:858–864

    Article  PubMed  CAS  Google Scholar 

  • de la Fuente van Bentem S, Vossen JH, de Vries KJ, van Wees S, Tameling WI, Dekker HL, de Koster CG, Haring MA, Takken FL, Cornelissen BJ (2005) Heat shock protein 90 and its cochaperone protein phosphatase 5 interact with distinct regions of the tomato I-2 disease resistance protein. Plant J 43:284–298

    Article  PubMed  Google Scholar 

  • Ding X, Richter T, Chen M, Fujii H, Seo YS, Xie M, Zheng X, Kanrar S, Stevenson RA, Dardick C, Li Y, Jiang H, Zhang Y, Yu F, Bartley LE, Chern M, Bart R, Chen X, Zhu L, Farmerie WG, Gribskov M, Zhu JK, Fromm ME, Ronald PC, Song WY (2009) A rice kinase-protein interaction map. Plant Physiol 149:1478–1492

    Article  PubMed  CAS  Google Scholar 

  • Fenton WA, Horwich AL (2003) Chaperonin-mediated protein folding: fate of substrate polypeptide. Quart Rev Biophys 36:229–256

    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

    Article  PubMed  CAS  Google Scholar 

  • Fujita Y, Yoshida T, Yamaguchi-Shinozaki K (2012) Pivotal role of the AREB/ABF-SnRK2 pathway in ABRE-mediated transcription in response to osmotic stress in plants. Physiol Plant doi: 10.1111/j.1399-3054.2012.01635.x.

  • Genevaux P, Schwager F, Georgopoulos C, Kelley WL (2002) Scanning mutagenesis identifies amino acid residues essential for the in vivo activity of the Escherichia coli DnaJ (Hsp40) Jdomain. Genetics 162:1045–1053

    PubMed  CAS  Google Scholar 

  • Gu H, Zhu P, Jiao Y, Meng Y, Chen M (2011) PRIN: a predicted rice interactome network. BMC Bioinformatics 12:161

    Article  PubMed  Google Scholar 

  • Guimaraes AJ, Nakayasu ES, Sobreira TJ, Cordero RJ, Nimrichter L, Almeida IC, Nosanchuk JD (2011) Histoplasma capsulatum heat-shock 60 orchestrates the adaptation of the fungus to temperature stress. PloS One 6:e14660

    Article  PubMed  CAS  Google Scholar 

  • Guo L, Wang ZY, Lin H, Cui WE, Chen J, Liu M, Chen ZL, Qu LJ, Gu H (2006) Expression and functional analysis of the rice plasma-membrane intrinsic protein gene family. Cell Res 16:277–286

    Article  PubMed  CAS  Google Scholar 

  • Homann U, Tester M (1997) Ca2+-independent and Ca2+/GTPbinding protein-controlled exocytosis in a plant cell. Proc Natl Acad Sci U S A 94:6565–6570

    Article  PubMed  CAS  Google Scholar 

  • Hossain MA, Lee Y, Cho JI, Ahn CH, Lee SK, Jeon JS, Kang H, Lee CH, An G, Park PB (2010) The bZIP transcription factor OsABF1 is an ABA responsive element binding factor that enhances abiotic stress signaling in rice. Plant Mol Biol 72:557–566

    Article  Google Scholar 

  • Hu WH, Hu GC, 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 

  • Josine TL, Ji J, Wang G, Guan CF (2011) Advances in genetic engineering for plants abiotic stress control. Afr J Biotechnol 10:5402–5413

    Google Scholar 

  • Jung K-H, An G, Ronald PC (2008a) Towards a better bowl of rice: assigning function to tens of thousands of rice genes. Nat Rev Genet 9:91–101

    PubMed  CAS  Google Scholar 

  • Jung KH, Dardick C, Bartley LE, Cao P, Phetsom J, Canlas P, Seo YS, Shultz M, Ouyang S, Yuan Q, Frank BC, Ly E, Zheng L, Jia Y, Hsia AP, An K, Chou HH, Rocke D, Lee GC, Schnable PS, An G, Buell CR, Ronald PC (2008b) Refinement of lightresponsive transcript lists using rice oligonucleotide arrays: evaluation of gene-redundancy. PLoS One 3:e3337

    Article  PubMed  Google Scholar 

  • Jung KH, Cao P, Seo YS, Dardick C, Ronald PC (2010) The Rice Kinase Phylogenomics Database: a guide for systematic analysis of the rice kinase super-family. Trends Plant Sci 15:595–599

    Article  PubMed  CAS  Google Scholar 

  • Jung KH, Jeon JS, An G (2011) Web Tools for Rice Transcriptome Analyses. J Plant Biol 54:65–80

    Article  CAS  Google Scholar 

  • Jung KH, KO HJ, Kim SR, Ronald PC, An G (2012) Genome-wide Identification and Analysis of Early Heat Stress Responsive Genes in Rice. J Plant Biol Accepted

  • Kaye FJ, Modi S, Ivanovska I, Koonin EV, Thress K, Kubo A, Kornbluth S, Rose MD (2000) A family of ubiquitin-like proteins binds the ATPase domain of Hsp70-like Stch. FEBS Letters 467:348–355

    Article  PubMed  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 U S A 108:18548–18553

    Article  PubMed  CAS  Google Scholar 

  • Lee JR, Lee SS, Jang HH, Lee YM, Park JH, Park SC, Moon JC, Park SK, Kim SY, Lee SY, Chae HB, Jung YJ, Kim WY, Shin MR, Cheong GW, Kim MG, Kang KR, Lee KO, Yun DJ (2009a) Heat-shock dependent oligomeric status alters the function of a plant-specific thioredoxin-like protein, AtTDX. Proc Natl Acad Sci U S A 106:5978–5983

    Article  PubMed  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 (2009b) 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

    Article  PubMed  CAS  Google Scholar 

  • Li CG, Chen QJ, Gao XQ, Qi BS, Chen NZ, Xu SM, Chen J, Wang XC (2005a) AtHsfA2 modulates expression of stress responsive genes and enhances tolerance to heat and oxidative stress in Arabidopsis. Sci China Ser C 48:540–550

    Article  CAS  Google Scholar 

  • Li HY, Chang CS, Lu LS, Liu CA, Chan MT, Charng YY (2005b) Over-expression of Arabidopsis thaliana heat shock factor gene (AtHsfA1b) enhances chilling tolerance in transgenic tomato (vol 44, pg 129, 2003). Bot Bull Acad Sinica 46:91–91

    Google Scholar 

  • Liu AL, Zou J, Zhang XW, Zhou XY, Wang WF, Xiong XY, Chen LY, Chen XB (2010) Expression Profiles of Class A Rice Heat Shock Transcription Factor Genes Under Abiotic Stresses. J Plant Biol 53:142–149

    Article  Google Scholar 

  • Liu HT, Gao F, Cui SJ, Han JL, Sun DY, Zhou RG (2006) Primary evidence for involvement of IP3 in heat-shock signal transduction in Arabidopsis. Cell Res 16:394–400

    Article  PubMed  CAS  Google Scholar 

  • Ma JF, Mitani N, Nagao S, Konishi S, Tamai K, Iwashita T, Yano M (2004) Characterization of the silicon uptake system and molecular mapping of the silicon transporter gene in rice. Plant Physiol 136:3284–3289

    Article  PubMed  CAS  Google Scholar 

  • Miller G, Suzuki N, Rizhsky L, Hegie A, Koussevitzky S, Mittler R (2007) 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 stresses. Plant Physiol 144:1777–1785

    Article  PubMed  CAS  Google Scholar 

  • Mishra SK, Tripp J, Winkelhaus S, Tschiersch B, Theres K, Nover L, Scharf KD (2002) In the complex family of heat stress transcription factors, HSfA1 has a unique role as master regulator of thermotolerance in tomato. Genes Dev 16:1555–1567

    Article  PubMed  CAS  Google Scholar 

  • Mittal D, Chakrabarti S, Sarkar A, Singh A, Grover A (2009) Heat shock factor gene family in rice: Genomic organization and transcript expression profiling in response to high temperature, low temperature and oxidative stresses. Plant Physiol Bioch 47:785–795

    Article  CAS  Google Scholar 

  • Miyata Y, Yahara I (1992) The 90-kDa heat shock protein, HSP90, binds and protects casein kinase II from self-aggregation and enhances its kinase activity. J Biol Chem 267:7042–7047

    PubMed  CAS  Google Scholar 

  • Mogk A, Deuerling E, Vorderwulbecke S, Vierling E, Bukau B (2003) Small heat shock proteins, ClpB and the DnaK system form a functional triade in reversing protein aggregation. Mol Microbiol 50:585–595

    Article  PubMed  CAS  Google Scholar 

  • Murshid A, Chou SD, Prince T, Zhang Y, Bharti A, Calderwood SK (2010) Protein kinase A binds and activates heat shock factor 1. PloS One 5:e13830

    Article  PubMed  Google Scholar 

  • Nakashima K, Ito Y, Yamaguchi-Shinozaki K (2009) Transcriptional Regulatory Networks in Response to Abiotic Stresses in Arabidopsis and Grasses. Plant Physiol 149:88–95

    Article  PubMed  CAS  Google Scholar 

  • Nguyen TO, Capra JD, Sontheimer RD (1996) Calreticulin is transcriptionally upregulated by heat shock, calcium and heavy metals. Mol Immunol 33:379–386

    Article  PubMed  CAS  Google Scholar 

  • Nishizawa A, Yabuta Y, Yoshida E, Maruta T, Yoshimura K, Shigeoka S (2006) Arabidopsis heat shock transcription factor A2 as a key regulator in response to several types of environmental stress. Plant J 48:535–547

    Article  PubMed  CAS  Google Scholar 

  • Noel LD, Cagna G, Stuttmann J, Wirthmuller L, Betsuyaku S, Witte CP, Bhat R, Pochon N, Colby T, Parker JE (2007) Interaction between SGT1 and cytosolic/nuclear HSC70 chaperones regulates Arabidopsis immune responses. Plant Cell 19:4061–4076

    Article  PubMed  CAS  Google Scholar 

  • Ouyang S, Zhu W, Hamilton J, Lin H, Campbell M, Childs K, Thibaud-Nissen F, Malek RL, Lee Y, Zheng L, Orvis J, Haas B, Wortman J, Buell CR (2007) The TIGR Rice Genome Annotation Resource: improvements and new features. Nucleic Acids Res 35:D883–887

    Article  PubMed  CAS  Google Scholar 

  • Peltier JB, Ytterberg AJ, Sun Q, van Wijk KJ (2004) New functions of the thylakoid membrane proteome of Arabidopsis thaliana revealed by a simple, fast, and versatile fractionation strategy. J Biol Chem 279:49367–49383

    Article  PubMed  CAS  Google Scholar 

  • Ramsey AJ, Russell LC, Whitt SR, Chinkers M (2000) Overlapping sites of tetratricopeptide repeat protein binding and chaperone activity in heat shock protein 90. J Biol Chem 275:17857–17862

    Article  PubMed  CAS  Google Scholar 

  • Rees DC, Johnson E, Lewinson O (2009) ABC transporters: the power to change. Nat Rev Mol Cell Biol 10:218–227

    Article  PubMed  CAS  Google Scholar 

  • Rohila JS, Chen M, Chen S, Chen J, Cerny R, Dardick C, Canlas P, Xu X, Gribskov M, Kanrar S, Zhu JK, Ronald P, Fromm ME (2006) Protein-protein interactions of tandem affinity purification-tagged protein kinases in rice. Plant J 46:1–13

    Article  PubMed  CAS  Google Scholar 

  • Saidi Y, Finka A, Goloubinoff P (2011) Heat perception and signalling in plants: a tortuous path to thermotolerance. New Phytol 190:556–565

    Article  PubMed  CAS  Google Scholar 

  • Saitoh H, Cooke CA, Burgess WH, Earnshaw WC, Dasso M (1996) Direct and indirect association of the small GTPase ran with nuclear pore proteins and soluble transport factors: studies in Xenopus laevis egg extracts. Mol Biol Cell 7:1319–1334

    PubMed  CAS  Google Scholar 

  • Sato Y, Antonio BA, Namiki N, Takehisa H, Minami H, Kamatsuki K, Sugimoto K, Shimizu Y, Hirochika H, Nagamura Y (2011) RiceXPro: a platform for monitoring gene expression in japonica rice grown under natural field conditions. Nucleic Acids Res 39:D1141–1148

    Article  PubMed  Google Scholar 

  • Scheufler C, Brinker A, Bourenkov G, Pegoraro S, Moroder L, Bartunik H, Hartl FU, Moarefi I (2000) Structure of TPR domain-peptide complexes: critical elements in the assembly of the Hsp70-Hsp90 multichaperone machine. Cell 101:199–210

    Article  PubMed  CAS  Google Scholar 

  • Seo YS, Chern M, Bartley LE, Han M, Jung KH, Lee I, Walia H, Richter T, Xu X, Cao P, Bai W, Ramanan R, Amonpant F, Arul L, Canlas PE, Ruan R, Park CJ, Chen X, Hwang S, Jeon JS, Ronald PC (2011) Towards establishment of a rice stress response interactome. PLoS Genet 7:e1002020

    Article  PubMed  CAS  Google Scholar 

  • Shack S, Gorospe M, Fawcett TW, Hudgins WR, Holbrook NJ (1999) Activation of the cholesterol pathway and Ras maturation in response to stress. Oncogene 18:6021–6028

    Article  PubMed  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

    Article  PubMed  CAS  Google Scholar 

  • Smith DF, Sullivan WP, Marion TN, Zaitsu K, Madden B, McCormick DJ, Toft DO (1993) Identification of a 60-kilodalton stress-related protein, p60, which interacts with hsp90 and hsp70. Mol Cell Biol 13:869–876

    PubMed  CAS  Google Scholar 

  • Song HO, Lee W, An K, Lee HS, Cho JH, Park ZY, Ahnn J (2009) C. elegans STI-1, the homolog of Sti1/Hop, is involved in aging and stress response. J Mol Biol 390:604–617

    Article  PubMed  CAS  Google Scholar 

  • Szklarczyk D, Franceschini A, Kuhn M, Simonovic M, Roth A, Minguez P, Doerks T, Stark M, Muller J, Bork P, Jensen LJ, von Mering C (2011) The STRING database in 2011: functional interaction networks of proteins, globally integrated and scored. Nucleic Acids Res 39:D561–568

    Article  PubMed  Google Scholar 

  • Takabatake R, Ando Y, Seo S, Katou S, Tsuda S, Ohashi Y, Mitsuhara I (2007) MAP kinases function downstream of HSP90 and upstream of mitochondria in TMV resistance gene N-mediated hypersensitive cell death. Plant Cell Physiol 48:498–510

    Article  PubMed  CAS  Google Scholar 

  • Urbanczyk-Wochniak E, Usadel B, Thimm O, Nunes-Nesi A, Carrari F, Davy M, Blasing O, Kowalczyk M, Weicht D, Polinceusz A, Meyer S, Stitt M, Fernie AR (2006) Conversion of MapMan to allow the analysis of transcript data from Solanaceous species: effects of genetic and environmental alterations in energy metabolism in the leaf. Plant Mol Biol 60:773–792

    Article  PubMed  CAS  Google Scholar 

  • Usadel B, Nagel A, Thimm O, Redestig H, Blaesing OE, Palacios-Rojas N, Selbig J, Hannemann J, Piques MC, Steinhauser D, Scheible WR, Gibon Y, Morcuende R, Weicht D, Meyer S, Stitt M (2005) Extension of the visualization tool MapMan to allow statistical analysis of arrays, display of corresponding genes, and comparison with known responses. Plant Physiol 138:1195–1204

    Article  PubMed  CAS  Google Scholar 

  • Wang C, Zhang Q, Shou HX (2009) Identification and expression analysis of OsHsfs in rice. J Zhejiang Univ-Sc B 10:291–300

    Article  CAS  Google Scholar 

  • Xing T, Higgins VJ, Blumwald E (1996) Regulation of Plant Defense Response to Fungal Pathogens: Two Types of Protein Kinases in the Reversible Phosphorylation of the Host Plasma Membrane H+-ATPase. Plant Cell 8:555–564

    PubMed  CAS  Google Scholar 

  • Yang SD, Lee SC, Chang HC (1997) Heat stress induces tyrosine phosphorylation/activation of kinase FA/GSK-3 alpha (a human carcinoma dedifferentiation modulator) in A431 cells. J Cell Biochem 66:16–26

    Article  PubMed  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

    Article  PubMed  CAS  Google Scholar 

  • Zeng LR, Qu S, Bordeos A, Yang C, Baraoidan M, Yan H, Xie Q, Nahm BH, Leung H, Wang GL (2004) Spotted leaf11, a negative regulator of plant cell death and defense, encodes a Ubox/armadillo repeat protein endowed with E3 ubiquitin ligase activity. Plant Cell 16:2795–2808

    Article  PubMed  CAS  Google Scholar 

  • Zimmermann P, Laule O, Schmitz J, Hruz T, Bleuler S, Gruissem W (2008) Genevestigator transcriptome meta-analysis and biomarker search using rice and barley gene expression databases. Mol Plant 1:851–857

    Article  PubMed  CAS  Google Scholar 

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  1. Department of Plant Molecular Systems Biotechnology & Crop Biotech Institute, Kyung Hee University, Yongin, 446-701, Korea

    Ki-Hong Jung & Gynheung An

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Jung, KH., An, G. Application of MapMan and RiceNet drives systematic analyses of the early heat stress transcriptome in rice seedlings. J. Plant Biol. 55, 436–449 (2012). https://doi.org/10.1007/s12374-012-0270-0

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