Horticulture, Environment, and Biotechnology

, Volume 58, Issue 2, pp 152–161 | Cite as

Transcriptomic changes in dormant buds of two grapevine cultivars following exposure to freezing temperature

  • Seon Ae Kim
  • Soon Young Ahn
  • Hae Keun Yun
Research Report Genetics and Breeding


In this study, transcriptomes of buds from two grapevine (Vitis labruscana) cultivars, moderately cold-tolerant ‘Campbell Early’ and cold-susceptible ‘Muscat Baily A’, exposed to freezing temperatures were analyzed to identify genes involved in cold hardiness. Selected differentially expressed genes (DEGs) were evaluated for their expression patterns and transcripts obtained from next generation sequencing were analyzed for their gene ontologies. We assembled ~100 million high-quality trimmed reads, and the functional categorization of transcripts induced by freezing revealed the differential regulation of genes involved in cellular processes, metabolic processes, and cellular metabolic process in ‘Campbell Early’ and ‘Muscat Baily A’ grapes. The most upregulated genes in ‘Campbell Early’ included those encoding a chalcone and stilbene synthase family protein, a RmlC-like cupin superfamily protein, a homolog of carrot EP3-3 chitinase, and a cytochrome P450. The most downregulated genes in the cold-sensitive ‘Muscat Baily A’ included those encoding a 17.6 kDa class II heat shock protein, a HXXXD-type acyl-transferase family protein, and GIBBERELLIN 2-OXIDASE 8. All major DEGs identified by the transcriptomic analysis were confirmed to be differentially expressed using real-time PCR. A protein domain analysis using UniprotKB revealed that non-specific serine/threonine protein kinase, nitrilase and cyanoalanine nitrilase were upregulated in both grapevine cultivars. The transcriptome profile of dormant buds exposed to freezing can provide valuable molecular information about the tolerance of grapevines to extremely low temperatures during winter.

Additional key words

Cold tolerant DEG RNA-Seq Transcriptomics Vitis labruscana 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Literature Cited

  1. Ahn SY, Kim SH, Choi SJ, Yun HK (2012) Characteristics of cold hardiness and growth in grapevines grown in rain shelter type cultivation system in the vineyard. Korean J Hortic Sci Technol 30:626–634CrossRefGoogle Scholar
  2. Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11:R106CrossRefPubMedPubMedCentralGoogle Scholar
  3. Boutte J, Aliaga B, Lima O, Carvalho JF, Ainouche A, Macas J, Rousseau-Gueutin M, Cortion O, Ainouche M, Salmon A (2016) Haplotype detection from next-generation sequencing in high-ploidylevel species: 45S rDNA gene copies in the hexaploid Spartina maritima. G3-Genes Genom Genet 6:29–40Google Scholar
  4. Budak H, Khan Z, Kantar M (2015) History and current status of wheat miRNAs using next-generation sequencing and their roles in development and stress. Brief Funct Genomics 14:189–198CrossRefPubMedGoogle Scholar
  5. Cansev A, Gulen H, Eris A (2011) The activities of catalase and ascorbate peroxidase in olive (Olea europaea L. cv. Gemilk) under low temperature stress. Hortic Envrion Biotechnol 52:113–120CrossRefGoogle Scholar
  6. Carvallo MA, Pino MT, Jeknic Z, Zou C, Doherty CJ, Shiu SH, Chen THH, Thomashow MF (2011) A comparison of the low temperature transcriptomes and CBF regulons of three plant species that differ in freezing tolerance: Solanum commersonii, Solanum tuberosum, and Arabidopsis thaliana. J Exp Bot 62:3807–3819CrossRefPubMedPubMedCentralGoogle Scholar
  7. Chen S, Huang X, Yan X, Liang Y, Wang Y, Li X, Peng X, Ma X, Zhang L, et al (2013) Transcriptome analysis in sheepgrass (Leymus chinensis): a dominant perennial grass of the eurasian steppe. PLoS ONE 8(7):e67974CrossRefPubMedPubMedCentralGoogle Scholar
  8. Chenk PW, Snaar-Jagalska BE (1999) Signal perception and transduction: the role of protein kinases. Biochim Biophys Acta 1449:1–24CrossRefGoogle Scholar
  9. Christie PJ, Alfenito MR, Walbot V (1994) Impact of low-temperature stress on general phenylpropanoid and anthocyanin pathways: enhancement of transcript abundance and anthocyanin pigmentation in maize seedlings. Planta 194:541–549CrossRefGoogle Scholar
  10. Ferreira PG (1991) The Arabidopsis functional homolog of the P34cdc2 protein kinase. Plant Cell 3:531–540PubMedPubMedCentralGoogle Scholar
  11. Fritech L, Fischer R, Wambach C, Dudek M, Schillberg S, Schroper F (2015) Next-generation sequencing is a robust strategy for the high-throughput detection of zygosity in transgenic maize. Transgenic Res 24:615–623CrossRefGoogle Scholar
  12. Fuchigami LH, Weiser CJ, Kobayashi K, Timmis R, Gusta LV (1982) A degree growth stage (°GS) model and cold acclimation in temperate woody plants. In PH Li, A Sakai, eds, Plant Cold and Freezing Stress. Academic Press, New York, USA, pp 93–116CrossRefGoogle Scholar
  13. Gong Z, Lee H, Xiong L, Jagendorf A, Stevenson B, Zhu JK (2002) RNA helicase-like protein as an early regulator of transcription factors for plant chilling and freezing tolerance. Proc Natl Acad Sci USA 99:11507–11512CrossRefPubMedPubMedCentralGoogle Scholar
  14. Guy CL (1990) Cold acclimation and freezing stress tolerance: role of protein metabolism. Annu Rev Plant Physiol Plant Mo1 Biol 41:187–223CrossRefGoogle Scholar
  15. Guy CL, Niemi KJ, Brambl R (1985) Altered gene expression during cold acclimation of spinach. Proc Natl Acad Sci USA 82:3673–3677CrossRefPubMedPubMedCentralGoogle Scholar
  16. Hemstad PR, Luby JJ (2000) Utilization of Vitis riparia for the development of new wine varieties with resistance to disease and extreme cold. Acta Hort 528:487–490CrossRefGoogle Scholar
  17. Howarth CJ, Ougham HJ (1993) Gene expression under temperature stress. New Phytol 125:1–26CrossRefGoogle Scholar
  18. Hu Y, Jiang L, Wang F, Yu D (2013) Jasmonate regulates the inducer of CBF expression-c-repeat binding factor/DRE binding factor1 cascade and freezing tolerance in Arabidopsis. Plant Cell 25:2907–2924CrossRefPubMedPubMedCentralGoogle Scholar
  19. Huang Y, Si Y, Dane F (2011) Impact of grafting on cold responsive gene expression in Satsuma mandarin (Citrus unshiu). Euphytica 177:25–32CrossRefGoogle Scholar
  20. Hughes MA, Dunn MA (1990) The effect of temperature on plant growth and development. Biotechnol Genet Eng Rev 8:161–187CrossRefGoogle Scholar
  21. Irving RM, Landphear FO (1967) Environtmental control of cold hardiness in woody plants. Plant Physiol 42:1191–1196CrossRefPubMedPubMedCentralGoogle Scholar
  22. Kaplan F, Kopka J, Sung DY, Zhao W, Popp M, Porat R, Guy CL (2007) Transcript and metabolite profiling during cold acclimation of Arabidopsis reveals an intricate relationship of cold-regulated gene expression with modifications in metabolite content. Plant J 50:967–981PubMedGoogle Scholar
  23. Kim SA, Ahn SY, Yun HK (2016) Transcriptome analysis of grapevine shoots exposed to chilling temperature for four weeks. Hortic Environ Biotechnol 57:161–172CrossRefGoogle Scholar
  24. Kim SH, Seo HH, Cho JG, Jeon SJ, Kwon YS, Jeong YR (2009) Studies on adaptability and influence evaluation for suitable zone in horticultural crop with temperature rising. Ann Res Rept RDA Agenda 5, pp 712–714Google Scholar
  25. Koussevitzky S, Suzuki N, Huntington S, Armijo L, Sha W, Cortes D, Shulaev X, Mittler R (2008) Ascorbate peroxidase 1 plays a key role in the response of Arabidopsis thaliana to stress combination. J Biol Chem 283:34197–34203CrossRefPubMedPubMedCentralGoogle Scholar
  26. Larionov A, Krause A, Miller W (2005) A standard curve based method for relative real time PCR data processing. BMC Bioinformatics. 6:62CrossRefPubMedPubMedCentralGoogle Scholar
  27. Lee BH, Park YS, Kwon YH, Han JH, Park HS (2015) Bud development and bud break characteristics in water cuttings of ‘Campbell Early’ grapevine during dormancy. Korean J Hortic Sci Technol 33:202–209CrossRefGoogle Scholar
  28. Lee SP, Chen THH (1993) Molecular biology of plant cold hardiness development. In PH Li, L Christersson, eds, Advances in Plant Cold Hardiness. CRC, Boca Raton, FL, USA, pp 1-29Google Scholar
  29. Luby JJ, Mansfield AK, Hemstad PR, Beam BA (2003) Development and evaluation of cold hardy wine grape breeding selections and cultivars in the upper Midwest. AVERN ReportGoogle Scholar
  30. Mathiason K, He D, Grimplet J, Venkateswari J, Galbraith DW, Or E, Fennell A (2009) Transcript profiling in Vitis riparia during chilling requirement fulfillment reveals coordination of gene expression patterns with optimized bud break. Funct Integr Genomics 9:81–96CrossRefPubMedGoogle Scholar
  31. Oono Y, Seki M, Satou M, Iida K, Akiyama K, Sakurai T, Fujita M, Yamaguchi-Shinozaki K, Shinozaki K (2006) Monitoring expression profiles of Arabidopsis genes during cold acclimation and deacclimation using DNA microarrays. Funct Integr Genomics 6:212–234CrossRefPubMedGoogle Scholar
  32. Pearce RS (2001) Plant freezing and damage. Ann Bot 87:417–424CrossRefGoogle Scholar
  33. Rudrabhatla P, Reddy MM, Rajasekharan R (2006) Genome-wide analysis and experimentation of plant serine/threonine/tyrosine-specific protein kinases. Plant Mol Biol 60:293–319CrossRefPubMedGoogle Scholar
  34. Saarinen T, Lundell R, Hanninen H (2011) Recovery of photosynthetic capacity in Vaccinium vitis-idaea during mild spells in winter. Plant Ecol 212:1429–1440CrossRefGoogle Scholar
  35. Sakai A, Larcher W (1987) Frost survival of plants: Responses and adaptation to freezing stress. Ecological studies, vol. 62. Springer, Berlin, pp 1–321Google Scholar
  36. Shim KM, Lee JT, Lee YS, Kim GY (2004) Reclassification of winter barley cultivation zones in Korea based on recent evidences in climate change. Korean J Agri Forest Meteorol 6:218–234.Google Scholar
  37. Sreekantan L, Mathiason K, Grimplet J, Schlauch K, Dicherson JA, Fennell AY (2010) Differential floral development and gene expression in grapevines during long and short photoperiods suggests a role for floral genes in dormancy transitioning. Plant Mol Biol 73:191–205CrossRefPubMedGoogle Scholar
  38. Stone JM, Walker JC (1995) Plant protein kinase families and signal transduction. Plant Physiol 108:451–457CrossRefPubMedPubMedCentralGoogle Scholar
  39. Strickler SR, Bombarely A, Muller LA (2012) Designing a transcriptome next-generation sequencing project for a nonmodel plant species. Am J Bot 99:257–266CrossRefPubMedGoogle Scholar
  40. Sun JH, Chen JY, Kuang JF, Chen WX, Lu WJ (2010) Expression of sHSP genes as affected by heat shock and cold acclimation in relation to chilling tolerance in plum fruit. Postharvest Biol Technol 55:91–96CrossRefGoogle Scholar
  41. Tattersall EAR, Grimplet J, DeLuc L, Whearley MD, Vincent D, Osborne C, Ergul A, Lomen E, Blank RR, Schlauch KA, Cushman JC, Cramer GR (2007) Transcript abundance profiles reveal larger and more complex responses of grapevine to chilling compared to osmotic and salinity stress. Funct Intergr Genomics 7:317–333CrossRefGoogle Scholar
  42. Thomashow MF (1990) Molecular genetics of cold acclimation in higher plants. In JG Scandalios, ed, Advances in genetics, genomic responses to environmental stress, vol 28. Academic Press, New York, pp 99–131CrossRefGoogle Scholar
  43. Thomashow MF (1993) Genes induced during cold acclimation in higher plants. In PL Steponkus, ed, Advances in low-temperature biology, vol 2. JAI, London, pp 183–210Google Scholar
  44. Thomashow MF (1998) Role of cold-responsive genes in plant freezing tolerance. Plant Physiol 118:1–7CrossRefPubMedPubMedCentralGoogle Scholar
  45. Wu J, Zhang Y, Zhang H, Huang H, Folta KM, Lu J (2010) Whole genome wide expression profiles of Vitis amurensis grape responding to downy mildew by using Solexa sequencing technology. BMC Plant Biol 10:234CrossRefPubMedPubMedCentralGoogle Scholar
  46. Yang G, Zhou R, Tang T, Shi S (2008) Simple and efficient isolation of high-quality total RNA from Hibiscus tiliaceus, a mangrove associate and its relatives. Prep Biochem Biotechnol 38:257–264CrossRefPubMedGoogle Scholar
  47. Zhu YN, Shi DQ, Ruan MB, Zhang LL, Meng ZH, Liu J, Yang WC (2013) Transcriptome analysis reveals crosstalk of responsive genes to multiple abiotic stresses in cotton (Gossypium hirsutum L.). PLoS ONE 8:11Google Scholar

Copyright information

© Korean Society for Horticultural Science and Springer-Verlag GmbH 2017

Authors and Affiliations

  1. 1.Department of Horticultural ScienceYeungnam UniversityGyeongsanKorea

Personalised recommendations