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Genome-wide Classification, Identification and Expression Profile of the C3HC4-type RING Finger Gene Family in Poplar (Populus trichocarpa)

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Abstract

C3HC4-type RING finger genes belong to a large gene family in plants and play crucial roles in diverse stress responses. In this study, a comprehensive analysis of the poplar (Populus trichocarpa) C3HC4-type RING finger gene family was performed, including analysis of phylogenetic relationships, chromosomal locations, gene structures, motif compositions, possible cis-elements, and expression profiles. Ninety-one poplar C3HC4-type RING finger genes were identified, which were clustered phylogenetically into seven distinct subfamilies and distributed predominantly across 17 linkage groups. Motif analysis revealed the presence of 15 conserved motifs with unknown functions within the predicted proteins. Promoter cis-element analysis indicated that most of the C3HC4-type RING finger genes contained abiotic stress-related cis-elements. Further, expression profiling showed that a number of genes were expressed differentially across disparate tissues and under various stresses, such as wood formation and drought. Additionally, quantitative real-time RT-PCR was performed on 24 selected C3HC4-type RING finger genes to confirm their responses to drought stress treatment. We found that PtrRHC7, 20 and 70 were not only abundantly transcribed in leaves, but also were upregulated in roots under drought stress. These results represent the foundation for further investigation of the roles of these candidate genes and for future genetic engineering and gene functional studies in Populus.

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References

  • Anderson PK, Cunningham AA, Patel NG, Morales FJ, Epstein PR, Daszak P (2004) Emerging infectious diseases of plants: pathogen pollution, climate change and agrotechnology drivers. Trends Ecol Evol 19:535–544

    Article  PubMed  Google Scholar 

  • Andersson-Gunnerås S, Mellerowicz EJ, Love J, Segerman B, Ohmiya Y, Coutinho PM, Nilsson P, Henrissat B, Moritz T, Sundberg B (2006) Biosynthesis of cellulose-enriched tension wood in Populus: global analysis of transcripts and metabolites identifies biochemical and developmental regulators in secondary wall biosynthesis. Plant J 45:144–165

    Article  PubMed  CAS  Google Scholar 

  • Bailey TL, Williams N, Misleh C, Li WW (2006) MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res 34(suppl 2):W369–W373

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Barakat A, Bagniewska-Zadworna A, Choi A, Plakkat U, DiLoreto DS, Yellanki P, Carlson JE (2009) The cinnamyl alcohol dehydrogenase gene family in Populus: phylogeny, organization, and expression. BMC Plant Biol 9:26

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Berg JM, Shi Y (1996) The galvanization of biology: a growing appreciation for the roles of zinc. Science 271:1081–1085

    Article  PubMed  CAS  Google Scholar 

  • Borden KL, Freemont PS (1996) The RING finger domain: a recent example of a sequence-structure family. Curr Opin Struc Biol 6:395–401

    Article  CAS  Google Scholar 

  • Brochu V, Girard-Martel M, Duval I, Lerat S, Grondin G, Domingue O, Beaulieu C, Beaudoin N (2010) Habituation to thaxtomin A in hybrid poplar cell suspensions provides enhanced and durable resistance to inhibitors of cellulose synthesis. BMC Plant Biol 10:272

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Callis J, Vierstra RD (2000) Protein degradation in signaling. Curr Opin Plant Biol 3(5):381–386

    Article  PubMed  CAS  Google Scholar 

  • Chai GH, Hu RB, Zhang DY, Qi G, Zuo R, Cao YP, Chen P, Kong YZ, Zhou GK (2012) Comprehensive analysis of CCCH zinc finger family in poplar (Populus trichocarpa). BMC Genomics 13:253

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chang S, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Rep 11:113–116

    Article  CAS  Google Scholar 

  • Cheung MY, Zeng NY, Tong SW, Li FWY, Zhao KJ, Zhang Q, Sun SSM, Lam HM (2007) Expression of a RING-HC protein from rice improves resistance to Pseudomonas syringae pv. tomato DC3000 in transgenic Arabidopsis thaliana. J Exp Bot 58:4147–4159

    Article  PubMed  CAS  Google Scholar 

  • Cho SK, Ryu MY, Seo DH, Kang BG, Kim WT (2011) The Arabidopsis RING E3 ubiquitin ligase AtAIRP2 plays combinatory roles with AtAIRP1 in abscisic acid-mediated drought stress responses. Plant Physiol 157:2240–2257

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Díaz-Martín J, Almoguera C, Prieto-Dapena P, Espinosa JM, Jordano J (2005) Functional interaction between two transcription factors involved in the developmental regulation of a small heat stress protein gene promoter. Plant Physiol 139:1483–1494

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Finn RD, Mistry J, Tate J, Coggill P, Heger A, Pollington JE, Gavin OL, Gunasekaran P, Ceric G, Forslund K et al (2010) The Pfam protein families database. Nucleic Acids Res 38:D211–D222

  • Gasteiger E, Hoogland C, Gattiker A, Wilkins MR, Appel RD, Bairoch A (2005) Protein identification and analysis tools on the ExPASy server. In: John MW (ed) The proteomics protocols handbook. Humana, New York, pp 571–607

    Chapter  Google Scholar 

  • Guo AY, Zhu QH, Chen X, Luo JC (2007) GSDS: a gene structure display server. Yi Chuan 29:1023–1026

    Article  PubMed  CAS  Google Scholar 

  • Guo YH, Yu YP, Wang D, Wu CA, Yang GD, Huang JG, Zheng CC (2009) GhZFP1, a novel CCCH-type zinc finger protein from cotton, enhances salt stress tolerance and fungal disease resistance in transgenic tobacco by interacting with GZIRD21A and GZIPR5. New Phytol 183:62–75

    Article  PubMed  CAS  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hardtke CS, Okamoto H, Stoop-Myer C, Deng XW (2002) Biochemical evidence for ubiquitin ligase activity of the Arabidopsis COP1 interacting protein 8 (CIP8). Plant J 30:385–394

    Article  PubMed  CAS  Google Scholar 

  • Hellgren JM, Olofsson K, Sundberg B (2004) Patterns of auxin distribution during gravitational induction of reaction wood in poplar and pine. Plant Physiol 135:212–220

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Horton P, Park KJ, Obayashi T, Fujita N, Harada H, Adams-Collier CJ, Nakai K (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res 35(suppl 2):W585–W587

    Article  PubMed  PubMed Central  Google Scholar 

  • Hu RB, Chi XY, Chai GH, Kong YZ, He G, Wang XY, Shi DH, Zhang DY, Zhou GK (2012) Genome-wide identification, evolutionary expansion, and expression profile of homeodomain-leucine zipper gene family in poplar (Populus trichocarpa). PLoS One 7:e31149

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kim JH, Kim WT (2013) The Arabidopsis RING E3 ubiquitin ligase AtAIRP3/LOG2 participates in positive regulation of high-salt and drought stress responses. Plant Physiol 162:1733–1749

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kosarev P, Mayer KF, Hardtke CS (2002) Evaluation and classification of RING-finger domains encoded by the Arabidopsis genome. Genome Biol 3:RESEARCH0016

    Article  PubMed  PubMed Central  Google Scholar 

  • Lafarguette F, Leplé JC, Déjardin A, Laurans F, Costa G, Lesage-Descauses MC, Pilate G (2004) Poplar genes encoding fasciclin-like arabinogalactan proteins are highly expressed in tension wood. New Phytol 164:107–121

    Article  CAS  Google Scholar 

  • Laity JH, Lee BM, Wright PE (2001) Zinc finger proteins: new insights into structural and functional diversity. Curr Opin Plant Biol 11:39–46

    Article  CAS  Google Scholar 

  • Lenka SK, Katiyar A, Chinnusamy V, Bansal KC (2011) Comparative analysis of drought-responsive transcriptome in Indica rice genotypes with contrasting drought tolerance. Plant Biotechnol J 9:315–327

    Article  PubMed  CAS  Google Scholar 

  • Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Peer YV, Rouzé P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Letunic I, Copley RR, Schmidt S, Ciccarelli FD, Doerks T, Schultz J, Ponting CP, Bork P (2004) SMART 4.0: towards genomic data integration. Nucleic Acids Res 32(suppl 1):D142–D144

    Article  PubMed  PubMed Central  Google Scholar 

  • Lim SD, Yim WC, Moon JC, Kim DS, Lee BM, Jang CS (2010) A gene family encoding RING finger proteins in rice: their expansion, expression diversity, and co-expressed genes. Plant Mol Biol 72:369–380

    Article  PubMed  CAS  Google Scholar 

  • Liu K, Wang L, Xu Y, Chen N, Ma Q, Li F, Chong K (2007a) Overexpression of OsCOIN, a putative cold inducible zinc finger protein, increased tolerance to chilling, salt and drought, and enhanced proline level in rice. Planta 226:1007–1016

    Article  PubMed  CAS  Google Scholar 

  • Liu Y, Koornneef M, Soppe JJ (2007b) The absence of histone H2B monoubiquitination in the Arabidopsis hub1 (rdo4) mutant reveals a role for chromatin remodeling in seed dormancy. Plant Cell 19:433–444

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liu YK, Zhang D, Wang L, Li DQ (2013) Genome-wide analysis of mitogen-activated protein kinase gene family in maize. Plant Mol Biol Rep 31:1446–1460

    Article  CAS  Google Scholar 

  • Liu TK, Song XM, Duan WK, Huang ZN, Liu GF, Li Y, Hou XL (2014) Genome-wide analysis and expression patterns of NAC transcription factor family under different developmental stages and abiotic stresses in Chinese cabbage. Plant Mol Biol Rep 32:1041–1056. doi:10.1007/s11105-014-0712-6

  • Lovering R, Hanson IM, Borden KL, Martin S, O’Reilly NJ, Evan GI, Rahman D, Pappin DJ, Trowsdale J, Freemont PS (1993) Identification and preliminary characterization of a protein motif related to the zinc finger. Proc Natl Acad Sci USA 90:2112–2116

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ma K, Xiao J, Li X, Zhang Q, Lian X (2009) Sequence and expression analysis of the C3HC4-type RING finger gene family in rice. Gene 444:33–45

    Article  PubMed  CAS  Google Scholar 

  • Matsuda N, Suzuki T, Tanaka K, Nakano A (2001) Rma1, a novel type of RING finger protein conserved from Arabidopsis to human, is a membrane-bound ubiquitin ligase. J Cell Sci 114:1949–1957

    PubMed  CAS  Google Scholar 

  • Müller BSDF, Sakamoto T, Silveira RDD, Zambussi-Carvalho PF, Pereira M, Pappas GJ, Vianello-Brondani RP (2014) Differentially expressed genes during flowering and grain filling in common bean (Phaseolus vulgaris) grown under drought stress conditions. Plant Mol Biol Rep 32:438–451

    Article  CAS  Google Scholar 

  • Narusaka Y, Nakashima K, Shinwari ZK, Sakuma Y, Furihata T, Abe H, Narusaka M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Interaction between two cis-acting elements, ABRE and DRE, in ABA-dependent expression of Arabidopsis rd29A gene in response to dehydration and high-salinity stresses. Plant J 34:137–148

    Article  PubMed  CAS  Google Scholar 

  • Ohlrogge J, Benning C (2000) Unraveling plant metabolism by EST analysis. Curr Opin Plant Biol 3:224–228

    Article  PubMed  CAS  Google Scholar 

  • Pilate G, Déjardin A, Laurans F, Leplé JC (2004) Tension wood as a model for functional genomics of wood formation. New Phytol 164:63–72

    Article  CAS  Google Scholar 

  • Plomion C, Leprovost G, Stokes A (2001) Wood formation in trees. Plant Physiol 27:1513–1523

    Article  CAS  Google Scholar 

  • Qin F, Sakuma Y, Phan-Tran LS, Maruyama K, Kidokoro S, Fujita Y, Fujita M, Umezawa T, Sawano Y, Miyazono K, Tanokura M, Shinozaki K, Yamaguchi-Shinozaki K (2008) Arabidopsis DREB2A-interacting proteins function as RING E3 Ligases and negative regulate plant drought stress-responsive gene expression. Plant Cell 20:1693–1707

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Saurin AJ, Borden KLB, Boddy MN, Freemont PS (1996) Does this have a familiar RING? Trends Biochem Sci 21:208–214

    Article  PubMed  CAS  Google Scholar 

  • Shinwari ZK, Nakashima K, Miura S, Kasuga M, Seki M, Yamaguchi-Shinozaki K, Shinozaki K (1998) An Arabidopsis gene family encoding DRE/CRT binding proteins involved in low-temperature-responsive gene expression. Biochem Biophys Res Commun 250:161–170

    Article  PubMed  CAS  Google Scholar 

  • Singh KB, Foley RC, Oñate-Sánchez L (2002) Transcription factors in plant defense and stress responses. Curr Opin Plant Biol 5:430–436

    Article  PubMed  CAS  Google Scholar 

  • Sjodin A, Street NR, Sandberg G, Gustafsson P, Jansson S (2009) The Populus genome integrative explorer (PopGenIE): a new resource for exploring the Populus genome. New Phytol 182:1013–1025

    Article  PubMed  CAS  Google Scholar 

  • Song CP, Agarwal M, Ohta M, Guo Y, Halfter U, Wang P, Zhu JK (2005) Role of an Arabidopsis AP2/EREBP-type transcriptional repressor in abscisic acid and drought stress responses. Plant Cell 17:2384–2396

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Stone SL, Hauksdóttir H, Troy A, Herschleb J, Kraft E, Callis J (2005) Functional analysis of the RING-type ubiquitin ligase family of Arabidopsis. Plant Physiol 137:13–30

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Street NR, Sjödin A, Bylesjö M, Gustafsson P, Trygg J, Jansson S (2008) A cross-species transcriptomics approach to identify genes involved in leaf development. BMC Genomics 9:589

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  PubMed  CAS  Google Scholar 

  • Taylor G (2002) Populus: Arabidopsis for forestry. Do we need a model tree? Ann Bot 90:681–689

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, Schein J, Sterck L, Aerts A, Bhalerao RR, Bhalerao RP, Blaudez D, Boerjan W, Brun A, Brunner A, Busov V, Campbell M, Carlson J, Chalo M, Chapman J, Chen GL, Cooper D, Coutinho PM, Couturier J, Covert S, Cronk Q et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604

    Article  PubMed  CAS  Google Scholar 

  • Wang YS, Pi LY, Chen XH, Chakrabarty PK, Jiang J, De Leon AL, Liu GZ, Li LC, Benny U, Oard J, Ronald P, Song WY (2006) Rice XA21 binding protein 3 is a ubiquitin ligase required for full Xa21-mediated disease resistance. Plant Cell 18:3635–3646

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang ZC, Zhang HZ, Yang JL, Chen YL, Xu XM, Mao XL, Li CH (2013) Phylogenetic, expression, and bioinformatic analysis of the ABC1 gene family in Populus trichocarpa. Sci World J Article ID:785070

  • Wilkins O, Nahal H, Foong J, Provart NJ, Campbell MM (2009) Expansion and diversification of the Populus R2R3-MYB family of transcription factors. Plant Physiol 149:981–993

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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Acknowledgments

This work was supported by the National High Technology Research and Development Program of China (863 Program, 2013AA102704), the Fundamental Research Funds for the Central Universities (2572014AA35), and the Fundamental Research Funds for the Central Universities (DL11EA02).

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Authors and Affiliations

  1. State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, 150040, China

    Quangang Liu, Jingli Yang, Zhanchao Wang, Xuliang Mao, Dandan Li, Xiaoqing Hu & Chenghao Li

  2. Library of Northeast Forestry University, Harbin, 150040, China

    Xuemei Xu

  3. College of Agriculture, Yanbian University, Yanji, 133002, China

    Dongchun Jin

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  1. Quangang Liu
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  2. Jingli Yang
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  3. Zhanchao Wang
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Correspondence to Chenghao Li.

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Liu, Q., Yang, J., Wang, Z. et al. Genome-wide Classification, Identification and Expression Profile of the C3HC4-type RING Finger Gene Family in Poplar (Populus trichocarpa). Plant Mol Biol Rep 33, 1740–1754 (2015). https://doi.org/10.1007/s11105-015-0870-1

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