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Transcriptome and digital gene expression analysis of herbaceous peony (Paeonia lactiflora Pall.) to screen thermo-tolerant related differently expressed genes

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Abstract

Herbaceous peony (Paeonia lactiflora Pall.) is easily injured by heat stress (HS), which greatly restricts its application and promotion. In this study, the thermo-tolerance of three representative P. lactiflora cultivars had been firstly assessed. ‘Zifengyu’ was identified as the thermo-tolerant cultivar with relatively lower values and smaller variations in malondialdehyde, hydrogen peroxide (H2O2) and proline contents under HS. Subsequently, their transcriptomes were sequenced by RNA sequencing (RNA-seq) technology to construct a complete database. 81,599 unigenes were obtained, and 34,940 unigenes had been annotated. Moreover, through digital gene expression analysis of thermo-tolerant ‘Zifengyu’ and moderately thermo-tolerant ‘Hongyanzhenghui’, 161 heat stress response genes had been screened involving heat shock protein genes, plant hormone signal transduction related genes, fatty acid synthesis genes, reactive oxygen species-scavenging genes and secondary metabolites related genes. And the effectively and timely response of these genes to HS could endow thermo-tolerance to ‘Zifengyu’. Among these genes, 11 key thermo-tolerant related genes whose expressions were all significantly up-regulated in ‘Zifengyu’ and ‘Hongyanzhenghui’ during development and the former possessed higher levels could be regarded as the candidate genes, including isoprene synthase gene, 2 peroxidase genes, 3-oxoacyl-acyl carrier protein reductase gene (FabG), 3 transcription factor genes (bHLH, NAC and WRKY), HSP20 and 3 HSP70. These results could provide a better understanding of heat stress response in P. lactiflora, and pave for the breeding of thermo-tolerant cultivars.

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References

  • Al-Whaibi MH (2011) Plant heat-shock proteins: a mini review. J King Saud Univ Sci 23:139–150

    Article  Google Scholar 

  • Audic S, Claverie JM (1997) The significance of digital gene expression profiles. Genome Res 7:986–995

    CAS  PubMed  Google Scholar 

  • Barnabas B, Jaeger K, Feher A (2008) The effect of drought and heat stress on reproductive processes in cereals. Plant Cell Environ 31:11–38

    CAS  PubMed  Google Scholar 

  • 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  CAS  PubMed  Google Scholar 

  • Chauhan H, Khurana N, Nijhavan A, Khurana JP, Khurana P (2012) The wheat chloroplastic small heat shock protein (sHSP26) is involved in seed maturation and germination and imparts tolerance to heat stress. Plant Cell Environ 35:1912–1931

    Article  CAS  PubMed  Google Scholar 

  • Chen J, Huang P, McCarl BA, Shiva L (2014) Climate change, society, and agriculture: an economic and policy perspective. In: Alfen NKV (ed) Encyclopedia of agriculture and food systems. Academic Press, Oxford, pp 294–306

    Chapter  Google Scholar 

  • Chinnusamy V, Schumaker K, Zhu JK (2004) Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants. J Exp Bot 55:225–236

    Article  CAS  PubMed  Google Scholar 

  • Chung E, Kim KM, Lee JH (2013) Genome-wide analysis and molecular characterization of heat shock transcription fctor family in Glycine max. J Genet Genomics 40:127–135

    Article  CAS  PubMed  Google Scholar 

  • Cruz RM, Vieira MC, Silva CL (2006) Effect of heat and thermosonication treatments on peroxidase inactivation kinetics in watercress (Nasturtium officinale). J Food Eng 72:8–15

    Article  CAS  Google Scholar 

  • Cvikrova M, Gemperlova L, Dobra J, Martincova O, Prasil IT, Gubis J, Vankova R (2012) Effect of heat stress on polyamine metabolism in proline-over-producing tobacco plants. Plant Sci 182:49–58

    Article  CAS  PubMed  Google Scholar 

  • Gong SJ, Hao ZJ, Meng JS, Liu D, Wei MR, Tao J (2015) Digital gene expression analysis to screen disease resistance-relevant genes from leaves of herbaceous peony (Paeonia lactiflora Pall.) infected by Botrytis cinerea. PLoS One. doi:10.1371/journal.pone.0133305

    Google Scholar 

  • Guertin MJ, Lis JT (2010) Chromatin landscape dictates HSF binding to target DNA elements. PLoS Genet 6:e1001114. doi:10.1371/journal.pgen.1001114

    Article  PubMed  PubMed Central  Google Scholar 

  • Guo J, Wu J, Ji Q, Wang C, Luo L, Yuan Y, Wang Y, Wang J (2008) Genome-wide analysis of heat shock transcription factor families in rice and Arabidopsis. J Genet Genomics 35:105–118

    Article  CAS  PubMed  Google Scholar 

  • Han CX (2013) Preliminary research on physiological mechanism of thermostability in herbaceous peony. Masters dissertation, Yangzhou University, Yangzhou, pp 15–16 (in Chinese)

  • Havaux M (1998) Carotenoids as membrane stabilizers in chloroplasts. Trends Plant Sci 3:147–151

    Article  Google Scholar 

  • Horváth I, Glatza A, Nakamotob H, Mishkindd M, Munnike T, Saidif Y, Goloubinofff P, Harwoodg J, Vigha L (2012) Heat shock response in photosynthetic organisms: membrane and lipid connections. Prog Lipid Res 51:208–220

    Article  PubMed  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  PubMed  Google Scholar 

  • Janka E, Korner O, Rosenqvist E, Ottosen CO (2013) High temperature stress monitoring and detection using chlorophyll a fluorescence and infrared thermography in chrysanthemum (Dendranthema grandiflora). Plant Physiol Bioch 67:87–94

    Article  CAS  Google Scholar 

  • Joyce SM, Cassells AC, Jain SM (2003) Stress and aberrant phenotypes in in vitro culture. Plant Cell Tissue Org Cult 74:103–121

    Article  CAS  Google Scholar 

  • Kawanishi T, Shima K, Hayashi H, Douzono M, Hisamatsu T (2012) Effect of short-term rising temperature treatment performed around the end of the day on the growth, flowering, and cut-flower quality of spray-type chrysanthemums. Hortic Res 11:241–249

    Article  Google Scholar 

  • Kim OT, Cha SW, Park HW, Hyun DY, Bang KH, Jung SJ, Kim YC, Shin YS, Kim DH, Kim SW, Seong NS, Cha SW, Park HW (2007) Thermotolerant transgenic ginseng (Panax ginseng C.A. Meyer) by introducing isoprene synthase gene through Agrobacterium tumefaciens-mediated transformation. Korean J Med Crop Sci 15:95–99

    Google Scholar 

  • Kotak S, Larkindale J, Lee U, von Koskull-Doering 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 

  • Li R, Yu C, Li Y, Lam TW, Yiu SM, Kristiansen K, Wang J (2009) SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25:1966–1967

    Article  CAS  PubMed  Google Scholar 

  • Liang WD, Bi YT, Wang HY, Dong S, Li KS, Li JS (2013) Gene expression profiling of Clostridium botulinum under heat shock stress. BioMed Res Int 2013:760904

    PubMed  PubMed Central  Google Scholar 

  • Liu XZ, Huang BR (2000) Heat stress injury in relation to membrane lipid peroxidation in creeping bentgrass. Crop Sci 40:503–510 (in Chinese)

    Article  CAS  Google Scholar 

  • Lockhart DJ, Winzeler EA (2000) Genomics, gene expression and DNA arrays. Nature 405:827–836

    Article  CAS  PubMed  Google Scholar 

  • Lv C, Liu L (2008) Effects of high temperature on physiological and biochemical characteristics of Paeonia lactiflora. J Hunan Agric Univ (Nat Sci) 34:664–667 (in Chinese)

    Google Scholar 

  • Maestri E, Klueva N, Perrotta C, Gulli M, Nguyen HT, Marmiroli N (2002) Molecular genetics of heat tolerance and heat shock proteins in cereals. Plant Mol Biol 48:667–681

    Article  CAS  PubMed  Google Scholar 

  • Meehl GA, Tebaldi C (2004) More intense, more frequent, and longer lasting heat waves in the 21st century. Science 305:994–997

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Niu L, Fu X, Liu A (2010) Application of herbaceous peony in flower border. North Hortic 4:97–100 (in Chinese)

    Google Scholar 

  • Nover L, Bharti K, Doring P, Mishra SK, Ganguli A, Scharf KD (2001) Arabidopsis and the heat stress transcription factor world: how many heat stress transcription factors do we need? Cell Stress Chaperon 6:177–189

    Article  CAS  Google Scholar 

  • Ranney TG, Blazich FA, Warren SL (1995) Heat tolerance of selected species and populations of rhododendron. J Am Soc Hortic Sci 120:423–428

    Google Scholar 

  • Rivero RM, Ruiz JM, Garcia PC, Lopez-Lefebre LR, Sanchez E, Romero L (2001) Resistance to cold and heat stress: accumulation of phenolic compounds in tomato and watermelon plants. Plant Sci 160:315–321

    Article  CAS  PubMed  Google Scholar 

  • Santos TBD, Budzinski IG, Marur CJ, Petkowicz CL, Pereira LF, Vieira LG (2011) Expression of three galactinol synthase isoforms in Coffea arabica L. and accumulation of raffinose and stachyose in response to abiotic stresses. Plant Physiol Biochem 49:441–448

    Article  PubMed  Google Scholar 

  • Savchenko G, Klyuchareva E, Abramchik L, Serdyuchenko E (2002) Effect of periodic heat shock on the inner membrane system of etioplasts. Russ J Plant Physiol 49:349–359

    Article  CAS  Google Scholar 

  • Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3(6):1101–1108

    Article  CAS  PubMed  Google Scholar 

  • Somerville C (1991) Plant lipids: metabolism, mutants, and membranes. Science 252:80

    Article  CAS  PubMed  Google Scholar 

  • Sun J, Ren L, Cheng Y, Gao J, Dong B, Chen S, Chen F, Jiang J (2014) Identification of differentially expressed genes in Chrysanthemum nankingense (Asteraceae) under heat stress by RNA Seq. Gene 552:59–66

    Article  CAS  PubMed  Google Scholar 

  • Suzuki N, Mittler R (2006) Reactive oxygen species and temperature stresses: a delicate balance between signaling and destruction. Physiol Plant 126:45–51

    Article  CAS  Google Scholar 

  • Turoczy Z, Kis P, Toeroek K, Cserhati M, Lendvai A, Dudits D, Horvath GV (2011) Overproduction of a rice aldo-keto reductase increases oxidative and heat stress tolerance by malondialdehyde and methylglyoxal detoxification. Plant Mol Biol 75:399–412

    Article  CAS  PubMed  Google Scholar 

  • Vicente AR, Martínez GA, Chaves AR, Civello PM (2006) Effect of heat treatment on strawberry fruit damage and oxidative metabolism during storage. Postharvest Biol Technol 40:116–122

    Article  CAS  Google Scholar 

  • Wahid A (2007) Physiological implications of metabolite biosynthesis for net assimilation and heat-stress tolerance of sugarcane (Saccharum officinarum) sprouts. J Plant Res 120:219–228

    Article  PubMed  Google Scholar 

  • Wahid A, Ghazanfar A (2006) Possible involvement of some secondary metabolites in salt tolerance of sugarcane. J Plant Physiol 163:723–730

    Article  CAS  PubMed  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 

  • Wan XL, Zhou Q, Wang YY, Wang WE, Bao MZ, Zhang JW (2015) Identification of heat-responsive genes in carnation (Dianthus caryophyllus L.) by RNA-seq. Front. Plant Sci 6:519

    Google Scholar 

  • Wang L, Li P, Brutnell TP (2010) Exploring plant transcriptomes using ultra high-throughput sequencing. Brief Funct Genomics 9:118–128

    Article  CAS  PubMed  Google Scholar 

  • Webb L, Darbyshire R, Goodwin I (2014) Climate change: horticulture. In: Alfen NKV (ed) Encyclopedia of agriculture and food systems. Academic Press, Oxford, pp 266–283

    Chapter  Google Scholar 

  • Wu X, Kishitani S, Ito Y, Toriyama K (2009) Accumulation of raffinose in rice seedlings overexpressing OsWRKY11 in relation to desiccation tolerance. Plant Biotech 26:431–434

    Article  CAS  Google Scholar 

  • Xu S, Li JL, Zhang XQ, Wei H, Cui LJ (2006) Effects of heat acclimation pretreatment on changes of membrane lipid peroxidation, antioxidant metabolites, and ultrastructure of chloroplasts in two cool-season turfgrass species under heat stress. Environ Exp Bot 56:274–285

    Article  CAS  Google Scholar 

  • Yin H, Chen Q, Yi M (2008) Effects of short-term heat stress on oxidative damage and responses of antioxidant system in Lilium longiflorum. Plant Growth Regul 54:45–54

    Article  CAS  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. doi:10.1371/journal.pone.0049652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang XW, Rerksiri W, Liu A, Zhou X, Xiong H, Xiang J, Chen X, Xiong X (2013) Transcriptome profile reveals heat response mechanism at molecular and metabolic levels in rice flag leaf. Gene 530:185–192

    Article  CAS  PubMed  Google Scholar 

  • Zhao TY, Martin D, Meeley RB, Downie B (2004) Expression of the maize GALACTINOL SYNTHASE gene family: (II) Kernel abscission, environmental stress and myo-inositol influences accumulation of transcript in developing seeds and callus cells. Physiol Plant 121:647–655

    Article  CAS  Google Scholar 

  • Zhao DQ, Zhou CH, Tao J (2011) Carotenoid accumulation and carotenogenic genes expression during two types of persimmon fruit (Diospyros kaki L.) development. Plant Mol Biol Rep 29:646–654

    Article  CAS  Google Scholar 

  • Zhao DQ, Tao J, Han CX, Ge JT (2012) An actin gene as the internal control for gene expression analysis in herbaceous peony (Paeonia lactiflora Pall.). Afr J Agric Res 7(14):2153–2159

    Google Scholar 

  • Zhao DQ, Jiang Y, Ning CL, Meng JS, Lin S, Ding W, Tao J (2014) Transcriptome sequencing of a chimaera reveals coordinated expression of anthocyanin biosynthetic genes mediating yellow formation in herbaceous peony (Paeonia lactiflora Pall.). BMC Genom 15:689

    Article  Google Scholar 

  • Zhao DQ, Han CX, Zhou CH, Tao J (2015) Shade ameliorates high temperature-induced inhibition of growth in herbaceous peony (Paeonia lactiflora). Int J Agric Biol 17:911–919

    Article  CAS  Google Scholar 

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Acknowledgments

This work was supported by the College Natural Science Research of Jiangsu Province (14KJB210011), the Opening Project of Jiangsu Key Laboratory for Horticultural Crop Genetic Improvement (2014014), the Natural Science Foundation of Yangzhou City (YZ2014033), and the Priority Academic Program Development from Jiangsu Government.

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Correspondence to Jun Tao.

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Zhaojun Hao, Mengran Wei, Saijie Gong, Daqiu Zhao and Jun Tao declares no conflict of interest.

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Hao, Z., Wei, M., Gong, S. et al. Transcriptome and digital gene expression analysis of herbaceous peony (Paeonia lactiflora Pall.) to screen thermo-tolerant related differently expressed genes. Genes Genom 38, 1201–1215 (2016). https://doi.org/10.1007/s13258-016-0465-8

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