Horticulture, Environment, and Biotechnology

, Volume 59, Issue 1, pp 59–70 | Cite as

Transcriptomic and gene expression changes in response to postharvest surface pitting in ‘Lingwu Long’ jujube fruit

  • Xia Liu
  • Tengyue Wang
  • Lan Chen
  • Limei Li
  • Yong Wang
  • Xihong Li
  • Yage Xing
Research Report


‘Lingwu Long’ jujube (Ziziphus jujuba cv. Mill) is a fresh fruit variety that is popular in China. Low temperature storage is an important method for retaining fruit quality postharvest. However, jujube fruits are susceptible to surface pitting under low temperature storage. Therefore, we performed transcriptome analysis to investigate the changes in gene expression in surface-pitted jujube fruit (SPF). First, we developed cDNA libraries of SPF and surface-intact fruit (SIF) that had been stored at − 1 ± 0.5 °C. As a result, 21,136,649 and 21,663,126 high-quality clean reads were generated and 47,386 contigs were obtained. Second, we performed sequences annotation by gene description and gene ontology (GO term) analysis, which clustered the genes into three functional groups. A total of 2706 predicted proteins were assigned to specific metabolic pathways by the Kyoto Encyclopedia of Genes and Genomes database. An analysis of differential gene expression between SPF and SIF revealed more than 1210 genes that are differentially expressed in jujube in response to surface-pitting under low temperature storage, which are involved in lipid, carbohydrate, energy, amino acid, terpenoids, and polyketides metabolism, as well as membrane transport, signal transduction, translation, signal transduction, and biosynthesis of other secondary metabolites. We investigated the pattern of phenylalanine ammonia lyase gene expression in SPF by quantitative reverse-transcription PCR analysis. Our results provide new insights into the biology of surface pitting in jujube, which occurs under low temperature storage. Our findings help confirm the low-temperature tolerance pathways that function in postharvest fruit.


Jujube fruit Surface pitting RNA-seq Low temperature Storage 



This work was supported by the Key Projects in the National Science and Technology Pillar Program during the Twelve Five-year Plan Period of China (2015BAD16B02) and Natural Science Foundation of Tianjin (17JCZDJC34300).

Supplementary material

13580_2018_7_MOESM1_ESM.xls (14.7 mb)
Supplementary material 1 (XLS 15039 kb)
13580_2018_7_MOESM2_ESM.xls (18 kb)
Supplementary material 2 (XLS 18 kb)
13580_2018_7_MOESM3_ESM.xls (190 kb)
Supplementary material 3 (XLS 190 kb)
13580_2018_7_MOESM4_ESM.xlsx (108 kb)
Supplementary material 4 (XLSX 108 kb)
13580_2018_7_MOESM5_ESM.xlsx (53 kb)
Supplementary material 5 (XLSX 52 kb)


  1. Aghdam MS, Bodbodak S (2014) Postharvest heat treatment for mitigation of chilling injury in fruits and vegetables. Food Bioprocess Technol 7:37–53CrossRefGoogle Scholar
  2. Aghdam MS, Asghari M, Farmani B, Mohayeji M, Moradbeygi H (2012) Impact of postharvest brassinosteroids treatment on PAL activity in tomato fruit in response to chilling stress. Sci Hortic 144:116–120CrossRefGoogle Scholar
  3. Allen DJ, Ort DR (2001) Impacts of chilling temperatures on photosynthesis in warm-climate plants. Trends Plant Sci 6:36–42CrossRefPubMedGoogle Scholar
  4. Baginsky S, Hennig L, Zimmermann P, Gruissem W (2010) Gene expression analysis, proteomics, and network discovery. Plant Physiol 152:402–410CrossRefPubMedPubMedCentralGoogle Scholar
  5. Cao S, Yang Z, Zheng Y (2013) Sugar metabolism in relation to chilling tolerance of loquat fruit. Food Chem 136:139–143CrossRefPubMedGoogle Scholar
  6. Chen ZZ, Xue CH, Zhu S, Zhou FF, Ling X, Liu GP, Chen LB (2005) GoPipe: streamlined gene ontology annotation for batch anonymous sequences with statistics. Prog Biochem Biophys 32:187–190Google Scholar
  7. Fung R, Wang CY, Smith DL, Gross KC, Tian MS (2004) MeSA and MeJA increase steady-state transcript levels of alternative oxidase and resistance against chilling injury in sweet peppers (Capsicum annuum L.). Plant Sci 166:711–719CrossRefGoogle Scholar
  8. Huang J, Zhang C, Zhao X, Fei Z, Wan K, Zhang Z, Pang X, Yin X, Bai Y, Sun X, Gao L, Li R, Zhang J, Li X (2016) The jujube genome provides insights into genome evolution and the domestication of sweetness/acidity taste in fruit trees. PLoS Genet 12(12):e1006433. CrossRefPubMedPubMedCentralGoogle Scholar
  9. Hwang EW, Kim KA, Park SC, Jeong MJ, Byun MO, Kwon HB (2005) Expression profiles of hot pepper (Capsicum annuum) genes under cold stress conditions. J Biosci 30:657–667CrossRefPubMedGoogle Scholar
  10. Kanehisa M, Goto S, Furumichi M, Tanabe M, Hirakawa M (2010) KEGG for representation and analysis of molecular networks involving diseases and drugs. Nucleic Acids Res 381:D355–D360CrossRefGoogle Scholar
  11. Li L, Ban Z, Li X, Xue T (2014a) Effect of 1-methylcyclopropene and calcium chloride treatments on quality maintenance of ‘Lingwu Long’ jujube fruit. J Food Sci Technol 51:700–707CrossRefPubMedGoogle Scholar
  12. Li P, Zheng X, Liu Y, Zhu Y (2014b) Pre-storage application of oxalic acid alleviates chilling injury in mango fruit by modulating proline metabolism and energy status under chilling stress. Food Chem 142:72–78CrossRefPubMedGoogle Scholar
  13. Li Y, Xu C, Lin X, Cui B, Wu R, Pang X (2014c) De novo assembly and characterization of the fruit transcriptome of Chinese jujube (Ziziphus jujuba Mill.) using 454 pyrosequencing and the development of novel tri-nucleotide SSR markers. PLoS ONE 9:e106438CrossRefPubMedPubMedCentralGoogle Scholar
  14. Liu H, Jiang-Kuo LI, Nong SZ, Zhang P, Kou WL (2012) Effect of different temperature on chilling injury of ‘Dongzao’ Jujube. Sci Technol Food Ind 33:344–348Google Scholar
  15. Liu M, Zhao J, Cai Q, Liu G, Wang J, Zhao Z, Liu P, Dai L, Yan G, Wang W, Li X, Chen Y, Sun Y, Liu Z, Lin M, Xiao J, Chen Y, Li X, Wu B, Ma Y, Jian J, Yang W, Yuan Z, Sun X, Wei Y, Yu L, Zhang C, Liao S, He R, Guang X, Wang Z, Zhang Y, Luo L (2014) The complex jujube genome provides insights into fruit tree biology. Nat Commun 5:5315CrossRefPubMedPubMedCentralGoogle Scholar
  16. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408CrossRefPubMedGoogle Scholar
  17. Mirdehghan SH, Rahemi M, Martinez-Romero D, Guillen F, Valverde JM, Zapata PJ, Serrano M, Valero D (2007) Reduction of pomegranate chilling injury during storage after heat treatment: role of polyamines. Postharvest Biol Technol 44:19–25CrossRefGoogle Scholar
  18. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5:621–628CrossRefPubMedGoogle Scholar
  19. Ng P, Wei CL, Sung WK, Chiu KP, Lipovich L, Ang CC, Gupta S, Shahab A, Ridwan A, Wong CH, Liu ET, Ruan Y (2005) Gene identification signature (GIS) analysis for transcriptome characterization and genome annotation. Nat Methods 2:105–111CrossRefPubMedGoogle Scholar
  20. Nordby HE, Mcdonald RE (1991) Relationship of epicuticular wax composition of grapefruit to chilling injury. J Agric Food Chem 39:957–962CrossRefGoogle Scholar
  21. Rice P, Longden I, Bleasby A (2000) EMBOSS: the European molecular biology open software suite. Trends Genet 16:276–277CrossRefPubMedGoogle Scholar
  22. Ruelland E, Vaultier M, Zachowski A, Hurry V (2009) Cold signalling and cold acclimation in plants. In: Kader JC, Delseny M (eds) Advances in botanical research. Academic Press, Cambridge, pp 35–150Google Scholar
  23. Rui H, Cao S, Shang H, Jin P, Wang K, Zheng Y (2010) Effects of heat treatment on internal browning and membrane fatty acid in loquat fruit in response to chilling stress. J Sci Food Agric 90:1557–1561CrossRefPubMedGoogle Scholar
  24. Sanchez-Bel P, Egea I, Teresa Sanchez-Ballesta M, Martinez-Madrid C, Fernandez-Garcia N, Romojaro F, Olmos E, Estrella E, Bolarin MC, Borja Flores F (2012) Understanding the mechanisms of chilling injury in bell pepper fruits using the proteomic approach. J Proteomics 75:5463–5478CrossRefPubMedGoogle Scholar
  25. Sevillano L, Sanchez-Ballesta MT, Romojaro F, Flores FB (2009) Physiological, hormonal and molecular mechanisms regulating chilling injury in horticultural species. Postharvest technologies applied to reduce its impact. J Sci Food Agric 89:555–573CrossRefGoogle Scholar
  26. Singh Z (2015) Lost fresh horticultural produce and maintenance of quality in supply chain: tropical and sub-tropical fruit. In: Acedo AL, Kanlayanarat S (eds) Acta horticulturae, vol 1. International Society for Horticultural Science, Leuven, pp 29–39Google Scholar
  27. Wan CY, Wilkins TA (1994) A modified hot borate method significantly enhances the yield of high-quality RNA from cotton (Gossypium hirsutum L.). Anal Biochem 223:7–12CrossRefPubMedGoogle Scholar
  28. Wang C (1982) Physiological and biochemical responses of plants to chilling stress. HortScience 17:173–186Google Scholar
  29. Wang Y, Chen J, Jiang Y, Lu W (2007) Cloning and expression analysis of phenylalanine ammonia-lyase in relation to chilling tolerance in harvested banana fruit. Postharvest Biol Technol 44:34–41CrossRefGoogle Scholar
  30. Wang L, Feng Z, Wang X, Wang X, Zhang X (2010) DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26:136–138CrossRefPubMedGoogle Scholar
  31. Watkins CB, Gapper NE, Nock JF, Giovannoni JJ, Rudell DA, Leisso R, Lee J, Buchanan D, Mattheis J, Hertog M, Nicolai BM, Johnston J, Schaffer R (2015) Interactions between 1-MCP and controlled atmospheres on quality and storage disorders of fruits and vegetables. In: Amodio ML, Colelli G (eds) Acta horticulturae, vol 1. International Society for Horticultural Science, Leuven, pp 45–58Google Scholar
  32. Xiao J, Zhao J, Liu M, Liu P, Dai L, Zhao Z (2015) Genome-wide characterization of simple sequence repeat (SSR) Loci in Chinese jujube and jujube SSR primer transferability. PLoS ONE 10:e0127812CrossRefPubMedPubMedCentralGoogle Scholar
  33. Zhang C, Tian S (2009) Crucial contribution of membrane lipids’ unsaturation to acquisition of chilling-tolerance in peach fruit stored at 0 °C. Food Chem 115:405–411CrossRefGoogle Scholar
  34. Zhang C, Tian S (2010) Peach fruit acquired tolerance to low temperature stress by accumulation of linolenic acid and N-acylphosphatidylethanolamine in plasma membrane. Food Chem 120:864–872CrossRefGoogle Scholar
  35. Zhang C, Ding Z, Xu X, Wang Q, Qin G, Tian S (2010) Crucial roles of membrane stability and its related proteins in the tolerance of peach fruit to chilling injury. Amino Acids 39:181–194CrossRefPubMedGoogle Scholar
  36. Zhang Z, Tian S, Zhu Z, Xu Y, Qin G (2012) Effects of 1-methylcyclopropene(1-MCP) on ripening and resistance of jujube (Zizyphus jujuba cv. Huping) fruit against postharvest disease. LWT Food Sci Technol 45:13–19CrossRefGoogle Scholar

Copyright information

© Korean Society for Horticultural Science and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Xia Liu
    • 1
    • 2
    • 3
  • Tengyue Wang
    • 1
  • Lan Chen
    • 3
  • Limei Li
    • 1
  • Yong Wang
    • 2
  • Xihong Li
    • 1
  • Yage Xing
    • 4
  1. 1.State Key Laboratory of Food Nutrition and SafetyTianjin University of Science and TechnologyTianjinChina
  2. 2.Department of Plant Biology and Ecology, College of Life SciencesNankai UniversityTianjinChina
  3. 3.Tianjin Gasin-Donghui Preservation Technologies Co., Ltd.TianjinChina
  4. 4.Sichuan Province Key Laboratory of Grain and Oil Processing and Food Safety, Food and Bioengineering CollegeXihua UniversityChengduChina

Personalised recommendations