Skip to main content
Log in

Genome-wide analysis of the RING finger gene family in apple

  • Original Paper
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

The RING finger protein family plays a crucial role in plant growth and development and in response to biotic and abiotic stresses. However, no detailed information concerning this family is available for apple (Malus × domestica L. Borkh) due to the limited information on whole genome sequences. In this study, 688 RING domains in 663 predicted proteins were identified in apple. Based on the spacing between metal ligands or substitutions at one or more of the metal ligand positions, nine RING types were identified: RING-H2, RING-HC, RING-C2, RING-v, RING-D, RING-S/T, RING-G, RING-mH2, and RING-mHC, in which the first seven types were described previously in Arabidopsis, while the latter two were newly identified in apple. Proteins containing RING finger motifs were further classified into 57 groups according to the different known or unknown domains outside the RING domains. A total of 643 retrieved proteins appear to be distributed over all 17 linkage groups with different densities. Microarray and expressed sequence tag data revealed that only a few of these RING finger proteins may be involved in fruit development. As a first step towards genome-wide analyses of the RING-containing genes in apple, our results provide valuable information for understanding the classification and putative functions of the RING finger gene family in higher plants.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Botton A, Eccher G, Forcato C, Ferrarini A, Begheldo M, Zermiani M, Moscatello S, Battistelli A, Velasco R, Ruperti B, Ramina A (2010) Signaling pathways mediating the induction of apple fruitlet abscission. Plant Physiol 155:185–208

    Article  PubMed  Google Scholar 

  • Cerqueira GC, Bartholomeu DC, DaRocha WD, Hou L, Freitas-Silva DM, Machado CR, El-Sayed NM, Teixeira SM (2008) Sequence diversity and evolution of multigene families in Trypanosoma cruzi. Mol Biochem Parasitol 157:65–72

    Article  PubMed  CAS  Google Scholar 

  • Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, Higgins DG, Thompson JD (2003) Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res 31:3497–3500

    Article  PubMed  CAS  Google Scholar 

  • Chow ED, Liu OW, O’Brien S, Madhani HD (2007) Exploration of whole-genome responses of the human AIDS-associated yeast pathogen Cryptococcus neoformans var grubii: nitric oxide stress and body temperature. Curr Genet 52:137–148

    Article  PubMed  CAS  Google Scholar 

  • Costa F, Peace CP, Stella S, Serra S, Musacchi S, Bazzani M, Sansavini S, Van de Weg WE (2010) QTL dynamics for fruit firmness and softening around an ethylene-dependent polygalacturonase gene in apple (Malus × domestica Borkh.). J Exp Bot 61:3029–3039

    Article  PubMed  CAS  Google Scholar 

  • Dimick PS, Hoskin JC (1983) Review of apple flavor—state of the art. Crit Rev Food Sci Nutr 18:387–409

    Article  PubMed  CAS  Google Scholar 

  • Doherty FJ, Dawson S, Mayer RJ (2002) The ubiquitin-proteasome pathway of intracellular proteolysis. Essays Biochem 38:51–63

    PubMed  CAS  Google Scholar 

  • Dong CH, Agarwal M, Zhang Y, Xie Q, Zhu JK (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 USA 103:8281–8286

    Article  PubMed  CAS  Google Scholar 

  • Freemont PS (1993) The RING finger. A novel protein sequence motif related to the zinc finger. Ann NY Acad Sci 684:174–192

    Article  PubMed  CAS  Google Scholar 

  • Freemont PS (2000) RING for destruction? Curr Biol 10:R84–R87

    Article  PubMed  CAS  Google Scholar 

  • Freemont PS, Hanson IM, Trowsdale J (1991) A novel cysteine-rich sequence motif. Cell 64:483–484

    Article  PubMed  CAS  Google Scholar 

  • Gagne JM, Downes BP, Shiu SH, Durski AM, Vierstra RD (2002) The F-box subunit of the SCF E3 complex is encoded by a diverse superfamily of genes in Arabidopsis. Proc Natl Acad Sci USA 99:11519–11524

    Article  PubMed  CAS  Google Scholar 

  • Gao Y, Nishikawa H, Badejo AA, Shibata H, Sawa Y, Nakagawa T, Maruta T, Shigeoka S, Smirnoff N, Ishikawa T (2011) Expression of aspartyl protease and C3HC4-type RING zinc finger genes are responsive to ascorbic acid in Arabidopsis thaliana. J Exp Bot

  • Gray WM, Muskett PR, Chuang HW, Parker JE (2003) Arabidopsis SGT1b is required for SCF(TIR1)-mediated auxin response. Plant Cell 15:1310–1319

    Article  PubMed  CAS  Google Scholar 

  • Han SE, Seo YS, Kim D, Sung SK, Kim WT (2007) Expression of MdCAS1 and MdCAS2, encoding apple beta-cyanoalanine synthase homologs is concomitantly induced during ripening and implicates MdCASs in the possible role of the cyanide detoxification in Fuji apple (Malus domestica Borkh.) fruits. Plant Cell Rep 26:1321–1331

    Article  PubMed  CAS  Google Scholar 

  • Han SE, Seo YS, Heo S, Kim D, Sung SK, Kim WT (2008) Structure and expression of MdFBCP1, encoding an F-box-containing protein 1 during Fuji apple (Malus domestica Borkh.) fruit ripening. Plant Cell Rep 27:1291–1301

    Article  PubMed  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 

  • Hsia MM, Callis J (2010) BRIZ1 and BRIZ2 proteins form a heteromeric E3 ligase complex required for seed germination and post-germination growth in Arabidopsis thaliana. J Biol Chem 285:37070–37081

    Article  PubMed  CAS  Google Scholar 

  • Huang Y, Li CY, Pattison DL, Gray WM, Park S, Gibson SI (2010) SUGAR-INSENSITIVE3, a RING E3 ligase, is a new player in plant sugar response. Plant Physiol 152:1889–1900

    Article  PubMed  CAS  Google Scholar 

  • Janssen BJ, Thodey K, Schaffer RJ, Alba R, Balakrishnan L, Bishop R, Bowen JH, Crowhurst RN, Gleave AP, Ledger S, McArtney S, Pichler FB, Snowden KC, Ward S (2008) Global gene expression analysis of apple fruit development from the floral bud to ripe fruit. BMC Plant Biol 8:16

    Article  PubMed  Google Scholar 

  • Kawasaki T, Nam J, Boyes DC, Holt BF 3rd, Hubert DA, Wiig A, Dangl JL (2005) A duplicated pair of Arabidopsis RING-finger E3 ligases contribute to the RPM1- and RPS2-mediated hypersensitive response. Plant J 44:258–270

    Article  PubMed  CAS  Google Scholar 

  • Kepinski S, Leyser O (2005) The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435:446–451

    Article  PubMed  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

    Google Scholar 

  • Kraft E, Stone SL, Ma L, Su N, Gao Y, Lau OS, Deng XW, Callis J (2005) Genome analysis and functional characterization of the E2 and RING-type E3 ligase ubiquitination enzymes of Arabidopsis. Plant Physiol 139:1597–1611

    Article  PubMed  CAS  Google Scholar 

  • Kraft E, Bostick M, Jacobsen SE, Callis J (2008) ORTH/VIM proteins that regulate DNA methylation are functional ubiquitin E3 ligases. Plant J 56:704–715

    Article  PubMed  CAS  Google Scholar 

  • Lee YP, Yu GH, Seo YS, Han SE, Choi YO, Kim D, Mok IG, Kim WT, Sung SK (2007) Microarray analysis of apple gene expression engaged in early fruit development. Plant Cell Rep 26:917–926

    Article  PubMed  CAS  Google Scholar 

  • Lee HK, Cho SK, Son O, Xu Z, Hwang I, Kim WT (2009) Drought stress-induced Rma1H1, a RING membrane-anchor E3 ubiquitin ligase homolog, regulates aquaporin levels via ubiquitination in transgenic Arabidopsis plants. Plant Cell 21:622–641

    Article  PubMed  CAS  Google Scholar 

  • Leng S, Song W, Gu Y, Wang Y (2003) Associations of Bsm1 polymorphism of the vitamin D receptor gene and blood lead, zinc protoporphyrin, and physical development in 476 environmental lead-exposed children. Wei Sheng Yan Jiu 32:610–612

    PubMed  CAS  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 

  • 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  CAS  Google Scholar 

  • Molnar G, Bancos S, Nagy F, Szekeres M (2002) Characterisation of BRH1, a brassinosteroid-responsive RING-H2 gene from Arabidopsis thaliana. Planta 215:127–133

    Article  PubMed  CAS  Google Scholar 

  • Park S, Sugimoto N, Larson MD, Beaudry R, van Nocker S (2006) Identification of genes with potential roles in apple fruit development and biochemistry through large-scale statistical analysis of expressed sequence tags. Plant Physiol 141:811–824

    Article  PubMed  CAS  Google Scholar 

  • Peng M, Hannam C, Gu H, Bi YM, Rothstein SJ (2007) A mutation in NLA, which encodes a RING-type ubiquitin ligase, disrupts the adaptability of Arabidopsis to nitrogen limitation. Plant J 50:320–337

    Article  PubMed  CAS  Google Scholar 

  • Perez-Torres CA, Lopez-Bucio J, Cruz-Ramirez A, Ibarra-Laclette E, Dharmasiri S, Estelle M, Herrera-Estrella L (2008) Phosphate availability alters lateral root development in Arabidopsis by modulating auxin sensitivity via a mechanism involving the TIR1 auxin receptor. Plant Cell 20:3258–3272

    Article  PubMed  CAS  Google Scholar 

  • Prasad ME, Schofield A, Lyzenga W, Liu H, Stone SL (2010) Arabidopsis RING E3 ligase XBAT32 regulates lateral root production through its role in ethylene biosynthesis. Plant Physiol 153:1587–1596

    Article  PubMed  CAS  Google Scholar 

  • Qin R, Gao S, McDonald JA, Ajwa H, Shem-Tov S, Sullivan DA (2008) Effect of plastic tarps over raised-beds and potassium thiosulfate in furrows on chloropicrin emissions from drip fumigated fields. Chemosphere 72:558–563

    Article  PubMed  CAS  Google Scholar 

  • Ruegger M, Dewey E, Gray WM, Hobbie L, Turner J, Estelle M (1998) The TIR1 protein of Arabidopsis functions in auxin response and is related to human SKP2 and yeast grr1p. Genes Dev 12:198–207

    Article  PubMed  CAS  Google Scholar 

  • Serrano M, Guzman P (2004) Isolation and gene expression analysis of Arabidopsis thaliana mutants with constitutive expression of ATL2, an early elicitor-response RING-H2 zinc-finger gene. Genetics 167:919–929

    Article  PubMed  CAS  Google Scholar 

  • Smalle J, Vierstra RD (2004) The ubiquitin 26S proteasome proteolytic pathway. Annu Rev Plant Biol 55:555–590

    Article  PubMed  CAS  Google Scholar 

  • Stone SL, Hauksdottir 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  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 

  • Torii KU, Stoop-Myer CD, Okamoto H, Coleman JE, Matsui M, Deng XW (1999) The RING finger motif of photomorphogenic repressor COP1 specifically interacts with the RING-H2 motif of a novel Arabidopsis protein. J Biol Chem 274:27674–27681

    Article  PubMed  CAS  Google Scholar 

  • Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, Kalyanaraman A, Fontana P, Bhatnagar SK, Troggio M, Pruss D, Salvi S, Pindo M, Baldi P, Castelletti S, Cavaiuolo M, Coppola G, Costa F, Cova V, Dal Ri A, Goremykin V, Komjanc M, Longhi S, Magnago P, Malacarne G, Malnoy M, Micheletti D, Moretto M, Perazzolli M, Si-Ammour A, Vezzulli S, Zini E, Eldredge G, Fitzgerald LM, Gutin N, Lanchbury J, Macalma T, Mitchell JT, Reid J, Wardell B, Kodira C, Chen Z, Desany B, Niazi F, Palmer M, Koepke T, Jiwan D, Schaeffer S, Krishnan V, Wu C, Chu VT, King ST, Vick J, Tao Q, Mraz A, Stormo A, Stormo K, Bogden R, Ederle D, Stella A, Vecchietti A, Kater MM, Masiero S, Lasserre P, Lespinasse Y, Allan AC, Bus V, Chagne D, Crowhurst RN, Gleave AP, Lavezzo E, Fawcett JA, Proost S, Rouze P, Sterck L, Toppo S, Lazzari B, Hellens RP, Durel CE, Gutin A, Bumgarner RE, Gardiner SE, Skolnick M, Egholm M, Van de Peer Y, Salamini F, Viola R (2010) The genome of the domesticated apple (Malus × domestica Borkh.). Nat Genet 42:833–839

    Article  PubMed  CAS  Google Scholar 

  • Vierstra RD (2009) The ubiquitin-26S proteasome system at the nexus of plant biology. Nat Rev Mol Cell Biol 10:385–397

    Article  PubMed  CAS  Google Scholar 

  • Wilkinson KD (2000) Ubiquitination and deubiquitination: targeting of proteins for degradation by the proteasome. Semin Cell Dev Biol 11:141–148

    Article  PubMed  CAS  Google Scholar 

  • Xie Q, Frugis G, Colgan D, Chua NH (2000) Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development. Genes Dev 14:3024–3036

    Article  PubMed  CAS  Google Scholar 

  • Xie Q, Guo HS, Dallman G, Fang S, Weissman AM, Chua NH (2002) SINAT5 promotes ubiquitin-related degradation of NAC1 to attenuate auxin signals. Nature 419:167–170

    Article  PubMed  CAS  Google Scholar 

  • Xu R, Li QQ (2003) A RING-H2 zinc-finger protein gene RIE1 is essential for seed development in Arabidopsis. Plant Mol Biol 53:37–50

    Article  PubMed  CAS  Google Scholar 

  • Zhang X, Garreton V, Chua NH (2005) The AIP2 E3 ligase acts as a novel negative regulator of ABA signaling by promoting ABI3 degradation. Genes Dev 19:1532–1543

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Natural Science Foundation (Grant No. 30970230) and the Genetically Modified Organisms Breeding Major Projects (2009ZX08009-092B) in China.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Chengchao Zheng.

Additional information

Communicated by P. Westhoff.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Li, Y., Wu, B., Yu, Y. et al. Genome-wide analysis of the RING finger gene family in apple. Mol Genet Genomics 286, 81–94 (2011). https://doi.org/10.1007/s00438-011-0625-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-011-0625-0

Keywords

Navigation