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A Novel U-Box Protein Gene from “Zuoshanyi” Grapevine (Vitis amurensis Rupr. cv.) Involved in Cold Responsive Gene Expression in Arabidopsis thanliana

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Abstract

Ubiquitination plays an important role in posttranscriptional modification of proteins. As a component of the ubiquitin conjugation system, E3 ligase is believed to be a key element determining the substrate specificity of ubiquitination. In this research, a novel putative U-box type E3 ligase VaPUB (plant U-box protein) was isolated from a very cold-hardy “Zuoshanyi” (Vitis amurensis Rupr. cv.) grapevine. Real-time PCR demonstrated that PUB was upregulated by cold stress and expressed more strongly in cold-tolerant grapevines than in cold-sensitive grapevines. In cold-hardy V. amurensis Zuoshanyi grapevine, the expression of PUB was upregulated by cold in all tissues, although more dramatic increases were found in the leaves and shoot tips than in the roots or stems. Over-expression of VaPUB in Arabidopsis resulted in an enhancement of cold and salt stress tolerance. The transcription factors, CBF1/DREB1B and CBF3/DREB1A, and cold inducing genes, COR15A, COR47, KIN1, RD29A, and SuSy, were expressed in a higher level in VaPUB transgenic plants than the wild type. In contrast, the expression of transcription factor CBF2/DREB1C was repressed by VaPUB. These results demonstrated that VaPUB enhanced plant cold and salt stress tolerance and its over-expression affected the expression of cold responsive genes.

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References

  • Agarwal M, Hao Y, Kapoor A, Dong CH, Fujii H et al (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

    Article  CAS  PubMed  Google Scholar 

  • Aravind L, Koonin EV (2000) The U-box is a modified RING finger: a common domain in ubiquitination. Curr Biol 10:R132–R134

    Article  CAS  PubMed  Google Scholar 

  • Banzai T, Hershkovits G, Katcoff DJ, Hanagata N, Dubinsky Z et al (2002) Identification and characterization of mRNA transcripts differentially expressed in response to high salinity by means of differential display in the mangrove, Bruguiera gymnorrhiza. Plant Sci 162:499–505

    Article  CAS  Google Scholar 

  • Bieniawska Z, Barratt DHP, Garlick AP, Thole V, Kruger NJ et al (2007) Analysis of the sucrose synthase gene family in Arabidopsis. Plant J 49:810–828

    Article  CAS  PubMed  Google Scholar 

  • Bray EA (1997) Plant responses to water deficit. Trends Plant Sci 2:48–54

    Article  Google Scholar 

  • Catala R, Salinas J (2008) Regulatory mechanisms involved in cold acclimation response: a review. Span J Agric Res 6:211–220

    Article  Google Scholar 

  • Catala R, Ouyang J, Abreu IA, Hu YX, Seo H et al (2007) The Arabidopsis E3 SUMO ligase SIZ1 regulates plant growth and drought responses. Plant Cell 19:2952–2966

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chinnusamy V, Ohta M, Kanrar S, Lee BH, Hong XH et al (2003) ICE1: A regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genes Dev 17:1043–1054

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chinnusamy V, Zhu J, Zhu J-K (2006) Gene regulation during cold acclimation in plants. Physiol Plant 126:52–61

    Article  CAS  Google Scholar 

  • Cho SK, Ryu MY, Song C, Kwak JM, Kim WT (2008) Arabidopsis PUB22 and PUB23 are homologous U-box E3 ubiquitin ligases that play combinatory roles in response to drought stress. Plant Cell 20:1899–1914

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  CAS  PubMed  Google Scholar 

  • Dong C-H, Agarwal M, Zhang Y, Xie Q, Zhu J-K (2006) The negative regulator of plant cold responses, HOS1, is a RING E3 ligase that mediates the ubiquitination and degradation of ICE1. Proc Natl Acad Sci U S A 103:8281–8286

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dreher K, Callis J (2007) Ubiquitin, hormones and biotic stress in plants. Ann Bot 99:787–822

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dubouzet JG, Sakuma Y, Ito Y, Kasuga M, Dubouzet E et al (2003) OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high- salt- and cold-responsive gene expression. Plant J 33:751–763

    Article  CAS  PubMed  Google Scholar 

  • Gilmour SJ, Sebolt AM, Salazar MP, Everard JD, Thomashow MF (2000) Overexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation. Plant Physiol 124:1854–1865

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499

    Article  CAS  PubMed  Google Scholar 

  • Hatakeyama S, Yada M, Matsumoto M, Ishida N, Nakayama KI (2001) U-box proteins as a new family of ubiquitin–protein ligases. J Biol Chem 276:33111–33120

    Article  CAS  PubMed  Google Scholar 

  • Hicke L, Dunn R (2003) Transport by ubiquitin and ubiquitin-binding proteins. Annu Rev Cell Dev Biol 19:141–172

    Article  CAS  PubMed  Google Scholar 

  • Huang L, Kinnucan E, Wang G, Beaudenon S, Howley PM et al (1999) Structure of an E6AP-UbcH7 complex: insights into ubiquitination by the E2-E3 ligase cascade. Science 286:1321–1326

    Article  CAS  PubMed  Google Scholar 

  • Ingram J, Bartels D (1996) The molecular basis of dehydration tolerance in plants. Annu Rev Plant Physiol Plant Mol Biol 47:377–403

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Kasuga M, Miura S, Shinozaki K, Yamaguchi-Shinozaki K (1999) Improving plant drought, salt and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat Biotechnol 17:287–291

    Article  CAS  PubMed  Google Scholar 

  • Lee H, Xiong L, Gong Z, Ishitani M, Stevenson B, Zhu JK (2001) The ArabidopsisHOS1 gene negatively regulates cold signal transduction and encodes a RING finger protein that displays cold-regulated nucleo-cytoplasmic partitioning. Genes Dev 15:912–924

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 Rep 31:1518–1528

    Article  CAS  Google Scholar 

  • Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S et al (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA-binding domain separate two cellular signal transduction pathways in drought and low-temperature-responsive gene expression respectively in Arabidopsis. Plant Cell 10:1391–1406

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:4402–4408

    Article  Google Scholar 

  • Luo J, Shen G, Yan J, He C, Zhang H (2006) AtCHIP functions as an E3 ubiquitin ligase of protein phosphatase 2A subunits and alters plant response to abscisic acid treatment. Plant J 46:649–657

    Article  CAS  PubMed  Google Scholar 

  • Ma YY, Zhang YL, Shao H, 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 196:212–219

    Article  CAS  Google Scholar 

  • Mano Y, Nakazumi H, Takeda K (1996) Varietal variation in and effects of some major genes on salt tolerance at the germination stage in barley. Breeding Sci 46:227–233

    Google Scholar 

  • Miura K, Jin JB, Lee J, Yoo CY, Stirm V et al (2007) SIZ1-mediated sumoylation of ICE1 controls CBF3/DREB1A expression and freezing tolerance in Arabidopsis. Plant Cell 19:1403–1414

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Novillo F, Alonso JM, Ecker JR, Salinas J (2004) CBF2/DREB1C is a negative regulator of CBF1/DREB1B and CBF3/DREB1A expression and plays a central role in stress tolerance in Arabidopsis. Proc Natl Acad Sci U S A 101:3985–3990

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Samuel MA, Salt JN, Shiu SH, Goring DR (2006) Multifunctional arm repeat domains in plants. Int Rev Cytol 253:1–26

    Article  CAS  PubMed  Google Scholar 

  • Schnell JD, Hicke L (2003) Non-traditional functions of ubiquitin and ubiquitin-binding proteins. J Biol Chem 278:35857–35860

    Article  CAS  PubMed  Google Scholar 

  • Shan X, Li Y, Jiang Y, Jiang Z, Hao W (2013) Transcriptome profile analysis of maize seedlings in response to high-salinity, drought and cold stresses by deep sequencing. Plant Mol Biol Rep 31:1485–1491

    Article  CAS  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58:221–227

    Article  CAS  PubMed  Google Scholar 

  • Smalle J, Vierstra RD (2004) The ubiquitin 26S proteasome proteolytic pathway. Annu Rev Plant Biol 55:55–90

    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 U S A 94:1035–1040

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Stone SL, Callis J (2007) Ubiquitin ligases mediate growth and development by promoting protein death. Curr Opin Plant Biol 10:624–632

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Ueki S, Lacroix B, Krichevsky A, Lazarowitz SG, Citovsky V (2009) Functional transient genetic transformation of Arabidopsis leaves by biolistic bombardment. Nat Protoc 4:71–77

    Article  CAS  PubMed  Google Scholar 

  • Vogel JT, Zarka DG, Van Buskirk HA, Fowler SG, Thomashow MF (2005) Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis. Plant J 41:195–211

    Article  CAS  PubMed  Google Scholar 

  • Wu J, Zhang Y, Wu N, Zhang H, Jiao L et al (2012) Identification and expression analysis of cold-regulated genes in Vitis amurensis Rupr. cv. Zuoshan-1. J Hortic Sci Biotech 87:557–564

    Google Scholar 

  • Xiao HG, 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  PubMed  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (1994) A novel cis acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature or high-salt stress. Plant Cell 6:251–264

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yan JQ, Wang J, Li QT, Hwang JR, Patterson C et al (2003) AtCHIP, a U-box-containing E3 ubiquitin ligase, plays a critical role in temperature stress tolerance in Arabidopsis. Plant Physiol 132:861–869

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yang C, Li A, Zhao Y, Zhang Z, Zhu Y et al (2011) Overexpression of a wheat CCaMK gene reduces ABA sensitivity of Arabidopsis thaliana during seed germination and seedling growth. Plant Mol Biol Rep 29:681–692

    Article  CAS  Google Scholar 

  • Yee D, Goring DR (2009) The diversity of plant U-box E3 ubiquitin ligases: from upstream activators to downstream target substrates. J Exp Bot 60:1109–1121

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Yang C, Li Y, Zheng N, Chen H et al (2007) SDIR1 is a RING finger E3 ligase that positively regulates stress-responsive abscisic acid signaling in Arabidopsis. Plant Cell 19:1912–1929

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhu J, Shi H, Lee B-H, Damsz B, Cheng S et al (2004) An Arabidopsis homeodomain transcription factor gene, HOS9, mediates cold tolerance through a CBF-independent pathway. Proc Natl Acad Sci U S A 101:9873–9878

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhu J, Verslues PE, Zheng X, Lee B, Zhan X et al (2005) HOS10 encodes an R2R3-type MYB transcription factor essential for cold acclimation in plants. PNAS 102:9966–9971

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by the Chinese Universities Scientific Fund (Grant No. 2012RC019) and earmarked fund for Chinese Agricultural Research System (CARS-30-yz-2).

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Authors and Affiliations

  1. The Viticulture and Enology Program, College of Food Science and Nutritional Engineering, China Agricultural University, Beijing, 100083, China

    Li Jiao, Yali Zhang, Jiao Wu, Huiqin Zhang & Jiang Lu

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  1. Li Jiao
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Correspondence to Jiang Lu.

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Supplementary Fig. 1

Sequence alignment of PUB between V. amurensis ‘Zuoshanyi’ and V. quinquangularis ‘Maoputao’. The U-box domain is indicated by a solid line. Sequences conserved in these two cultivars are shown in black (GIF 60.8 kb)

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Jiao, L., Zhang, Y., Wu, J. et al. A Novel U-Box Protein Gene from “Zuoshanyi” Grapevine (Vitis amurensis Rupr. cv.) Involved in Cold Responsive Gene Expression in Arabidopsis thanliana . Plant Mol Biol Rep 33, 557–568 (2015). https://doi.org/10.1007/s11105-014-0783-4

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