Advertisement

Horticulture, Environment, and Biotechnology

, Volume 57, Issue 2, pp 161–172 | Cite as

Transcriptome analysis of grapevine shoots exposed to chilling temperature for four weeks

  • Seon Ae Kim
  • Soon Young Ahn
  • Hae Keun YunEmail author
Research Report

Abstract

Low temperature is an important factor that can limit the growth of grapevine (Vitis spp.). In this study, we analyzed the transcriptome of grapevine shoots exposed to cold temperatures to identify genes expressed specifically at low temperature, determine their function based on GO-term analysis, and compare their differential expression. We analyzed two varieties that differed in cold tolerance, the more-tolerant ‘Campbell Early’ and the less-tolerant ‘Kyoho’ grapevine varieties. This was accomplished through annotation of data from sequencing short reads on the Solexa platform. We assembled more than 120 million high-quality trimmed reads using Velvet followed by Oases. Functional categorization of up-regulated transcripts revealed the conservation of genes involved in various biological processes including cellular processes, primary metabolic processes, and biological regulation. The major up-regulated genes in ‘Campbell Early’ included loci encoding response regulator 20, expansin-like B1, a leucine-rich repeat (LRR) family protein, and galactinol synthase 2. The major down-regulated genes in ‘Campbell Early’ included loci encoding fasciclinlike arabinogalactan 9, a GDSL-like lipase/acylhydrolase superfamily protein, early nodulin-like protein 14, and trichome birefringence-like 38. The differential expression observed by sequence analysis was confirmed by real-time PCR. Genes encoding a non-specific serine/threonine protein kinase, peroxidase, and ubiquitin-protein ligase showed reduced expression in response to low temperature in both grapevine varieties. Transcriptome analysis of shoots exposed to chilling could lead to new insights into the molecular basis of tolerance to low-temperature in grapevine.

Additional key words

differential gene expression functional categorization short read sequencing transcript 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Literature Cited

  1. Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11:R106CrossRefPubMedPubMedCentralGoogle Scholar
  2. Arora R, Agarwal P, Ray S, Singh AK, Singh VP, Tyagi AK, Kapoor S (2007) MADA-box gene family in rice: Genome-wide identification, organization and expression profiling during reproductive development and stress. BMC Genomics 8:242CrossRefPubMedPubMedCentralGoogle Scholar
  3. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, et al (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25:25–29PubMedGoogle Scholar
  4. Barka EA, Nowak J, Clement C (2006) Enhancement of chilling resistance of inoculated grapevine plantlets with a plant growthpromoting rhizobacterium, Burkholderia phytofirmans Strain PsJN. Appl Environ Microbiol 72:7246–7255CrossRefGoogle Scholar
  5. Buttrose MS (1969) Vegetative growth of grapevine varieties under controlled temperature and light intensity. Vitis 8:280–285Google Scholar
  6. Chang S, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol 11:113–116CrossRefGoogle Scholar
  7. Cook D, Fowler S, Fiehn O, Thomashow MF (2004) A prominent role for the CBF cold response pathway in configuring the low temperature metabolome of Arabidopsis. Proc Natl Acad Sci USA 101:15243–15248CrossRefPubMedPubMedCentralGoogle Scholar
  8. Cox MP, Peterson DA, Biggs PJ (2010) SolexaQA: At-a-glance quality assessment of Illumina second-generation sequencing data. BMC Bioinformatics 11:485CrossRefPubMedPubMedCentralGoogle Scholar
  9. 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 14:1675–1690CrossRefPubMedPubMedCentralGoogle Scholar
  10. Fuller MP, Telli G (1999) An investigation of the frost hardiness of grapevine (Vitis vinifera) during bud break. Ann Appl Biol 135:589–595CrossRefGoogle Scholar
  11. Hannah MA, Wiese D, Freund S, Fiehn O, Heyer AG, Hincha DK (2006) Natural genetic variation of freezing tolerance in Arabidopsis. Plant Physiol 142:98–112CrossRefPubMedPubMedCentralGoogle Scholar
  12. Harding HP, Zhang Y, Zeng H, Novoa I, Lu PD, Calfon M, Sadri N, Yun C, Popko B, Paules R, et al (2003) An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol Cell 11:619–633CrossRefPubMedGoogle Scholar
  13. Hemstad PR, Luby JJ (2000) Utilization of Vitis riparia for the development of new wine varieties with resistance to disease and extreme cold. Acta Hortic 528:487–490CrossRefGoogle Scholar
  14. Hewezi T, Leger M, Kayal WE, Gentzbittel L (2006) Transcriptional profiling of sunflower plants growing under low temperatures reveals an extensive down-regulation of gene expression associated with chilling sensitivity. J Exp Bot 57:3109–3122CrossRefPubMedGoogle Scholar
  15. Horák J, Grefen C, Berendzen KW, Hahn A, Stierhof YD, Stadelhofer B, Stahl M, Koncz C, Harter K (2008) The Arabidopsis thaliana response regulator ARR22 is a putative AHP phospho-histidine phosphatase expressed in the chalaza of developing seeds. BMC Plant Biol 8:77CrossRefPubMedPubMedCentralGoogle Scholar
  16. Huang W, Li L, Myers JR, Marth GT (2012) ART: A next-generation sequencing read simulator. Bioinformatics 28:593–594CrossRefPubMedPubMedCentralGoogle Scholar
  17. Huang DW, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4:44–57CrossRefGoogle Scholar
  18. Jeon J, Kim J (2013) Arabidopsis response regulator1 and Arabidopsis histidine phosphotransfer protein2 (AHP2), AHP3, and AHP5 function in cold signaling. Plant Physiol 161:408–424CrossRefPubMedPubMedCentralGoogle Scholar
  19. Jeon J, Kim NY, Kim S, Kang NY, Novák O, Ku SJ, Cho C, Lee DJ, Lee EJ, Strnad M, et al (2010) A subset of cytokinin two-component signaling system plays a role in cold temperature stress response in Arabidopsis. J Biol Chem 285:23371–23386CrossRefPubMedPubMedCentralGoogle Scholar
  20. Kacperska A (1989). Metabolic consequences of low temperature stress in chilling-insensitive plants. In PH Li, ed, Low Temperature Stress Physiology in Crops, CRC Press, Boca Raton, FL, pp 27–40Google Scholar
  21. Kanehisa M, Goto S, Kawashima S, Okuno Y, Hattori M (2004) The KEGG resource for deciphering the genome. Nucleic Acids Res 32:D277–280CrossRefPubMedPubMedCentralGoogle 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 50:967–981CrossRefPubMedGoogle Scholar
  23. Kim SA, Ahn SY, Han JH, Kim SH, Noh JH, Yun HK (2013) Differential expression screening of defense related genes in dormant buds of cold-treated grapevines. Plant Breed Biotechnol 1:14–23CrossRefGoogle Scholar
  24. Kotak S, Larkindale J, Lee U, von Koskull-Doring P, Vierling E, Scharf KD (2007) Complexity of the heat stress response in plants. Curr Opin Plant Biol 10:310–316CrossRefPubMedGoogle Scholar
  25. Larkindale J, Hall JD, Knight MR, Vierling E (2005) Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance. Plant Physiol 138:882–888CrossRefPubMedPubMedCentralGoogle Scholar
  26. Lee BH, Henderson DA, Zhu JK (2005) The Arabidopsis coldresponsive transcriptome and its regulation by ICE1. Plant Cell 17:3155–3175CrossRefPubMedPubMedCentralGoogle Scholar
  27. Liu JX, Srivastava R, Che P, Howell SH (2007) Salt stress responses in Arabidopsis utilize a signal transduction pathway related to endoplasmic reticulum stress signaling. Plant J 51:897–909CrossRefPubMedPubMedCentralGoogle Scholar
  28. Liu X, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought-and lowtemperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10:1391–1406CrossRefPubMedPubMedCentralGoogle Scholar
  29. Lohrmann J, Harter K (2002) Plant two-component signaling systems and the role of response regulators. Plant Physiol 128:363–369CrossRefPubMedPubMedCentralGoogle Scholar
  30. 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
  31. Lv DK, Bai X, Li Y, Ding XD, Ge Y, Cai H, Ji W, Wu N, Zue YM (2010) Profiling of cold-stress-responsive miRNA in rice by microarrays. Gene 459:39–47CrossRefPubMedGoogle Scholar
  32. Lynch DV (1990) Chilling injury in plants: the relevance of membrane lipids. In F Katterman, ed, Environmental Injury to Plants, Academic press, New York, pp 17–34Google Scholar
  33. Ma YY, Zhang YL, Lu J (2010) Differential physio-biochemical responses to cold stress of cold-tolerant and non-tolerant grapes (Vitis L.) from China. J Agron Crop Sci 196:212–219CrossRefGoogle Scholar
  34. Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158CrossRefPubMedGoogle Scholar
  35. Mason MG, Mathews DE, Argyros DA, Maxwell BB, Kieber JJ, Alonso JM, Ecker JR, Schaller GE (2005) Multiple type-B response regulators mediate cytokinin signal transduction in Arabidopsis. Plant Cell 17:3007–3018CrossRefPubMedPubMedCentralGoogle Scholar
  36. 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
  37. Motosugi H (2000) Growth comparison between own-rooted of Portland, Niagara, and Campbell Early vines and their tetraploid sports. J ASEV Jpn 11:8–14Google Scholar
  38. Nam JC, Park SJ, Jeong SM, Noh JH, Hur YY, Park KS (2012) Threshold of winter injury according to low temperature in dormancy and growing stage in several grape (Vitis hybrid) cultivars. Korean J Hortic Sci Technol 30:100–101Google Scholar
  39. Oono Y, Seki M, Satoum 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 microaarays. Funct Integr Genomics 6:212–234CrossRefPubMedGoogle Scholar
  40. Park GH, Lim JW, E GJ (2000) Management of chilling injury in grapevine shoots in unheated plastic house in Korea. 2000 Research Report. Kyunggi-do Agricultural Research and Extension Services, Korea, pp 388–397Google Scholar
  41. Pontin MA, Piccoli PN, Francisco R, Botini R, Martinez-Zapater JM, Lijavetzky (2010) Transcriptome changes in grapevines (Vitis vinifera L.) cv. Malbec leaves induced by ultraviolet-B radiation. BMC Plant Biol 21:224CrossRefGoogle Scholar
  42. Ramamoorthy R, Jiang SY, Kumar N, Venkatesh PN, Ramachandran S (2008) A comprehensive transcriptional profiling of the WRKY gene family in rice under various abiotic and phytohormone treatments. Plant Cell Physiol 49:865–879CrossRefPubMedGoogle Scholar
  43. Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T, et al (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 31:279–292CrossRefPubMedGoogle Scholar
  44. Stitt M, Hurry V (2002) A plant for all seasons: alterations in photosynthetic carbon metabolism during cold acclimation in Arabidopsis. Curr Opin Plant Biol 5:199–206CrossRefPubMedGoogle Scholar
  45. Sweetman C, Wong DC, Ford CM, Drew DP (2012) Transcriptome analysis at four developmental stages of grape berry (Vitis vinifera cv. Shiraz) provides insights into regulated and coordinated gene expression. BMC Genomics 13:691PubMedGoogle Scholar
  46. Tattersall EAR, Grimplet J, DeLuc L, Whearley MD, Vincent D, Osborne C, Ergul A, Lomen E, Blank RR, Schlauch KA, et al (2007) Transcript abundance profiles reveal larger and more complex responses of grapevine to chilling compared to osmotic and salinity stress. Funct Integr Genomics 7:317–333CrossRefPubMedGoogle Scholar
  47. Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol 50: 571–599CrossRefGoogle Scholar
  48. Walker MA, McKersie BD, Pauls KP (1991) Effects of chilling on the biochemical and functional properties of thylakoid membranes. Plant Physiol 97:663–669CrossRefPubMedPubMedCentralGoogle Scholar
  49. Wang J, Yang Y, Liu X, Huang J, Wang Q, Gu J, Lu Y (2014) Transcriptome profiling of the cold response and signaling pathways in Lilium lancifolium. BMC Genomics 15:203CrossRefPubMedPubMedCentralGoogle Scholar
  50. Wang H, Liu D, SunJ, Zhang A (2005) Asparagine synthetase gene TaASN1 from wheat is up-regulated by salt stress, osmotic stress and ABA. J Plant Physiol 162:81–89CrossRefPubMedGoogle Scholar
  51. Wang XC, Zhao QY, Ma CL, Zhang ZH, Cao HL, Kong YM, Yue C, Hao XY, Chen L, Ma JQ, et al (2013) Global transcriptome profiles of Camellia sinensis during cold acclimation. BMC Genomics 14:415CrossRefPubMedPubMedCentralGoogle Scholar
  52. Warmund MR, Guinan P, Fernandez G (2008) Temperatures and cold damage to small fruit crops across the Eastern United States associated with the April 2007 freeze. Hortic Sci 43:1643–1647Google Scholar
  53. White MA, Diffenbaugh NS, Jones GV, Pal JS, Giorgi F (2006) Extreme heat reduces and shifts United States premium wine production in the 21st century. Proc Natl Acad Sci USA 103: 11217–11222CrossRefPubMedPubMedCentralGoogle Scholar
  54. 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 10:234–249CrossRefPubMedPubMedCentralGoogle Scholar
  55. 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 8:3Google Scholar
  56. Xu J (2014) Next-generation sequencing: Current Technologies and Applications. Caister Academic Press, Ontario, CanadaGoogle Scholar
  57. Yamauchi Y, OgawaM, Kuwahara A, Hanada A, Kamiya Y, Yamaguchi S (2004) Activation of gibberellin biosynthesis and response pathways by low temperature during imbibition of Arabidopsis thaliana seeds. Plant Cell 16:367–378CrossRefPubMedPubMedCentralGoogle Scholar
  58. Zhu J, Dong CH, Zhu JK (2007) Interplay between cold-responsive gene regulation, metabolism and RNA processing during plant cold acclimation. Curr Opin Plant Biol 10:290–295CrossRefPubMedGoogle Scholar
  59. Zhu T, Provart NJ (2003) Transcriptional responses to low temperature and their regulation in Arabidopsis. Can J Bot 81:1168–1174CrossRefGoogle Scholar
  60. Zononi 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 152:1787–1795CrossRefGoogle Scholar

Copyright information

© Korean Society for Horticultural Science and Springer-Verlag GmbH 2016

Authors and Affiliations

  1. 1.Department of Horticulture and Life ScienceYeungnam UniversityGyeongsanKorea

Personalised recommendations