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Transcriptome analysis of peach [Prunus persica (L.) Batsch] stigma in response to low-temperature stress with digital gene expression profiling

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Abstract

The peach [Prunus persica (L.) Batsch] is an important fruit crop that is prone to injury during spring frost, yet little is known about the molecular mechanism of the low temperature (LT) stress response in the peach. In this study, we employed next generation sequencing-technology to characterize the transcriptome of the peach stigma and identify differentially expressed genes (DEGs) of peaches treated at LT (−2 °C) for 4 and 26 h. We obtained a total of 31,273,923 (CK), 37,477,875 (S1), and 36,009,843 (S2) perfect reads from controls, 4 h LT treatment, and 26 h LT treatment, respectively. 96.4–96.8 % of the reads mapped to the peach genome. Gene ontology and pathway enrichment analysis revealed that the upregulated DEGs were predominately involved in response to temperature stimulus, carbohydrate metabolism, biological processes, cytoskeletal, hydrolase activity and primary metabolic pathways. Many of the genes coded for proteins involved in response to LT-associated mechanisms, including the U-box domain-containing protein, CBL-interacting protein kinase, NAC domain-containing protein, and dehydration-responsive element-binding protein. More genes were differentially expressed in S2 (966) compared to S1 (276), and of these, the U-box domain-containing protein 34 had the highest expression in S2. Furthermore, we confirmed differential expression of 20 selected genes via qPCR and found highly similar expression differences to the Illumina analysis. Overall, we identified candidate genes for LT stress in the peach and provide new insights for investigating the molecular mechanisms of LT stress.

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Abbreviations

CBF:

C-repeat binding factor

CBL:

Calcineurin B-like

DEG:

Differentially expression gene

DGE:

Digital gene expression

GO:

Gene ontology

KEGG:

Kyoto encyclopedia of genes and genomes

LT:

Low-temperature

NAC:

Nitrogen assimilation control

NGS:

Next-generation sequencing

References

  • Artlip TS, Wisniewski ME (2002) Induction of proteins in response to biotic and abiotic stresses. Handbook of plant and crop physiology. Marcel Dekker, New York, pp 657–679

    Google Scholar 

  • Arús P, Verde I, Sosinski B, Zhebentyayeva T, Abbott A (2012) The peach genome. Tree Genet Genomes 8:531–547

    Article  Google Scholar 

  • Asmann YW, Klee EW, Thompson EA, Perez EA, Middha S, Oberg AL, Therneau TM, Smith DI, Poland GA, Wieben ED (2009) 3′ tag digital gene expression profiling of human brain and universal reference RNA using illumina genome analyzer. BMC Genomics 10:531

    Article  PubMed  PubMed Central  Google Scholar 

  • Ballard EL, Proebsting EL, Tukey RE (1981) Critical temperatures for blossom buds, peaches. Washington State University Extension Bulletin, 0914

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B (Methodol) 57:289–300

    Google Scholar 

  • Chen N, Yang Q, Hu D, Pan L, Chi X, Chen M, Yang Z, Wang T, Wang M, He Y (2014a) Gene expression profiling and identification of resistance genes to low temperature in leaves of peanut (Arachis hypogaea L.). Sci Hortic 169:214–225

    Article  CAS  Google Scholar 

  • Chen Y, Mao Y, Liu H, Yu F, Li S, Yin T (2014b) Transcriptome analysis of differentially expressed genes relevant to variegation in peach flowers. PLoS One 9:e90842

    Article  PubMed  PubMed Central  Google Scholar 

  • Cheong YH, Kim KN, Pandey GK, Gupta R, Grant JJ, Luan S (2003) Cbl1, a calcium sensor that differentially regulates salt, drought, and cold responses in arabidopsis. Plant Cell 15:1833–1845

    Article  CAS  PubMed  PubMed Central  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 

  • Cui C, Wang LJ, Zhou QY, Tan ZF, Qu CM, Zhang ZS (2014) Expression profiling of genes related to photosynthesis and antioxidant capacity in flue-cured tobacco seedlings subjected to chilling stress. Acta Ecol Sin 34:6076–6089 (in Chinese)

    Google Scholar 

  • Davey JW, Hohenlohe PA, Etter PD, Boone JQ, Catchen JM, Blaxter ML (2011) Genome-wide genetic marker discovery and genotyping using next-generation sequencing. Nat Rev Genet 12:499–510

    Article  CAS  PubMed  Google Scholar 

  • De Lorgeril J, Zenagui R, Rosa RD, Piquemal D, Bachère E (2011) Whole transcriptome profiling of successful immune response to Vibrio infections in the oyster Crassostrea gigas by digital gene expression analysis. PLoS One 6:e23142

    Article  PubMed  PubMed Central  Google Scholar 

  • Fowler S, Thomashow MF (2002) Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the cbf cold response pathway. Plant Cell Online 14:1675–1690

    Article  CAS  Google Scholar 

  • Graham D, Patterson BD (1982) Responses of plants to low, nonfreezing temperatures: proteins, metabolism, and acclimation. Ann Rev Plant Physiol 33:347–372

    Article  CAS  Google Scholar 

  • Hao QN, Zhou XA, Ai HS, Wang C, Zhou R, Chen SL (2011) Identification of genes associated with nitrogen-use efficiency by genome-wide transcriptional analysis of two soybean genotypes. BMC Genomics 12:525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hughes MA, Dunn MA (1996) The molecular biology of plant acclimation to low temperature. J Exp Bot 47:291–305

    Article  CAS  Google Scholar 

  • Kaplan F, Sung DY, Guy CL (2006) Roles of β-amylase and starch breakdown during temperatures stress. Physiol Plantarum 126:120–128

    Article  CAS  Google Scholar 

  • Lee BH, Henderson DA, Zhu JK (2005) The Arabidopsis cold-responsive transcriptome and its regulation by ICE1. Plant Cell 17:3155–3175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li W, Ahn IP, Ning Y, Park CH, Zeng L, Whitehill JG, Lu H, Zhao Q, Ding B, Xie Q, Zhou JM, Dai L, Wang GL (2012) The U-Box/Arm E3 Ligase PUB13 regulates cell death, defense, and flowering time in Arabidopsis. Plant Physiol 159:239–250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liang L, Zhang B, Yin XR, Xu CJ, Sun CD, Chen KS (2013) Differential expression of the CBF gene family during postharvest cold storage and subsequent shelf-life of peach fruit. Plant Mol Biol Rep 31:1358–1367

    Article  CAS  Google Scholar 

  • Liang M, Chen D, Lin M, Zheng Q, Huang Z, Lin Z, Zhao G (2014) Isolation and characterization of two DREB1 genes encoding dehydration-responsive element binding proteins in chicory (Cichorium intybus). Plant Growth Regul 73:45–55

    Article  CAS  Google Scholar 

  • Liu J, Li W, Ning Y, Shirsekar G, Cai Y, Wang X, Dai L, Wang Z, Liu W, Wang GL (2012) The U-Box E3 Ligase SPL11/PUB13 is a convergence point of defense and flowering signaling in plants. Plant Physiol 160:28–37

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Medina J, Catalá R, Salinas J (2011) The CBFs: three arabidopsis transcription factors to cold acclimate. Plant Sci 180:3–11

    Article  CAS  PubMed  Google Scholar 

  • Meng QR, Wang WF, Liang YQ, Nie QJ, Li YH, Du SH, Yang JM (2008) Study on supercoiling point and freezing point in floral organs of apricot. Sci Agric Sin 41:1128–1133 (in Chinese)

    Google Scholar 

  • Miranda C, Santesteban LG, Royo JB (2005) Variability in the relationship between frost temperature and injury level for some cultivated Prunus species. HortScience 40:357–361

    Google Scholar 

  • Mizoguchi T, Hayashida N, Yamaguchi-Shinozaki K, Kamada H, Shinozaki K (1993) Atmpks: a gene family of plant map kinases in Arabidopsis Thaliana. FEBS Lett 336:440–444

    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 

  • Nielsen TH, Deiting U, Stitt M (1997) A [beta]-amylase in potato tubers is induced by storage at low temperature. Plant Physiol 113:503–510

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parkin KL, Marangoni A, Jackman RL, Yada RY, Stanley DW (1989) Chilling injury. A review of possible mechanisms. J Food Biochem 13:127–153

    Article  CAS  Google Scholar 

  • Proebsting EL, Mills HH (1978) Low temperature resistance of developing flower buds of six deciduous fruit species. J Am Soc Hort Sci 103:192–198

    Google Scholar 

  • Puhakainen T, Li C, Boije-Malm M, Kangasjärvi J, Heino P, Palva ET (2004) Short-day potentiation of low temperature-induced gene expression of a c-repeat-binding factor-controlled gene during cold acclimation in silver birch. Plant Physiol 136:4299–4307

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qi XH, Xu XW, Lin XJ, Zhang WJ, Chen XH (2012) Identification of differentially expressed genes in cucumber (Cucumis sativus L.) root under waterlogging stress by digital gene expression profile. Genomics 99:160–168

    Article  CAS  PubMed  Google Scholar 

  • Renaut J, Hausman JF, Bassett C, Artlip T, Cauchie HM, Witters E, Wisniewski M (2008) Quantitative proteomic analysis of short photoperiod and low-temperature responses in bark tissues of peach (Prunus persica L. Batsch). Tree Genet Genomes 4:589–600

    Article  Google Scholar 

  • Savitch LV, Allard G, Seki M, Robert LS, Tinker NA, Huner NP, Shinozaki K, Singh J (2005) The effect of overexpression of two brassica CBF/DREB1-like transcription factors on photosynthetic capacity and freezing tolerance in brassica napus. Plant Cell Physiol 46:1525–1539

    Article  CAS  PubMed  Google Scholar 

  • Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T (2002) Monitoring the expression profiles of 7000 arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 31:279–292

    Article  CAS  PubMed  Google Scholar 

  • Seo PJ, Jung JH, Park MJ, Lee K, Park CM (2013) Controlled turnover of CONSTANS protein by the HOS1 E3 ligase regulates floral transition at low temperatures. Plant Signal Behav 8:43277–43287

    Article  Google Scholar 

  • Shimono H, Okada M, Kanda E, Arakawa I (2007) Low temperature-induced sterility in rice: evidence for the effects of temperature before panicle initiation. Field Crops Res 101:221–231

    Article  Google Scholar 

  • Stockinger EJ, Gilmour SJ, Thomashow MF (1997) Arabidopsis Thaliana Cbf1 encodes an Ap2 domain-containing transcriptional activator that binds to the C-repeat/Dre, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proc Natl Acad Sci USA 94:1035–1040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Surget-Groba Y, Montoya-Burgos JI (2010) Optimization of de novo transcriptome assembly from next-generation sequencing data. Genome Res 20:1432–1440

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Biol 50:571–599

    Article  CAS  Google Scholar 

  • Tong Z, Gao Z, Wang F, Zhou J, Zhang Z (2009) Selection of reliable reference genes for gene expression studies in peach using real-time PCR. BMC Mol Biol 10:71

    Article  PubMed  PubMed Central  Google Scholar 

  • Vanková R, Kosová K, Dobrev P, Vítámvás P, Trávníčková A, Cvikrová M, Pešek B, Gaudinová A, Prerostová S, Musilová J (2014) Dynamics of cold acclimation and complex phytohormone responses in Triticum monococcum lines G3116 and DV92 differing in vernalization and frost tolerance level. Environ Exp Bot 101:12–25

    Article  Google Scholar 

  • Verde I, Abbott AG, Scalabrin S, Jung S, Shu S, Marroni F, Salamini F, Zuccolo A (2013) The high-quality draft genome of peach (Prunus persica) identifies unique patterns of genetic diversity, domestication and genome evolution. Nat Genet 45:487–494

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Welling A, Rinne P, Viherä-Aarnio A, Kontunen-Soppela S, Heino P, Palva ET (2004) Photoperiod and temperature differentially regulate the expression of two dehydrin genes during overwintering of birch (Betula pubescens Ehrh.). J Exp Bot 55:507–516

    Article  CAS  PubMed  Google Scholar 

  • Westwood MN (1993) Temperate-zone pomology: physiology and culture. Timber Press, Portland

    Google Scholar 

  • Wisniewski ME (2014) Field evaluation of apple overexpressing a peach CBF gene confirms its effect on cold hardiness, dormancy, and growth. In: Plant and animal genome XXII conference, plant and animal genome. https://pag.confex.com/pag/xxii/webprogram/Paper9853.html

  • Wisniewski M, Arora R (2000) Structural and biochemical aspects of cold hardiness in woody plants. In: Mohan SJ, Subhash MC (eds) Molecular biology of woody plants. Springer, Netherlands, pp 419–437

  • Wisniewski M, Bassett C, Gusta LV (2003) An overview of cold hardiness in woody plants: seeing the forest through the trees. HortScience 38:952–959

    Google Scholar 

  • Wisniewski ME, Bassett CL, Renaut J, Farrell R, Tworkoski T, Artlip TS (2006) Differential regulation of two dehydrin genes from peach (Prunus persica) by photoperiod, low temperature and water deficit. Tree Physiol 26:575–584

    Article  CAS  PubMed  Google Scholar 

  • Wisniewski M, Norelli J, Bassett C, Artlip T, Macarisin D (2011) Ectopic expression of a novel peach (Prunus persica) CBF transcription factor in apple (Malus × domestica) results in short-day induced dormancy and increased cold hardiness. Planta 233:971–983

    Article  CAS  PubMed  Google Scholar 

  • Wisniewski M, Norelli J, Phillips J, Artlip T, Korban S (2012) Using an apple microarray to characterize the CBF-regulon in transgenic ‘M. 26’ apple trees overexpressing a peach CBF gene. Meeting Abstract p 45

  • Xiao H, Siddiqua M, Braybrook S, Nassuth A (2006) Three grape CBF/DREB1 genes respond to low temperature, drought and abscisic acid. Plant, Cell Environ 29:1410–1421

    Article  CAS  Google Scholar 

  • Xie C, Mao X, Huang J, Ding Y, Wu J, Dong S, Kong L, Gao G, Li CY, Wei L (2011) Kobas 2.0: a web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Res 39:W316–W322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803

    Article  CAS  PubMed  Google Scholar 

  • Yoo SY, Kim Y, Kim SY, Lee JS, Ahn JH (2007) Control of flowering time and cold response by a NAC-domain protein in Arabidopsis. PLoS One 2:e642

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We thank Rangjin Xie for his comments on an earlier version and Yan Chen for his assistance in the data analysis. The Ningbo Agricultural Science and Education funded this research (Grant Number: 2015NK22).

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Authors and Affiliations

  1. Institute of Forestry, Ningbo Academy of Agricultural Science, No. 19 Dehou Street, Ningbo, 315040, Zhejiang, People’s Republic of China

    Yun Jiao

  2. Jiangsu Key Laboratory for Horticultural Crop Genetic Improvement, Institute of Horticulture, Jiangsu Academy of Agricultural Sciences, No. 50 Zhongling Street, Nanjing, 210014, Jiangsu, People’s Republic of China

    Yun Jiao, Zhijun Shen & Juan Yan

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  1. Yun Jiao
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  2. Zhijun Shen
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Correspondence to Yun Jiao.

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Jiao, Y., Shen, Z. & Yan, J. Transcriptome analysis of peach [Prunus persica (L.) Batsch] stigma in response to low-temperature stress with digital gene expression profiling. J. Plant Biochem. Biotechnol. 26, 141–148 (2017). https://doi.org/10.1007/s13562-016-0374-6

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