Skip to main content
SpringerLink
Log in

Transcriptomic analysis of cut tree peony with glucose supply using the RNA-Seq technique

  • Original Paper
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

Several unigenes encoding ACS and ERF involved in ethylene biosynthesis and signal transduction were greatly down-regulated in the petal transcriptome of cut tree peony ‘Luoyang Hong’ with glucose treatment. Glucose also repressed stress-related transcription factor genes DREB, CBF, NAC, WRKY and bHLH.

Abstract

Tree peony (Paeonia suffruticosa Andrews) is a famous traditional flower in China. Glucose supply prolonging vase life of cut tree peony flowers is associated with its role in the suppression of sensitivity to ethylene and ethylene production, but the regulation mechanism of sugar on ethylene biosynthesis and signaling is unclear. In the present work, a normalized cDNA pool was constructed as the reference transcriptome from mixed petals of different developmental cut tree peony ‘Luoyang Hong’ and sequenced using the Illumina HiSeq™ 2000 platform. We obtained 33,117 unigenes annotated with public protein databases. In addition, the transcriptome change in petals of cut tree peony with glucose supply and the control treatment was investigated. With non-redundant annotation, 173 differentially expressed genes were identified, with 41 up-regulated genes and 132 down-regulated genes. According to RNA-Seq data and real-time quantitative polymerase chain reaction validation, one unigene encoding ACS, a key ethylene synthetic enzyme, and four unigenes encoding ERF, which is involved in ethylene signal transduction was greatly down-regulated with glucose treatment. Furthermore, stress-related transcription factor genes DREB, CBF, NAC, WRKY and bHLH were also repressed with glucose supply, as well as several other stress-responsive and stress-tolerance genes, indicating that glucose supply probably releases the effects induced by various environmental stress. All the results and analysis are valuable resources for better understanding of the beneficial influence of exogenous sugars on cut tree peony.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

ACC:

1-Aminocyclopropane-1-carboxylate

ACO:

ACC oxidase

ACS:

ACC synthase

bHLH:

Helix-loop-helix

CBF:

C-repeat binding factor

DEG:

Differentially expressed gene

DREB:

Dehydration-responsive element-binding protein

EBF:

EIN3-binding f-box protein

EIN:

Ethylene-insensitive

ERF:

Ethylene-responsive transcription factor

NAC:

NAM/ATAF1/CUC

RNA-Seq:

RNA sequencing

RPKM:

Reads per kb per million reads

RT-qPCR:

Real-time quantitative polymerase chain reaction

References

  • Agarwal PK, Agarwal P, Reddy M, Sopory SK (2006) Role of DREB transcription factors in abiotic and biotic stress tolerance in plants. Plant Cell Rep 25:1263–1274

    Article  CAS  PubMed  Google Scholar 

  • Akhtar M, Jaiswal A, Taj G, Jaiswal J, Qureshi M, Singh N (2012) DREB1/CBF transcription factors: their structure, function and role in abiotic stress tolerance in plants. J Genet 91:385–395

    Article  CAS  PubMed  Google Scholar 

  • An F, Zhao Q, Ji Y, Li W, Jiang Z, Yu X, Zhang C, Han Y, He W, Liu Y, Zhang S, Ecker JR, Guo H (2010) Ethylene-induced stabilization of ETHYLENE INSENSITIVE3 and EIN3-LIKE1 is mediated by proteasomal degradation of EIN3 binding F-box 1 and 2 that requires EIN2 in Arabidopsis. Plant Cell 22:2384–2401

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Benjamini Y, Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. Ann Stat 29:1165–1188

    Article  Google Scholar 

  • Borochov A, Woodson WR (1989) Physiology and biochemistry of flower petal senescence. Hortic Rev 11:15–43

    CAS  Google Scholar 

  • Chang S, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Rep 11:113–116

    Article  CAS  Google Scholar 

  • Chen YF, Etheridge N, Schaller GE (2005) Ethylene signal transduction. Ann Bot 95:901–915

    Article  CAS  PubMed  Google Scholar 

  • Conesa A, Götz S, García-Gómez J, Terol J, Talón M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676

    Article  CAS  PubMed  Google Scholar 

  • Dalal M, Tayal D, Chinnusamy V, Bansal KC (2009) Abiotic stress and ABA-inducible group 4 LEA from Brassica napus plays a key role in salt and drought tolerance. J Biotechnol 139:137–145

    Article  CAS  PubMed  Google Scholar 

  • Dekkers BJW, Schuurmans JAMJ, Smeekens SCM (2008) Interaction between sugar and abscisic acid signalling during early seedling development in Arabidopsis. Plant Mol Biol 67:151–167

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gai S, Zhang Y, Mu P, Liu C, Liu S, Dong L, Zheng G (2012) Transcriptome analysis of tree peony during chilling requirement fulfillment: assembling, annotation and markers discovering. Gene 497:256–262

    Article  CAS  PubMed  Google Scholar 

  • Gao J, Dong L (2010) Cloning and sequence analysis of CTR1 gene family sequences and its 3′ cDNA ends from tree peony. Biotechnol Bull 9:100–105

    Google Scholar 

  • Gao J, Jia P, Wang Y, Zhang C, Wang W, Dong L (2011) Effects of ethylene and 1-MCP treatments on the expressions of CTR genes of tree peony. Acta Bot Boreal-Occident Sin 31:19–26

    CAS  Google Scholar 

  • Gibson SI (2000) Plant sugar-response pathways. Part of a complex regulatory web. Plant Physiol 124:1532–1539

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gibson SI (2005) Control of plant development and gene expression. Curr Opin Plant Biol 8:93–102

    Article  CAS  PubMed  Google Scholar 

  • Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Guo H, Ecker JR (2004) The ethylene signaling pathway: new insights. Curr Opin Plant Biol 7:40–49

    Article  CAS  PubMed  Google Scholar 

  • Guo WW, Dong L, Wang LY, Chen RX, Liu AQ (2004) The postharvest characteristics and water balance of some cultivars of tree-peony cut flowers. Scientia Silvae Sinicae 40:89–93

    Google Scholar 

  • Halevy AH, Mayak S (1979) Senescence and postharvest physiology of cut flowers. Part 1. Hortic Rev 1:204–236

    CAS  Google Scholar 

  • Hoeberichts FA, van Doorn WG, Vorst O, Hall RD, van Wordragen MF (2007) Sucrose prevents up-regulation of senescence-associated genes in carnation petals. J Exp Bot 58:2873–2885

    Article  CAS  PubMed  Google Scholar 

  • Iseli C, Jongeneel CV, Bucher P (1999) ESTScan: a program for detecting, evaluating, and reconstructing potential coding regions in EST sequences. Proc Int Conf Intell Syst Mol Biol 138–148

  • Jang JC, Sheen J (1994) Sugar sensing in higher plants. Plant Cell 6:1665–1679

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jia PY, Zhou L, Guo WW, Wang LY, Dong L (2008) Postharvest behavior and endogenous ethylene pattern of Paeonia suffruticosa cut flowers. Acta Hortic 768:445–450

    CAS  Google Scholar 

  • Kende H (1989) Enzymes of ethylene biosynthesis. Plant Physiol 91:1–4

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lee J, Noh EK, Choi HS, Shin SC, Park H, Lee H (2012) Transcriptome sequencing of the Antarctic vascular plant Deschampsia antarctica Desv. under abiotic stress. Planta 237:823–836

    Article  PubMed  Google Scholar 

  • León P, Sheen J (2003) Sugar and hormone connections. Trends Plant Sci 8:110–116

    Article  PubMed  Google Scholar 

  • Li Y, Lee KK, Walsh S, Smith C, Hadingham S, Sorefan K, Cawley G, Bevan MW (2006) Establishing glucose-and ABA-regulated transcription networks in Arabidopsis by microarray analysis and promoter classification using a relevance vector machine. Genome Res 16:414–427

    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 

  • Lin Z, Zhong S, Grierson D (2009) Recent advances in ethylene research. J Exp Bot 60:3311–3336

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Li J, Wang H, Fu Z, Liu L, Yu Y (2011) Identification and expression analysis of ERF transcription factor genes in petunia during flower senescence and in response to hormone treatments. J Exp Bot 62:825–840

    Article  CAS  PubMed  Google Scholar 

  • Lomax J (2005) Get ready to GO! A biologist’s guide to the gene ontology. Brief Bioinform 6:298–304

    Article  CAS  PubMed  Google Scholar 

  • Ma N, Xue J, Li Y, Liu X, Dai F, Jia W, Luo Y, Gao J (2008) Rh-PIP2; 1, a rose aquaporin gene, is involved in ethylene-regulated petal expansion. Plant Physiol 148:894–907

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Marrs KA (1996) The functions and regulation of glutathione S-transferases in plants. Annu Rev Plant Biol 47:127–158

    CAS  Google Scholar 

  • Mayak S, Dilley DR (1976) Effect of sucrose on response of cut carnation flowers to kinetin, ethylene and abscisic acid. J Am Soc Hort Sci 101:583–585

    CAS  Google Scholar 

  • Moore B, Zhou L, Rolland F, Hall Q, Cheng WH, Liu YX, Hwang I, Jones T, Sheen J (2003) Role of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signaling. Science 300:332–336

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Ogawa T, Ueda Y, Yoshimura K, Shigeoka S (2005) Comprehensive analysis of cytosolic nudix hydrolases in Arabidopsis thaliana. J Biol Chem 280:25277–25283

    Article  CAS  PubMed  Google Scholar 

  • Olsen AN, Ernst HA, Leggio LL, Skriver K (2005) NAC transcription factors: structurally distinct, functionally diverse. Trends Plant Sci 10:79–87

    Article  CAS  PubMed  Google Scholar 

  • Potuschak T, Lechner E, Parmentier Y, Yanagisawa S, Grava S, Koncz C, Genschik P (2003) EIN3-dependent regulation of plant ethylene hormone signaling by two Arabidopsis F box proteins-EBF1 and EBF2. Cell 115:679–689

    Article  CAS  PubMed  Google Scholar 

  • Pun UK, Ichimura K (2003) Role of sugars in senescence and biosynthesis of ethylene in cut flowers. Jarq-Jpn Agr Res Q 37:219–224

    CAS  Google Scholar 

  • Ramon M, Rolland F, Sheen J (2008) Sugar sensing and signaling. Arabidopsis Book 6:e0117. doi:10.1199/tab.0117

    Article  PubMed Central  PubMed  Google Scholar 

  • Rolland F, Moore B, Sheen J (2002) Sugar sensing and signaling in plants. Plant Cell 14(Suppl.):S185–S205

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol 57:675–709

    Article  CAS  PubMed  Google Scholar 

  • Ryu H-S, Han M, Lee S-K, Cho J-I, Ryoo N, Heu S, Lee Y-H, Bhoo SH, Wang G-L, Hahn T-R (2006) A comprehensive expression analysis of the WRKY gene superfamily in rice plants during defense response. Plant Cell Rep 25:836–847

    Article  CAS  PubMed  Google Scholar 

  • Sheen J, Zhou L, Jang JC (1999) Sugars as signaling molecules. Curr Opin Plant Biol 2:410–418

    Article  CAS  PubMed  Google Scholar 

  • Shu QY, Wischnitzki E, Liu ZA, Ren HX, Han XY, Hao Q, Gao FF, Xu SX, Wang LS (2009) Functional annotation of expressed sequence tags as a tool to understand the molecular mechanism controlling flower bud development in tree peony. Physiol Plant 135:436–449

    Article  CAS  PubMed  Google Scholar 

  • Smeekens S (2000) Sugar-induced signal transduction in plants. Annu Rev Plant Physiol Plant Mol Biol 51:49–81

    Article  CAS  PubMed  Google Scholar 

  • Smeekens S, Ma J, Hanson J, Rolland F (2010) Sugar signals and molecular networks controlling plant growth. Curr Opin Plant Biol 13:274–279

    Article  CAS  PubMed  Google Scholar 

  • Tanase K, Nishitani C, Hirakawa H, Isobe S, Tabata S, Ohmiya A, Onozaki T (2012) Transcriptome analysis of carnation (Dianthus caryophyllus L.) based on next-generation sequencing technology. BMC Genomics 13:292

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Trick M, Adamski NM, Mugford SG, Jiang CC, Febrer M, Uauy C (2012) Combining SNP discovery from next-generation sequencing data with bulked segregant analysis (BSA) to fine-map genes in polyploid wheat. BMC Plant Biol 12:14

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • van Doorn WG, Woltering EJ (2008) Physiology and molecular biology of petal senescence. J Exp Bot 59:453–480

    Article  PubMed  Google Scholar 

  • Verlinden S, Garcia JJV (2004) Sucrose loading decreases ethylene responsiveness in carnation (Dianthus caryophyllus cv. White Sim) petals. Postharvest Biol Technol 31:305–312

    Article  CAS  Google Scholar 

  • Wang H-Y, Klatte M, Jakoby M, Bäumlein H, Weisshaar B, Bauer P (2007) Iron deficiency-mediated stress regulation of four subgroup Ib BHLH genes in Arabidopsis thaliana. Planta 226:897–908

    Article  CAS  PubMed  Google Scholar 

  • Wang T, Tong Z, Ma N, Gao J (2009a) Isolation and expression analysis of Rh-DREB1s gene in cut roses (Rosa hybrida) under ethylene treatment and water deficit stress. Acta Hortic Sinica 36:65–72

    Google Scholar 

  • Wang Z, Gerstein M, Snyder M (2009b) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10:57–63

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wang XW, Luan JB, Li JM, Bao YY, Zhang CX, Liu SS (2010a) De novo characterization of a whitefly transcriptome and analysis of its gene expression during development. BMC Genomics 11:400

    Article  PubMed Central  PubMed  Google Scholar 

  • Wang Z, Fang B, Chen J, Zhang X, Luo Z, Huang L, Chen X, Li Y (2010b) De novo assembly and characterization of root transcriptome using Illumina paired-end sequencing and development of cSSR markers in sweet potato (Ipomoea batatas). BMC Genomics 11:726

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wang S, Wang X, He Q, Liu X, Xu W, Li L, Gao J, Wang F (2012a) Transcriptome analysis of the roots at early and late seedling stages using Illumina paired-end sequencing and development of EST-SSR markers in radish. Plant Cell Rep 31:1437–1447

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Dong L, Zhang C, Wang X (2012b) Reference gene selection for real-time quantitative PCR normalization in tree peony (Paeonia suffruticosa Andr.). J Agric Biotechnol 20:521–528

    CAS  Google Scholar 

  • Wang Y, Zhang C, Jia P, Wang X, Wang W, Dong L (2013) Isolation and expression analysis of three EIN3-like genes in tree peony (Paeonia suffruticosa). Plant Cell Tiss Organ Cult 112:181–190

    Article  CAS  Google Scholar 

  • Xie F, Burklew CE, Yang Y, Liu M, Xiao P, Zhang B, Qiu D (2012) De novo sequencing and a comprehensive analysis of purple sweet potato (Ipomoea batatas L.) transcriptome. Planta 236:101–113

    Article  CAS  PubMed  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  CAS  PubMed Central  PubMed  Google Scholar 

  • Yanagisawa S, Yoo SD, Sheen J (2003) Differential regulation of EIN3 stability by glucose and ethylene signalling in plants. Nature 425:521–525

    Article  CAS  PubMed  Google Scholar 

  • Yang SF, Hoffman NE (1984) Ethylene biosynthesis and its regulation in higher plants. Ann Rev Plant Physiol 35:155–189

    Article  CAS  Google Scholar 

  • Ye J, Fang L, Zheng H, Zhang Y, Chen J, Zhang Z, Wang J, Li S, Li R, Bolund L, Wang J (2006) WEGO: a web tool for plotting GO annotations. Nucleic Acids Res 34:W293–W297

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zenoni S, Ferrarini A, Giacomelli E, Xumerle L, Fasoli M, Malerba G, Bellin D, Pezzotti M, Delledonne M (2010) Characterization of transcriptional complexity during berry development in Vitis vinifera using RNA-Seq. Plant Physiol 152:1787–1795

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang C, Liu M, Fu J, Wang Y, Dong L (2012a) Exogenous sugars involvement in senescence and ethylene production of tree peony ‘Luoyang Hong’ cut flowers. Kor J Hort Sci Technol 30:718–724

    CAS  Google Scholar 

  • Zhang C, Zhou X, Jia P, Dong L, Zhang X (2012b) Postharvest characteristics of potted tree peony cultivars and response of postharvest quality of ‘Luoyanghong’ to 1-MCP treatment. J Northeast For Univ 40:14–18

    Google Scholar 

  • Zhang Y, Zhang S, Han S, Li X, Qi L (2012c) Transcriptome profiling and in silico analysis of somatic embryos in Japanese larch (Larix leptolepis). Plant Cell Rep 31:1637–1657

    Article  CAS  PubMed  Google Scholar 

  • Zhou L, Jia PY, Liu J, Wang WR, Huo ZP, Dong L (2009) Effect of ethylene on cut flowers of tree peony ‘Luoyanghong’ opening and senescence process and endogenous ethylene biosynthesis. Acta Hortic Sinica 36:239–244

    CAS  Google Scholar 

  • Zhou L, Dong L, Jia PY, Wang WR, Wang LY (2010) Expression of ethylene receptor and transcription factor genes, and ethylene response during flower opening in tree peony (Paeonia suffruticosa). Plant Growth Regul 62:171–179

    Article  CAS  Google Scholar 

  • Zhou L, Zhang C, Fu J, Liu M, Zhang Y, Wang Y, Dong L (2013) Molecular characterization and expression of ethylene biosynthetic genes during cut flower development in tree peony (Paeonia suffruticosa) in response to ethylene and functional analysis of PsACS1 in Arabidopsis. J Plant Growth Regul 32:362–375

    Article  CAS  Google Scholar 

  • Zhu G, Ye N, Zhang J (2009) Glucose-induced delay of seed germination in rice is mediated by the suppression of ABA catabolism rather than an enhancement of ABA biosynthesis. Plant Cell Physiol 50:644–651

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Natural Science Foundation of China (30972030).

Author information

Authors and Affiliations

  1. College of Landscape Architecture, National Flower Engineering Technology Research Center, Beijing Forestry University, Beijing, 100083, People’s Republic of China

    Chao Zhang, Yanjie Wang, Jianxin Fu, Li Dong, Shulin Gao & Danni Du

Authors
  1. Chao Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yanjie Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jianxin Fu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Li Dong
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Shulin Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Danni Du
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Li Dong.

Additional information

Communicated by H. Judelson.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhang, C., Wang, Y., Fu, J. et al. Transcriptomic analysis of cut tree peony with glucose supply using the RNA-Seq technique. Plant Cell Rep 33, 111–129 (2014). https://doi.org/10.1007/s00299-013-1516-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-013-1516-0

Keywords

Search

Navigation