Physiological Change and Transcriptome Analysis of Chinese Wild Vitis amurensis and Vitis vinifera in Response to Cold Stress

Abstract

The Chinese wild Vitis amurensis Rupr. is a crucial resource for cold-resistant germplasm, but the molecular mechanism of cold resistance in V. amurensis has not been clarified. We conducted a physiological and transcriptome analysis of potted plants of V. amurensis accession “Shuangyou” (cold-resistant) and Vitis vinifera cultivar “Red Globe” (cold-sensitive) subjected to 0 °C for 3, 12, 48, and 72 h. The “Shuangyou” exhibited lower electrolyte leakage (EL) and malondialdehyde (MDA) compared with “Red Globe.” The proline contents in “Shuangyou” was higher than “Red Globe” at 0 and 48 h while lower than “Red Globe” at other time points. On the whole, catalase (CAT), superoxide dismutase (SOD), and peroxidase (POD) activity in “Shuangyou” was higher than “Red Globe,” and ascorbate peroxidase (APX) activity in “Shuangyou” was lower than “Red Globe.” Transcriptome analysis showed that 240, 310, 1072, and 1107 differentially expressed genes (DEGs) were detected in “Red Globe” at 3, 12, 48, and 72 h, respectively, and 32, 1161, 1894, and 3290 DEGs were found in “Shuangyou” at the same time points, respectively. Functional categories of DEGs included metabolic processes and signal transduction involved with cold resistance in grapevine. The high expression level of encoding peroxiredoxin genes in V. amurensis revealed a strong ability to scavenge reactive oxygen species (ROS). The expression levels of 5 DEGs in “Shuangyou” were more than 20 times higher than those of “Red Globe” at all time points, indicating that some cold-related special pathways maybe involved in V. amurensis. These related genes, as candidate transcripts, may contribute to excellent cold-hardiness breeding in grape.

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References

  1. Adams E, Frank L (1970) Metabolism of proline and the hydroxyprolines. Annu Rev Biochem 5:1005–1061

    Google Scholar 

  2. Agarwal M, Hao Y, Kapoor A, Dong CH, Fujii H, Zheng X, Zhu JK (2006) A R2R3 type MYB transcription factor is involved in the cold regulation of CBF genes and in acquired freezing tolerance. J Biol Chem 281:37636–37645

    CAS  PubMed  Google Scholar 

  3. Al-aghabary K, Zhu Z, Shi Q (2005) Influence of silicon dupply on chlorophyll content, chlorophyll fluorescence, and antioxidative enzyme activities in tomato plants under salt stress. J Plant Nutr 27:2101–2115

    Google Scholar 

  4. Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11:R106

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Phsyiol Plant Mol Biol 50:601–639

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  7. Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  9. Chinnusamy V, Zhu J, Zhu JK (2007) Cold stress regulation of gene expression in plants. Trends Plant Sci 12:444–451

    CAS  PubMed  Google Scholar 

  10. Cui S, Huang F, Wang J, Ma X, Cheng Y, Dr JL (2005) A proteomic analysis of cold stress responses in rice seedlings. Proteomics 5:3162–3172

    CAS  PubMed  Google Scholar 

  11. Dhindsa RS, Plumbdhindsa P, Thorpe TA (1981) Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. J Exp Bot 32:93–101

    CAS  Google Scholar 

  12. Fahmy K, Nakano K, Violalita F (2015) Investigation on quantitative index of chilling injury in cucumber fruit based on the electrolyte leakage and malondialdehyde content. Int J Adv Sci Eng Inf Technol 5:222–225

    Google Scholar 

  13. Franklin KA, Whitelam GC (2007) Light-quality regulation of freezing tolerance in Arabidopsis thaliana. Nat Genet 39:1410–1413

    CAS  PubMed  Google Scholar 

  14. Garg N, Manchanda G (2009) ROS generation in plants: boon or bane? Plant Biosyst 143:81–96

    Google Scholar 

  15. Hao L, Zhang YS, Duan LS, Zhang MC, Li ZH (2017) Cloning, expression and functional analysis of brassinosteroid receptor gene (ZmBRI1) from Zea mays L. Acta Agron Sin 43:1261–1271

    Google Scholar 

  16. Jagloottosen KR, Gilmour SJ, Zarka DG, Schabenberger O, Thomashow MF (1998) Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280:104–106

    CAS  Google Scholar 

  17. Jaillon O, Aury JM, Noel B, Policriti A, Clepet C, Casagrande A, Choisne N, Aubourg S, Vitulo N, Jubin C, Vezzi A, Legeai F, Hugueney P, Dasilva C, Horner D, Mica E, Jublot D, Poulain J, Bruyère C, Billault A, Segurens B, Gouyvenoux M, Ugarte M, Cattonaro F, Anthouard V, Vico V, Del Fabbro C, Alaux M, Di Gaspero G, Dumas V, Felice N, Paillard S, Juman I, Moroldo M, Scalabrin S, Canaguier A, Le Clainche I, Malacrida G, Durand E, Pesole G, Laucou V, Chatelet P, Merdinoglu D, Delledonne M, Pezzotti M, Lecharny A, Scarpelli C, Artiguenave F, Pè ME, Valle G, Morgante M, Caboche M, Adam-Blondon AF, Weissenbach J, Quétier F, Wincker P, French-Italian Public Consortium for Grapevine Genome Characterization (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463–467

    CAS  PubMed  Google Scholar 

  18. Jakob U, Gaestel M, Engel K, Buchner J (1993) Small heat shock proteins are molecular chaperones. J Biol Chem 268:1517–1520

    CAS  PubMed  Google Scholar 

  19. Janská A, Maršík P, Zelenková S, Ovesná J (2010) Cold stress and acclimation - what is important for metabolic adjustment? Plant Biol 12:395–405

    PubMed  Google Scholar 

  20. Jiang B, Shi Y, Zhang X, Xin X, Qi L, Guo H, Li J, Yang S (2017) PIF3 is a negative regulator of the CBF pathway and freezing tolerance in Arabidopsis. P Natl Acad Sci USA 114:E6695

    CAS  Google Scholar 

  21. Krishna P, Sacco M, Cherutti JF, Hill S (1995) Cold-induced accumulation of HSP90 transcripts in Brassica napus. Plant Physiol 107:915–923

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Leivar P, Monte E (2014) PIFs: systems integrators in plant development. Plant Cell 26:56–78

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Leivar P, Monte E, Oka Y, Liu T, Carle C, Castillon A, Huq E, Quail PH (2008) Multiple phytochrome-interacting bHLH transcription factors repress premature seedling photomorphogenesis in darkness. Curr Biol 18:1815–1823

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Li H, Ding YL, Shi YT, Zhang XY, Zhang SQ, Gong ZZ, Yang SH (2017) MPK3- and MPK6-mediated ICE1 phosphorylation negatively regulates ICE1 stability and freezing tolerance in Arabidopsis. Dev Cell 43:630–642

    CAS  PubMed  Google Scholar 

  26. Li J, Wang N, Xin H, Li S (2013) Overexpression of VaCBF4, a transcription factor from Vitis amurensis, improves cold tolerance accompanying increased resistance to drought and salinity in Arabidopsis. Plant Mol Biol Report 31:1518–1528

    CAS  Google Scholar 

  27. Liu DB, Wei JY, Li SP (2008) Effects of brassinolid on chilling-resistance in banana seedlings. Bull Bot Res 28:195–198

    Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Londo JP, Kovaleski AP (2019) Deconstructing cold hardiness: variation in supercooling ability and chilling requirements in the wild grapevine Vitis riparia. Aust J Grape Wine R 25:276–285

    Google Scholar 

  30. Mao X, Zhang H, Tian S, Chang X, Jing R (2010) TaSnRK2.4, an SNF1-type serine/threonine protein kinase of wheat (Triticum aestivumL.), confers enhanced multistress tolerance in Arabidopsis. J Exp Bot 61:683–696

    CAS  PubMed  Google Scholar 

  31. Meyer K, Keil M, Naldrett MJ (1999) A leucine-rich repeat protein of carrot that exhibits antifreeze activity. FEBS Lett 447:171–178

    CAS  PubMed  Google Scholar 

  32. Moieni-Korbekandi Z, Karimzade G, Sharifi M (2014) Cold-induced changes of proline, malondialdehyde and chlorophyll in spring canolacultivars. JPPB 4:1–11

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  34. Mullins MG, Bouquet A, Williams LE (1992) Biology of the grapevine. Cambridge University Press, Cambridge

    Google Scholar 

  35. Neven LG, Haskell DW, Hofig A, Li QB, Guy CL (1993) Characterization of a spinach gene responsive to low temperature and water stress. Plant Mol Biol 21:291–305

    CAS  PubMed  Google Scholar 

  36. Routaboul JM, Fischer SF, Browse J (2000) Trienoic fatty acids are required to maintain chloroplast function at low temperatures. Plant Physiol 124:1697–1705

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Sakuma Y, Liu Q, Dubouzet JG, Abe H, Shinozaki K, Yamaguchi-Shinozaki K (2002) DNA-binding specificity of the ERF/AP2 domain of ArabidopsisDREBs, transcription factors involved in dehydration- and cold-inducible gene expression. Biochem Biophys Res Commun 290:998–1009

    CAS  PubMed  Google Scholar 

  38. Sharma MK, Kumar R, Solanke AU, Sharma R, Tyagi AK, Sharma AK (2010) Identification, phylogeny, and transcript profiling of ERF family genes during development and abiotic stress treatments in tomato. Mol Gen Genomics 284:455–475

    CAS  Google Scholar 

  39. Shinozaki K, Yamaguchishinozaki K (2000) Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Curr Opin Plant Biol 3:217–223

    CAS  PubMed  Google Scholar 

  40. Sidebottom C, Buckley S, Pudney P, Twigg S, Jarman C, Holt C, Telford J, Mcarthur A, Worrall D, Hubbard R (2000) Heat-stable antifreeze protein from grass. Nature 406:256–256

    CAS  PubMed  Google Scholar 

  41. Silva-Ortega CO, Ochoa-Alfaro AE, Reyes-Agüero JA, Aguado-Santacruz GA, Jiménez-Bremont JF (2008) Salt stress increases the expression of P5CS gene and induces proline accumulation in cactus pear. Plant Physiol Biochem 46:82–92

    CAS  PubMed  Google Scholar 

  42. 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. P Natl Acad SciUSA 94:1035–1040

    CAS  Google Scholar 

  43. Storey JD (2002) A direct approach to false discovery rates. J Roy Stat Soc B 64:479–498

    Google Scholar 

  44. Szabados LL, Savourcb A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97

    CAS  Google Scholar 

  45. Theilhaber J, Bushnell S, Jackson A, Fuchs R (2001) Bayesian estimation of fold-changes in the analysis of gene expression: the PFOLD algorithm. J Comput Biol 8:585–614

    CAS  PubMed  Google Scholar 

  46. Theocharis A, Clément C, Barka EA (2012) Physiological and molecular changes in plants grown at low temperatures. Planta 235:1091–1105

    CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  48. Tian Y, Zhang H, Pan X, Chen X, Zhang Z, Lu X, Huang R (2011) Overexpression of ethylene response factor ERF2 confers cold tolerance in rice seedlings. Transgenic Res 20:857–866

    CAS  PubMed  Google Scholar 

  49. Tillett RL, Wheatley MD, Tattersall EAR, Schlauch KA, Cramer GR, Cushman JC (2012) The Vitis vinifera C-repeat binding protein 4 (VvCBF4) transcriptional factor enhances freezing tolerance in wine grape. Plant Biotechnol J 10:105–124

    CAS  PubMed  Google Scholar 

  50. Tiwari BS, Belenghi B, Levine A (2002) Oxidative stress increased respiration and generation of reactive oxygen species, resulting in ATP depletion, opening of mitochondrial permeability transition, and programmed cell death. Plant Physiol 128:1271–1281

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Upadhyay A, Gaonkar T, Upadhyay AK, Jogaiah S, Shinde MP, Kadoo NY, Gupta VS (2018) Global transcriptome analysis of grapevine (Vitis vinifera L.) leaves under salt stress reveals differential response at early and late stages of stress in table grape cv. Thompson seedless. Plant Physiol Biochem 129:168–179

    CAS  PubMed  Google Scholar 

  52. Verbruggen N, Hermans C (2008) Proline accumulation in plants: a review. Amino Acids 35:753–759

    CAS  PubMed  Google Scholar 

  53. Verma V, Ravindran P, Kumar PP (2016) Plant hormone-mediated regulation of stress responses. BMC Plant Biol 16:86

    PubMed  PubMed Central  Google Scholar 

  54. Wan Y, Schwaninger H, Li D, Simon CJ, Wang YJ, He PC (2008) The eco-geographic distribution of wild grape germplasm in China. Vitis 47:77–80

    Google Scholar 

  55. Wang XC, Zhao QY, Ma CL, Zhang ZH, Cao HL, Kong YM, Yue C, Hao XY, Chen L, Ma JQ (2013) Global transcriptome profiles of Camellia sinensis during cold acclimation. BMC Genomics 14:415

    PubMed  PubMed Central  Google Scholar 

  56. Wildi B, Lütz C (1996) Antioxidant composition of selected high alpine plant species from different altitudes. Plant Cell Environ 19:138–146

    CAS  Google Scholar 

  57. Wolfraim LA, Langis R, Tyson H, Dhindsa RS (1993) cDNA sequence, expression, and transcript stability of a cold acclimation-specific gene, CAS18, of alfalfa (Medicago falcata) cells. Plant Physiol 101:1275–1282

    CAS  PubMed  PubMed Central  Google Scholar 

  58. Xin H, Zhu W, Wang L, Xiang Y, Fang L, Li J, Sun X, Wang N, Londo JP, Li S (2013) Genome wide transcriptional profile analysis of Vitis amurensis and Vitis vinifera in response to cold stress. PLoS One 8:e58740

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Xiong L, Zhu JK (2001) Abiotic stress signal transduction in plants: molecular and genetic perspectives. Physiol Plant 112:152–166

    CAS  PubMed  Google Scholar 

  60. Yang Y, Lei Z, Peng F (2007) Research advances about low-temperature-induced proteins and the cold tolerance in plants. Acta Botan Boreali-Occiden Sin 27:421–428

    Google Scholar 

  61. Zhang J, Wu X, Niu R, Liu Y, Liu N, Xu W, Wang Y (2012) Cold-resistance evaluation in 25 wild grape species. Vitis 51(4):153–160

    Google Scholar 

  62. Zhao L, Deng X, Shan L (2005) The response mechanism of active oxygen species removing system to drought stress. Acta Botan Boreali-Occiden Sin 25:413–418

    CAS  Google Scholar 

  63. Zhao CZ, Wang PC, Si T, Hsu HH, Wang L, Zayed O, Yu ZP, Zhu YF, Dong J, Tao WA, Zhu JK (2017) MAP kinase cascades regulate the cold response by modulating ICE1 protein stability. Dev Cell 43:618–629

    CAS  PubMed  PubMed Central  Google Scholar 

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Funding

This work received financial support from Shaanxi Province Key Project-Agriculture of the Peoples Republic of China (Grant no. 2017ZDXM-NY-026) and also from The National Science-Technology Support Plan Projects from the Ministry of Science and Technology of the Peoples Republic of China (Grant no. 2013BAD02B04-06).

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Contributions

Bao Gu performed qRT-PCR, data analysis and revision of the manuscript. Bo Zhang carried out grapevine materials preparation, the data analysis, and manuscript writing. Lan Ding, Peiying Li, and Li Shen measured the physiochemical indexes of grape leaves under cold stress and none-stress treatments. Jianxia Zhang designed the experiment and revised the manuscript.

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Correspondence to Jianxia Zhang.

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Highlights

The most cold-resistant Vitis amurensis was used for searching the key cold-resistant genes. Large numbers of DEGs related to cold response were identified, and most of them were related to metabolic processes and signal transduction. Some related peroxiredoxin and transcription factors were potential candidate genes to enhance the cold resistance of grapevine.

Electronic Supplementary Material

Fig. S1
figure8

Quantitative RT-PCR validations. Twelve genes were selected for the quantitative RT-PCR analysis, including zinc finger (AN1-like) family protein(A), cationic amino acid transporter(B), polyamine oxidase(C), E3 ubiquitin-protein ligase(D), allene oxide synthase(E), WRKY transcription factor 26(F), 3-ketoacyl-CoA synthase(G), omega-3 fatty acid desaturase(H), early light-induced protein(I), AAA-ATPase(J), DELLA protein(K). (PNG 4073 kb)

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Gu, B., Zhang, B., Ding, L. et al. Physiological Change and Transcriptome Analysis of Chinese Wild Vitis amurensis and Vitis vinifera in Response to Cold Stress. Plant Mol Biol Rep 38, 478–490 (2020). https://doi.org/10.1007/s11105-020-01210-5

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Keywords

  • Vitis amurensis
  • Vitis vinifera
  • Cold resistance
  • Physiological change
  • RNA sequencing
  • Differentially expressed genes (DEGs)