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Comparative transcriptome analysis reveals differential transcription in heat-susceptible and heat-tolerant pepper (Capsicum annum L.) cultivars under heat stress

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Abstract

Heat stress is an important agricultural problem around the world. In pepper (Capsicum annum L.), heat stress seriously affects pollination and yield. However, to date, the molecular basis of heat stress has not been extensively studied. Using the HiSeq™ 2000 sequencing platform, the seedling transcriptome of heat-susceptible C.annuum ‘S590’(CaS) and heat-tolerant ‘R597’ (CaR) under the heat stress was examined. Over five million clean reads were generated from each library, each corresponding to a coverage of >250,000 nt. About 73% of the reads were mapped to the pepper genome, and 3,799 and 4,010 differentially expressed genes (DEGs) were identified in ‘R597’ (CaR) and ‘S590’(CaS), respectively. Gene ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) analyses determined that the identified DEGs were involved in heat shock protein, heat shock transcription factors, hormone, as well as calcium and kinase signaling. Further validation identified 35 genes that were involved in stress response, and that most of the heat shock proteins were upregulated in two genotypes, and highly expressed in susceptible S590 than in tolerant cultivar R597; the transcription factors and hormone signaling genes showed higher levels of expression in the heat-tolerant cultivar R597 than that observed in the heat-susceptible S590. These findings facilitate in better understanding of the molecular mechanism underlying heat stress in different pepper genotypes.

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References

  • Bindea G, Mlecnik B, Hackl H, Charoentong P, Tosolini M, Kirilovsky A, Fridman WH, Pages F, Trajanoski Z, Galon J (2009) ClueGO: a Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks. Bioinformatics 25:1091–1093

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Campos PS, nia Quartin V, chicho Ramalho J, Nunes MA (2003) Electrolyte leakage and lipid degradation account for cold sensitivity in leaves of Coffea sp. plants. J Plant Physiol 160:283–292

    Article  CAS  PubMed  Google Scholar 

  • Chauhan H, Khurana N, Tyagi AK, Khurana JP, Khurana P (2011) Identification and characterization of high temperature stress responsive genes in bread wheat (Triticum aestivum L.) and their regulation at various stages of development. Plant Mol Biol 75:35–51

    Article  CAS  PubMed  Google Scholar 

  • Chen Z, Cuin TA, Zhou M, Twomey A, Naidu BP, Shabala S (2007) Compatible solute accumulation and stress-mitigating effects in barley genotypes contrasting in their salt tolerance. J Exp Bot 58:4245–4255

    Article  CAS  PubMed  Google Scholar 

  • Conesa A, Gotz S (2008) Blast2GO: A comprehensive suite for functional analysis in plant genomics. Int J Plant Genomics 2008:619832

    Article  PubMed Central  PubMed  Google Scholar 

  • Erickson AN, Markhart AH (2002) Flower developmental stage and organ sensitivity of bell pepper (Capsicum annuum L.) to elevated temperature. Plant Cell Environ 25:123–130

    Article  Google Scholar 

  • Frank G, Pressman E, Ophir R, Althan L, Shaked R, Freedman M, Shen S, Firon N (2009) Transcriptional profiling of maturing tomato (Solanum lycopersicum L.) microspores reveals the involvement of heat shock proteins, ROS scavengers, hormones, and sugars in the heat stress response. J Exp Bot 60:3891–3908

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fukao T, Xu K, Ronald PC, Bailey-Serres J (2006) A variable cluster of ethylene response factor-like genes regulates metabolic and developmental acclimation responses to submergence in rice. Plant Cell 18:2021–2034

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gajanayake B, Trader BW, Reddy KR, Harkess RL (2011) Screening Ornamental Pepper Cultivars for Temperature Tolerance Using Pollen and Physiological Parameters. Hort Sci 46:878–884

    Google Scholar 

  • Gilroy S, Suzuki N, Miller G, Choi W-G, Toyota M, Devireddy AR, Mittler R (2014) A tidal wave of signals: calcium and ROS at the forefront of rapid systemic signaling. Trends Plant Sci 19:623–630

    Article  CAS  PubMed  Google Scholar 

  • Gongora-Castillo E, Ibarra-Laclette E, Trejo-Saavedra DL, Rivera-Bustamante RF (2012) Transcriptome analysis of symptomatic and recovered leaves of geminivirus-infected pepper (Capsicum annuum). Virol J 9:295

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • González-Zamora A, Sierra-Campos E, Luna-Ortega JG, Pérez-Morales R, Ortiz JCR, García-Hernández JL (2013) Characterization of different (Capsicum) varieties by evaluation of their capsaicinoids content by high performance liquid chromatography, determination of pungency and effect of high temperature. Molecules 18:13471–13486

    Article  PubMed  Google Scholar 

  • Guo M, Yin YX, Ji JJ, Ma BP, Lu MH, Gong ZH (2014) Cloning and expression analysis of heat-shock transcription factor gene CaHsfA2 from pepper (Capsicum annuum L.). Genet Mol Res 13:1865–1875

    Article  CAS  PubMed  Google Scholar 

  • Hasanuzzaman M, Nahar K, Alam MM, Roychowdhury R, Fujita M (2013) Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. Int J Mol Sci 14:9643–9684

    Article  PubMed Central  PubMed  Google Scholar 

  • Hays DB, Do JH, Mason RE, Morgan G, Finlayson SA (2007) Heat stress induced ethylene production in developing wheat grains induces kernel abortion and increased maturation in a susceptible cultivar. Plant Sci 172:1113–1123

    Article  CAS  Google Scholar 

  • Hedhly A, Hormaza JI, Herrero M (2009) Global warming and sexual plant reproduction. Trends Plant Sci 14:30–36

    Article  CAS  PubMed  Google Scholar 

  • Jung K-H, Ko H-J, Nguyen M, 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 

  • Kafizadeh N, Carapetian J, Kalantari KM (2008) Effects of heat stress on pollen viability and pollen tube growth in pepper. Res J Biol Sci 3:1159–1162

    Google Scholar 

  • Kim S, Park M, Yeom SI, Kim YM, Lee JM, Lee HA, Seo E, Choi J, Cheong K, Kim KT, Jung K, Lee GW, Oh SK, Bae C, Kim SB, Lee HY, Kim SY, Kim MS, Kang BC, Jo YD, et al. (2014) Genome sequence of the hot pepper provides insights into the evolution of pungency in Capsicum species. Nat Genet 46:270–278

    Article  CAS  PubMed  Google Scholar 

  • Kotak S, Larkindale J, Lee U, von Koskull-Doring P, Vierling E, Scharf KD (2007) Complexity of the heat stress response in plants. Curr Opin Plant Biol 10:310–316

    Article  CAS  PubMed  Google Scholar 

  • Larkindale J, Hall JD, Knight MR, Vierling E (2005) Heat Stress Phenotypes of Arabidopsis Mutants Implicate Multiple Signaling Pathways in the Acquisition of Thermotolerance. Plant Physiol 138:882–897

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Larkindale J, Huang B (2004) Thermotolerance and antioxidant systems in Agrostis stolonifera: involvement of salicylic acid, abscisic acid, calcium, hydrogen peroxide, and ethylene. J Plant Physiol 161:405–413

    Article  CAS  PubMed  Google Scholar 

  • Lee S, Choi D (2013) Comparative transcriptome analysis of pepper (Capsicum annuum) revealed common regulons in multiple stress conditions and hormone treatments. Plant Cell Rep 32:1351–1359

    Article  CAS  PubMed  Google Scholar 

  • Lee S, Yun SC (2006) The ozone stress transcriptome of pepper (Capsicum annuum L.). Mol Cells 21:197–205

    CAS  PubMed  Google Scholar 

  • Li W, Cheng J, Wu Z, Qin C, Tan S, Tang X, Cui J, Zhang L, Hu K (2015) An InDel-based linkage map of hot pepper (Capsicum annuum). Mol Breeding 35:1–10

    Article  Google Scholar 

  • Liu C, Ma N, Wang PY, Fu N, Shen HL (2013) Transcriptome sequencing and de novo analysis of a cytoplasmic male sterile line and its near-isogenic restorer line in chili pepper (Capsicum annuum L.). PLoS One 8:e65209

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Liu F, Wang W, Sun X, Liang Z, Wang F (2014) RNA-Seq revealed complex response to heat stress on transcriptomic level in Saccharina japonica (Laminariales, Phaeophyta). J Appl Phycol 26:1585–1596

    Article  CAS  Google Scholar 

  • Liu GT, Wang JF, Cramer G, Dai ZW, Duan W, Xu HG, Wu BH, Fan PG, Wang LJ, Li SH (2012) Transcriptomic analysis of grape (Vitis vinifera L.) leaves during and after recovery from heat stress. BMC Plant Biol 12:174

    Article  PubMed Central  PubMed  Google Scholar 

  • Liu H-T, Liu Y-Y, Pan Q-H, Yang H-R, Zhan J-C, Huang W-D (2006) Novel interrelationship between salicylic acid, abscisic acid, and PIP2-specific phospholipase C in heat acclimation-induced thermotolerance in pea leaves. J Exp Bot 57:3337–3347

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Liu S, Chen C, Chen G, Cao B, Chen Q, Lei J (2012) RNA-sequencing tag profiling of the placenta and pericarp of pungent pepper provides robust candidates contributing to capsaicinoid biosynthesis. Plant Cell Tiss Organ Cult 110:111–121

    Article  CAS  Google Scholar 

  • Liu S, Li W, Wu Y, Chen C, Lei J (2013) De novo transcriptome assembly in chili pepper (Capsicum frutescens) to identify genes involved in the biosynthesis of capsaicinoids. PLoS One 8:e48156

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mangelsen E, Kilian J, Harter K, Jansson C, Wanke D, Sundberg E (2011) Transcriptome analysis of high-temperature stress in developing barley caryopses: early stress responses and effects on storage compound biosynthesis. Mol Plant 4:97–115

    Article  CAS  PubMed  Google Scholar 

  • Martinez-Lopez LA, Ochoa-Alejo N, Martinez O (2014) Dynamics of the chili pepper transcriptome during fruit development. BMC Genomics 15:143

    Article  PubMed Central  PubMed  Google Scholar 

  • Mateos RM, Jimenez A, Roman P, Romojaro F, Bacarizo S, Leterrier M, Gomez M, Sevilla F, Del Rio LA, Corpas FJ, Palma JM (2013) Antioxidant Systems from Pepper (Capsicum annuum L.): Involvement in the Response to Temperature Changes in Ripe Fruits. Int J Mol Sci 14:9556–9580

    Article  PubMed Central  PubMed  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 Biochem 47:785–795

    Article  CAS  PubMed  Google Scholar 

  • Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNASeq. Nat Methods 5:621–628

    Article  CAS  PubMed  Google Scholar 

  • Mosquna A, Peterson FC, Park S-Y, Lozano-Juste J, Volkman BF, Cutler SR (2011) Potent and selective activation of abscisic acid receptors in vivo by mutational stabilization of their agonistbound conformation. Proc Natl Acad Sci USA 108:20838–20843

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Oshino T, Abiko M, Saito R, Ichiishi E, Endo M, Kawagishi-Kobayashi M, Higashitani A (2007) Premature progression of anther early developmental programs accompanied by comprehensive alterations in transcription during high-temperature injury in barley plants. Mol Genet Genomics 278:31–42

    Article  CAS  PubMed  Google Scholar 

  • Pitzschke A (2015) Modes of MAPK substrate recognition and control. Trends Plant Sci 20:49–55

    Article  CAS  PubMed  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

    Article  PubMed Central  PubMed  Google Scholar 

  • Qu AL, Ding YF, Jiang Q, Zhu C (2013) Molecular mechanisms of the plant heat stress response. Biochem Biophys Res Commun 432:203–207

    Article  CAS  PubMed  Google Scholar 

  • Queitsch C, Hong S-W, Vierling E, Lindquist S (2000) Heat Shock Protein 101 Plays a Crucial Role in Thermotolerance in Arabidopsis. Plant Cell 12:479–492

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Reddy AS, Ali GS, Celesnik H, Day IS (2011) Coping with stresses: roles of calcium- and calcium/calmodulin-regulated gene expression. Plant Cell 23:2010–2032

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rizhsky L, Liang H, Shuman J, Shulaev V, Davletova S, Mittler R (2004) When Defense Pathways Collide. The Response of Arabidopsis to a Combination of Drought and Heat Stress. Plant Physiol 134:1683–1696

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sangwan V, Örvar BL, Beyerly J, Hirt H, Dhindsa RS (2002) Opposite changes in membrane fluidity mimic cold and heat stress activation of distinct plant MAP kinase pathways. Plant J 31:629–638

    Article  CAS  PubMed  Google Scholar 

  • Sinha AK, Jaggi M, Raghuram B, Tuteja N (2011) Mitogen-activated protein kinase signaling in plants under abiotic stress. Plant Signal Behav 6:196–203

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Su P-H, Li H-m (2008) Arabidopsis Stromal 70-kD Heat Shock Proteins Are Essential for Plant Development and Important for Thermotolerance of Germinating Seeds. Plant Physiol 146:1231–1241

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Swindell WR, Huebner M, Weber AP (2007) Transcriptional profiling of Arabidopsis heat shock proteins and transcription factors reveals extensive overlap between heat and non-heat stress response pathways. BMC Genomics 8:125

    Article  PubMed Central  PubMed  Google Scholar 

  • Timperio AM, Egidi MG, Zolla L (2008) Proteomics applied on plant abiotic stresses: Role of heat shock proteins (HSP). J Proteomics 71:391–411

    Article  CAS  PubMed  Google Scholar 

  • Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG (2012) Primer3—new capabilities and interfaces. Nucleic Acids Res 40:e115

  • Wahid A, Farooq M, Hussain I, Rasheed R, Galani S (2012) Responses and Management of Heat Stress in Plants, In Ahmad P, Prasad MNV eds, Environmental Adaptations and Stress Tolerance of Plants in the Era of Climate Change, Ed, Vol Springer New York pp 135–157

    Chapter  Google Scholar 

  • Wahid A, Gelani S, Ashraf M, Foolad MR (2007) Heat tolerance in plants: An overview. Environ Exp Bot 61:199–223

    Article  Google Scholar 

  • Xu H, Gao Y, Wang J (2012) Transcriptomic analysis of rice (Oryza sativa) developing embryos using the RNA-Seq technique. PLoS One 7:e30646

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Xu X, Lei J, Li Y, Luo S, Wang H, Xu X, Li T (2013) Comprehensive evaluation for high temperature and humidity resistance in pepper (Capsicum annuum L.) budding. J Chin Trop Crops 9:1747–1751

    Google Scholar 

  • Xu X, Lei J, Zhang C, Li y, Wang H, Li T, Xu X (2014) Methylationsensitive amplified polymorphism analysis of DNA methylation in hot pepper under high temperature and air humidity stress. J Nucl Agric Biol 28:1175–1180

    CAS  Google Scholar 

  • Yamada K, Fukao Y, Hayashi M, Fukazawa M, Suzuki I, Nishimura M (2007) Cytosolic HSP90 Regulates the Heat Shock Response That Is Responsible for Heat Acclimation in Arabidopsis thaliana. J Biol Chem 282:37794–37804

    Article  CAS  PubMed  Google Scholar 

  • Yang KA, Lim CJ, Hong JK, Park CY, Cheong YH, Chung WS, Lee KO, Lee SY, Cho MJ, Lim CO (2006) Identification of cell wall genes modified by a permissive high temperature in Chinese cabbage. Plant Sci 171:175–182

    Article  CAS  Google Scholar 

  • Zhang G, Chen M, Li L, Xu Z, Chen X, Guo J, Ma Y (2009) Overexpression of the soybean GmERF3 gene, an AP2/ERF type transcription factor for increased tolerances to salt, drought, and diseases in transgenic tobacco. J Exp Bot 60:3781–3796

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhang W, Zhou RG, Gao YJ, Zheng SZ, Xu P, Zhang SQ, Sun DY (2009) Molecular and genetic evidence for the key role of AtCaM3 in heat-shock signal transduction in Arabidopsis. Plant Physiol 149:1773–1784

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Vegetable Research Institute, Guangdong Academy of Agricultural Sciences, Guangzhou, 510640, China

    Tao Li, Xiaowan Xu, Ying Li, Hengming Wang, Zhiliang Li & Zhenxing Li

  2. Guangdong Key Laboratory for New Technology Research of Vegetables, Guangzhou, 510640, China

    Tao Li & Xiaowan Xu

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  1. Tao Li
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  2. Xiaowan Xu
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  3. Ying Li
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Correspondence to Xiaowan Xu.

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Li, T., Xu, X., Li, Y. et al. Comparative transcriptome analysis reveals differential transcription in heat-susceptible and heat-tolerant pepper (Capsicum annum L.) cultivars under heat stress. J. Plant Biol. 58, 411–424 (2015). https://doi.org/10.1007/s12374-015-0423-z

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  • DOI: https://doi.org/10.1007/s12374-015-0423-z

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