Skip to main content
SpringerLink
Log in

Functional analysis reveals pleiotropic effects of rice RING-H2 finger protein gene OsBIRF1 on regulation of growth and defense responses against abiotic and biotic stresses

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

RING finger proteins comprise a large family and play key roles in regulating growth/developmental processes, hormone signaling and responses to biotic and abiotic stresses in plants. A rice gene, OsBIRF1, encoding a putative RING-H2 finger protein, was cloned and identified. OsBIRF1 encodes a 396 amino acid protein belonging to the ATL family characterized by a conserved RING-H2 finger domain (C-X2-C-X15-C-X1-H-X2-H-X2-C-X10-C-X2-C), a transmembrane domain at the N-terminal, a basic amino acid rich region and a characteristic GLD region. Expression of OsBIRF1 was up-regulated in rice seedlings after treatment with benzothaidiazole, salicylic acid, l-aminocyclopropane-1-carboxylic acid and jasmonic acid, and was induced differentially in incompatible but not compatible interactions between rice and Magnaporthe grisea, the causal agent of blast disease. Transgenic tobacco plants that constitutively express OsBIRF1 exhibit enhanced disease resistance against tobacco mosaic virus and Pseudomonas syringae pv. tabaci and elevated expression levels of defense-related genes, e.g. PR-1, PR-2, PR-3 and PR-5. The OsBIRF1-overexpressing transgenic tobacco plants show increased oxidative stress tolerance to exogenous treatment with methyl viologen and H2O2, and up-regulate expression of oxidative stress-related genes. Reduced ABA sensitivity in root elongation and increased drought tolerance in seed germination were also observed in OsBIRF1 transgenic tobacco plants. Furthermore, the transgenic tobacco plants show longer roots and higher plant heights as compared with the wild-type plants, suggesting that overexpression of OsBIRF1 promote plant growth. These results demonstrate that OsBIRF1 has pleiotropic effects on growth and defense response against multiple abiotic and biotic stresses.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

ABA:

Abscisic acid

ACC:

1-Amino cyclopropane-1-carboxylic acid

BTH:

Benzothiadiazole

CaMV:

Cauliflower mosaic virus

ET:

Ethylene

H2O2 :

Hydrogen peroxide

JA:

Jasmonic acid

MV:

Methyl viologen

ORF:

Open reading frame

PCR:

Polymerase chain reaction

PEG:

Polyethylene glycol

PR:

Pathogenesis-related

RT-PCR:

Reverse transcription-PCR

SA:

Salicylic acid

TMV:

Tobacco mosaic virus

References

  • Cheung MY, Zeng NY, Tong SW, Li FWY, Zhao KJ, Zhang Q, Sun SM, 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 

  • Disch S, Anastasiou E, Sharma VK, Laux T, Fletcher JC, Lenhard M (2006) The E3 ubiquitin ligase BIG BROTHER controls Arabidopsis organ size in a dosage-dependent manner. Curr Biol 16:272–279

    Article  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 

  • Duek PD, Elmer MV, van Oosten VR, Fankhauser C (2004) The degradation of HFR1, a putative bHLH class transcription factor involved in light signaling, is regulated by phosphorylation and requires COP1. Curr Biol 14:2296–2301

    Article  PubMed  CAS  Google Scholar 

  • Durrant WE, Rowland O, Piedras P, Hammond-Kosack KE, Jones JDG (2000) cDNA-AFLP reveals a striking overlap in race specific resistance and wound response gene expression profiles. Plant Cell 12:963–977

    Article  PubMed  CAS  Google Scholar 

  • Fang S, Weissman AM (2004) A field guide to ubiquitylation. Cell Mol Life Sci 61:1546–1561

    Article  PubMed  CAS  Google Scholar 

  • Finkelstein RR, Gampala SS, Rock CD (2002) Abscisic acid signaling in seeds and seedlings. Plant Cell 14(suppl):S15–S45

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227

    Article  PubMed  CAS  Google Scholar 

  • Glickman MH, Ciechanover A (2002) The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol Rev 82:373–428

    PubMed  CAS  Google Scholar 

  • Hardtke CS, Gohda K, Osterlund MT, Oyama T, Okada K, Deng XW (2000) HY5 stability and activity in Arabidopsis is regulated by phosphorylation in its COP1 binding domain. EMBO J 19:4997–5006

    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 

  • Hershko A, Ciechanover A (1998) The ubiquitin system. Ann Rev Biochem 67:425–479

    Article  PubMed  CAS  Google Scholar 

  • Holm M, Ma LG, Qu LJ, Deng XW (2002) Two interacting bZIP proteins are direct targets of COP1-mediated control of light-dependent gene expression in Arabidopsis. Genes Dev 16:1247–1259

    Article  PubMed  CAS  Google Scholar 

  • Hondo D, Hase S, Kanayama Y, Yoshikawa N, Takenaka S, Takahashi H (2007) The LeATL6-associated ubiquitin/proteasome system may contribute to fungal elicitor-activated defense response via the jasmonic acid-dependent signaling pathway in tomato. Mol Plant Microbe Interact 20:72–81

    Article  PubMed  CAS  Google Scholar 

  • Hong JK, Choi HW, Hwang IS, Hwang BK (2007) Role of a novel pathogen-induced pepper C3-H-C4 type RING-finger protein gene, CaRFP1, in disease susceptibility and osmotic stress tolerance. Plant Mol Biol 63:571–588

    Article  PubMed  CAS  Google Scholar 

  • Jang IC, Yang JY, Seo HS, Chua NH (2005) HFR1 is targeted by COP1 E3 ligase for post-translational proteolysis during phytochrome A signaling. Genes Dev 19:593–602

    Article  PubMed  CAS  Google Scholar 

  • Joazeiro CA, Weissman AM (2000) RING finger proteins: mediators of ubiquitin ligase activity. Cell 102:549–552

    Article  PubMed  CAS  Google Scholar 

  • Kam J, Gresshoff P, Shorter R, Xue G-P (2007) Expression analysis of RING zinc finger genes from Triticum aestivum and identification of TaRZF70 that contains four RING-H2 domains and differentially responds to water deficit between leaf and root. Plant Sci 173:650–659

    Article  CAS  Google Scholar 

  • Karlowski WM, Hirsch AM (2003) The over-expression of an alfalfa RING-H2 gene induces pleiotropic effects on plant growth and development. Plant Mol Biol 52:121–133

    Article  PubMed  CAS  Google Scholar 

  • Katoh S, Hong C, Tsunoda Y, Murata K, Takai R, Minami E, Yamazaki T, Katoh E (2003) High precision NMR structure and function of the RING-H2 finger domain of EL5, a rice protein whose expression is increased upon exposure to pathogen-derived oligosaccharides. J Biol Chem 278:15341–15348

    Article  PubMed  CAS  Google Scholar 

  • Katoh S, Tsunoda Y, Murata K, Minami E, Katoh E (2005) Active site residues and amino acid specificity of the ubiquitin carrier protein-binding RING-H2 finger domain. J Biol Chem 280:41015–41024

    Article  PubMed  CAS  Google Scholar 

  • Kawasaki T, Nam J, Boyes DC, Holt 3rd BF, 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 

  • Ko JH, Yang SH, Han KH (2006) Upregulation of an Arabidopsis RING-H2 gene, XERICO, confers drought tolerance through increased abscisic acid biosynthesis. Plant J 47:343–355

    Article  PubMed  CAS  Google Scholar 

  • Koiwai H, Tagiri A, Katoh S, Katoh E, Ichikawa H, Minami E, Nishizawa Y (2007) RING-H2 type ubiquitin ligase EL5 is involved in root development through the maintenance of cell viability in rice. Plant J 51:92–104

    Article  PubMed  CAS  Google Scholar 

  • Lechner E, Goloubinoff P, Genschik P, Shen WH (2002) A gene trap dissociation insertion line, associated with a RING-H2 finger gene, shows tissue specific and developmental regulated expression of the gene in Arabidopsis. Gene 290:63–71

    Article  PubMed  CAS  Google Scholar 

  • Lee H, Xiong L, Gong Z, Ishitani M, Stevenson B, Zhu JK (2001) The Arabidopsis HOS1 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  CAS  Google Scholar 

  • Liu K, Wang L, Xu Y, Chen N, Ma Q, Li F, Chong K (2007) Overexpression of OsCOIN, a putative cold inducible zinc finger protein, increased tolerance to chilling, salt and drought, and enhanced proline level in rice. Planta 226:1007–1116

    Article  PubMed  CAS  Google Scholar 

  • Luo H, Song F, Goodman RM, Zheng Z (2005a) Up-regulation of OsBIHD1, a rice gene encoding BELL homeodomain transcriptional factor, in disease resistance responses. Plant Biol 7:459–468

    Article  PubMed  CAS  Google Scholar 

  • Luo H, Song F, Zheng Z (2005b) Overexpression in transgenic tobacco reveals different roles for the rice homeodomain gene OsBIHD1 in biotic and abiotic stress responses. J Exp Bot 56:2673–2682

    Article  PubMed  CAS  Google Scholar 

  • Ma L, Gao Y, Qu L, Chen Z, Li J, Zhao H, Deng XW (2002) Genomic evidence for COP1 as a repressor of light-regulated gene expression and development in Arabidopsis. Plant Cell 14:2383–2398

    Article  PubMed  CAS  Google Scholar 

  • Meng XB, Zhao WS, Lin RM, Wang M, Peng YL (2006) Molecular cloning and characterization of a rice blast-inducible RING-H2 type zinc finger gene. DNA Seq 17:41–48

    PubMed  CAS  Google Scholar 

  • Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) The reactive oxygen gene network of plants. Trends Plant Sci 9:490–498

    Article  PubMed  CAS  Google Scholar 

  • Mittler R, Kim Y, Song L, Coutu J, Coutu A, Ciftci-Yilmaz S, Lee H, Stevenson B, Zhu JK (2006) Gain- and loss-of-function mutations in Zat10 enhance the tolerance of plants to abiotic stress. FEBS Lett 580:6537–6542

    Article  PubMed  CAS  Google Scholar 

  • Molnar G, Bancoş 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 

  • Moon J, Parry G, Estelle M (2004) The ubiquitin-proteasome pathway and plant development. Plant Cell 16:3181–3195

    Article  PubMed  CAS  Google Scholar 

  • Nishimura R, Ohmori M, Fujita H, Kawaguchi M (2002) A Lotus basic leucine zipper protein with a RING-finger motif negatively regulates the developmental program of nodulation. Proc Natl Acad Sci USA 99:15206–15210

    Article  PubMed  CAS  Google Scholar 

  • Nodzon LA, Xu WH, Wang YS, Pi LY, Chakrabarty PK, Song WY (2004) The ubiquitin ligase XBAT32 regulates lateral root development in Arabidopsis. Plant J 40:996–1006

    Article  PubMed  CAS  Google Scholar 

  • Osterlund MT, Hardtke CS, Wei N, Deng XW (2000) Targeted destabilization of HY5 during light-regulated development of Arabidopsis. Nature 405:462–466

    Article  PubMed  CAS  Google Scholar 

  • Ramonell K, Berrocal-Lobo M, Koh S, Wan J, Edwards H, Stacey G, Somerville S (2005) Loss-of-function mutations in chitin responsive genes show increased susceptibility to the powdery mildew pathogen Erysiphe cichoracearum. Plant Physiol 138:1027–1036

    Article  PubMed  CAS  Google Scholar 

  • Sahin-Cevik M, Moore GA (2007) Isolation and characterization of a novel RING-H2 finger gene induced in response to cold and drought in the interfertile Citrus relative Poncirus trifoliate. Physiol Plant 126:153–161

    Article  Google Scholar 

  • Saijo Y, Sullivan JA, Wang H, Yang J, Shen Y, Rubio V, Ma L, Hoecker U, Deng XW (2003) The COP1-SPA1 interaction defines a critical step in phytochrome A-mediated regulation of HY5 activity. Genes Dev 17:2642–2647

    Article  PubMed  CAS  Google Scholar 

  • Salinas-Mondragon RE, Garciduenas-Pina C, Guzman P (1999) Early elicitor induction in members of a novel multigene family coding for highly related RING-H2 proteins in Arabidopsis thaliana. Plant Mol Biol 40:579–590

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Schumann U, Prestele J, O’Geen H, Brueggeman R, Wanner G, Gietl C (2007) Requirement of the C3HC4 zinc RING finger of the Arabidopsis PEX10 for photorespiration and leaf peroxisome contact with chloroplasts. Proc Natl Acad Sci USA 104:1069–1074

    Article  PubMed  CAS  Google Scholar 

  • Seo HS, Yang JY, Ishikawa M, Bolle C, Ballesteros ML, Chua NH (2003) LAF1 ubiquitination by COP1 controls photomorphogenesis and is stimulated by SPA1. Nature 423:995–999

    Article  PubMed  CAS  Google Scholar 

  • Seo HS, Watanabe E, Tokutomi S, Nagatani A, Chua NH (2004) Photoreceptor ubiquitination by COP1 E3 ligase desensitizes phytochrome A signaling. Genes Dev 18:617–622

    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 

  • Serrano M, Parra S, Alcaraz LD, Guzman P (2006) The ATL gene family from Arabidopsis thaliana and Oryza sativa comprises a large number of putative ubiquitin ligases of the RING-H2 type. J Mol Evol 62:434–445

    Article  PubMed  CAS  Google Scholar 

  • Shimomura K, Nomura M, Tajima S, Kouchi H (2006) LjnsRING, a novel RING finger protein, is required for symbiotic interactions between Mesorhizobium loti and Lotus japonicus. Plant Cell Physiol 47:1572–1581

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Song F, Goodman RM (2002) OsBIMK1, a rice MAP kinase gene involved in disease resistance responses. Planta 215:997–1005

    Article  PubMed  CAS  Google Scholar 

  • Sonoda Y, Yao SG, Sako K, Sato T, Kato W, Ohto MA, Ichikawa T, Matsui M, Yamaguchi J, Ikeda A (2007) SHA1, a novel RING finger protein, functions in shoot apical meristem maintenance in Arabidopsis. Plant J 50:586–596

    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 

  • Takai R, Hasegawa K, Kaku H, Shibuya N, Minami E (2001) Isolation and analysis of expression mechanisms of a rice gene, EL5, which shows structural similarity to ATL family from Arabidopsis, in response to N-acetylchitooligosaccharide elicitor. Plant Sci 160:577–583

    Article  PubMed  CAS  Google Scholar 

  • Takai R, Matsuda N, Nakano A, Hasegawa K, Akimoto C, Shibuya N, Minami E (2002) EL5, a rice N-acetylchitooligosaccharide elicitor-responsive RING-H2 finger protein, is a ubiquitin ligase which functions in vitro in co-operation with an elicitor-responsive ubiquitin-conjugating enzyme, OsUBC5b. Plant J 30:447–455

    Article  PubMed  CAS  Google Scholar 

  • Veronese P, Narasimhan ML, Stevenson RA, Zhu JK, Weller SC, Subbarao KV, Bressan RA (2003) Identification of a locus controlling Verticillium disease symptom response in Arabidopsis thaliana. Plant J 35:574–587

    Article  PubMed  CAS  Google Scholar 

  • Xie Q, Guo HS, Dallman G, Fang SY, 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 

  • Yang J, Lin R, Sullivan J, Hoecker U, Liu B, Xu L, Deng XW, Wang H (2005) Light regulates COP1-mediated degradation of HFR1, a transcription factor essential for light signaling in Arabidopsis. Plant Cell 17:804–821

    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 

  • Zhang Y, Yang C, Li Y, Zheng N, Chen H, Zhao Q, Gao T, Guo H, Xie Q (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  CAS  Google Scholar 

Download references

Acknowledgements

We are grateful to Dr Zuhua He, Shanghai Institute of Plant Physiology and Ecology, Chinese Academy of Science, for the rice near-isogenic lines H8R and H8S, and Mr Rongyao Chai, Zhejiang Academy of Agricultural Science, for the Magnaporthe grisea isolate 85-14B1. This study was supported by National Natural Science Foundation of China (grants no. 30571209 and 30771399), the National High-Tech (“863”) Project (2006AA10Z430), the National Key Basic Research and Development Program (2006CB101903) and the Fund for the New Century Talent Program from MOE of China.

Author information

Authors and Affiliations

  1. State Key Laboratory for Rice Biology, Institute of Biotechnology, Zhejiang University, Huajiachi Campus, Hangzhou, Zhejiang, 310029, People’s Republic of China

    Huizhi Liu, Huijuan Zhang, Yayun Yang, Guojun Li, Yuxia Yang, Xiao’e Wang, B. M. Vindhya S. Basnayake, Dayong Li & Fengming Song

  2. Department of Plant Protection, Zhejiang University, Huajiachi Campus, Hangzhou, Zhejiang, 310029, People’s Republic of China

    Fengming Song

Authors
  1. Huizhi Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Huijuan Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yayun Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Guojun Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yuxia Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xiao’e Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. B. M. Vindhya S. Basnayake
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Dayong Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Fengming Song
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fengming Song.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Liu, H., Zhang, H., Yang, Y. et al. Functional analysis reveals pleiotropic effects of rice RING-H2 finger protein gene OsBIRF1 on regulation of growth and defense responses against abiotic and biotic stresses. Plant Mol Biol 68, 17–30 (2008). https://doi.org/10.1007/s11103-008-9349-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-008-9349-x

Keywords

Search

Navigation