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A RING finger E3 ligase gene, Oryza sativa Delayed Seed Germination 1 (OsDSG1), controls seed germination and stress responses in rice

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Abstract

Seed germination is an important character for plant growth and seed quality. We identified a rice mutant that was delayed in its germination. There, T-DNA was inserted into Oryza sativa Delayed Seed Germination 1 (OsDSG1), causing a recessive null mutation. Overexpression of the gene enhanced seed germination. OsDSG1 is most similar to Arabidopsis AIP2, an E3 ligase targeting ABI3.Yeast two-hybrid experiments showed that our OsDSG1 binds to OsABI3, indicating that OsDSG1 is a rice ortholog of AIP2. Self-ubiquitination assay indicated that bacterially expressed OsDSG1 protein has E3 ubiquitin ligase activity. Real-time PCR analysis revealed that OsDSG1 was expressed in leaves and roots, and strongly in developing seeds. In addition to the delayed-germination phenotype, mutant plants were shorter and had greater tolerance to high-salt and drought stresses. In the osdsg1 mutant, transcript levels of ABA signaling genes and ABA responsive genes were significantly increased. By contrast, expressions of OsGAMYB and its downstream genes that encode hydrolytic enzymes were markedly reduced. These observations support that OsDSG1 is a major regulator of ABA signaling in germinating seeds. Finally, we observed that the germination rates of various rice cultivars depended upon the transcript levels of OsDSG1 and other ABA-signaling genes.

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References

  • Amador V, Monte E, Garcı′a-Martı′nez JL, Prat S (2001) Gibberellins signal nuclear import of PHOR1, a photoperiodresponsive protein with homology to Drosophila armadillo. Cell 106:343–354

    Article  CAS  PubMed  Google Scholar 

  • An G, Ebert PR, Mitra A, Ha SB (1988) Binary vectors. Plant Mol Biol Manual A3:1–19

    Google Scholar 

  • An S, Park S, Jeong DH, Lee DY, Kang HG, Yu JH, Hur J, Kim SR, Kim YH, Lee M, Han S, Kim SJ, Yang J, Kim E, Wi SJ, Chung HS, Hong JP, Choe V, Lee HK, Choi JH, Nam J, Park PB, Park KY, Kim WT, Choe S, Lee CB, An G (2003) Generation and analysis of end sequence database for T-DNA tagging lines in rice. Plant Physiol 133:2040–2047

    Article  CAS  PubMed  Google Scholar 

  • Asatsuma S, Sawada C, Itoh K, Okito M, Kitajima A, Mitsui T (2005) Involvement of α-amylase I-1 in starch degradation in rice chloroplasts. Plant Cell Physiol 46:858–869

    Article  CAS  PubMed  Google Scholar 

  • Assmann SM (2005) G protein signaling in the regulation of rice seed germination. Science 310:12–20

    Article  Google Scholar 

  • Bu Q, Li H, Zhao Q, Jiang H, Zhai Q, Zhang J, Wu X, Sun J, Xie Q, Wang D, Li C (2009) The Arabidopsis RING Finger E3 ligase RHA2a is a novel positive regulator of abscisic acid signaling during seed germination and early seedling development. Plant Physiol 150:463–481

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Cho SK, Chung HS, Ryu MY, Park MJ, Lee MM, Bahk Y-Y, Kim J, Pai HS, Kim WT (2006) Heterologous expression and molecular and cellular characterization of CaPUB1 encoding a hot pepper U-box E3 ubiquitin ligase homolog. Plant Physiol 142:1664–1682

    Article  CAS  PubMed  Google Scholar 

  • Deng XW, Caspar T, Quail PH (1991) cop1: a regulatory locus involved in light-controlled development and gene expression in Arabidopsis. Genes Dev 5:1172–1182

    Article  CAS  PubMed  Google Scholar 

  • Finkelstein RR, Wang ML, Lynch TJ, Rao S, Goodman HM (1998) The Arabidopsis abscisic acid response locus ABI4 encodes an APETALA 2 domain protein. Plant Cell 10:1043–1054

    Article  CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Gietz D, St Jean A, Woods RA, Schiestl RH (1992) Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res 20:1425–1436

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez-Lamothe R, Tsitsigiannis DI, Ludwig AA, Panicot M, Shirasu K, Jones JD (2006) The U-box protein CMPG1isrequired for efficient activation of defense mechanisms triggered by multiple resistance genes in tobacco and tomato. Plant Cell 18:1067–1083

    Article  CAS  PubMed  Google Scholar 

  • Han MJ, Jung KM, Yi G, Lee DY, An G (2006) Rice Immature Pollen 1 (RIP1) is a regulator of late pollen development. Plant Cell Physiol 47:1457–1472

    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 

  • Hegedus D, Yu M, Baldwin D, Gruber M, Sharpe A, Parkin I, Whitwill S, Lydiate D (2003) Molecular characterization of Brassica napus NAC domain transcriptional activators induced in response to biotic and abiotic stress. Plant Mol Biol 53:383–397

    Article  CAS  PubMed  Google Scholar 

  • Jeon J, Lee S, Jung KH, Jun SH, Jeong DH, Lee J, Kim C, Jang S, Yang K, Nam JM, An K, Han MJ, Sung RJ, Choi HS, Yu JW, Choi JH, Cho SY, Cha SS, An G (2000) T-DNA insertional mutagenesis for functional genomics in rice. Plant J 22:561–570

    Article  CAS  PubMed  Google Scholar 

  • Jeong DH, An S, Kang HG, Moon S, Han JJ, Park S, Lee HS, An K, An G (2002) T-DNA insertional mutagenesis for activation tagging in rice. Plant Physiol 130:1636–1644

    Article  CAS  PubMed  Google Scholar 

  • Jeong DH, An S, Park S, Kang HG, Park GG, Kim SR, Sim J, Kim YO, Kim MK, Kim SR, Kim J, Shin M, Jung M, An G (2006) Generation of flanking sequence-tag database for activation-tagging lines in japonica rice. Plant J 45:123–132

    Article  CAS  PubMed  Google Scholar 

  • Kang HG, Park S, Matsuoka M, An G (2005) White-core endosperm floury endosperm-4 in rice is generated by knockout mutations in the C4-type pyruvate orthophosphosphate dikinase gene (OsPPDKB). Plant J 42:901–911

    Article  CAS  PubMed  Google Scholar 

  • Kim SR, Lee S, Kang HG, Jeon JS, Kim KM, An G (2003) A complete sequence of the pGA1611 binary vector. J Plant Biol 16:211–214

    Article  Google Scholar 

  • Kim DH, Yamaguchi S, Lim SH, Oh EY, Park JM, Hanada A, Kamiya Y, Choi GS (2008) SOMNUS, a CCCH-type zinc finger protein in Arabidopsis, negatively regulates light-dependent seed germination downstream of PIL5. Plant Cell 10:1260–1277

    Article  Google Scholar 

  • Kim SR, Lee DY, Yang JI, Moon S, An G (2009) Cloning vectors for rice. J Plant Biol 52:73–78

    Article  CAS  Google Scholar 

  • Lee JH, Deng XW, Kim WT (2006) Possible role of light in the maintenance of EIN3/EIL1 stability in Arabidopsis seedlings. Biochem Biophys Res Commun 350:484–491

    Article  CAS  PubMed  Google Scholar 

  • Leubner-Metzger (2003) Functions and regulation of β-1,3-glucanases during seed germination, dormancy release and after-ripening. Seed Sci Res 13:17–34

  • Leung J, Bouvier-Durand M, Morris PC, Guerrier D, Chefdor F, Giraudat J (1994) Arabidopsis ABA response gene ABI1: Features of a calcium-modulated protein phosphatase. Science 264:1448–1452

    Article  CAS  PubMed  Google Scholar 

  • Liu H, Zhang H, Yang Y, Li G, Yang Y, Wang X, Basnayake BM, Li D, Song F (2008) 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 Moi Biol 68:17–30

    Article  CAS  Google Scholar 

  • Lopez-Molina L, Mongrand S, McLachlin DT, Chait BT, Chua NH (2002) ABI5 acts downstream of ABI3 to execute an ABA-dependent growth arrest during germination. Plant J 32:317–328

    Article  CAS  PubMed  Google Scholar 

  • Lorick KL, Jensen JP, Fang S, Ong AM, Hatakeyama S, Weissman AM (1999) RING fingers mediate ubiquitin-conjugating enzyme (E2)-dependent ubiquitination. Proc Natl Acad Sci USA 96:11364–11369

    Article  CAS  PubMed  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 

  • Moon YH, Jung JY, Kang HG, An G (1999) Identification of a rice APETALA3 homologue by yeast two-hybrid screening. Plant Mol Biol 40:167–177

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Nambara E, Marion-Poll A (2003) ABA action and interactions in seeds. Trends Plant Sci 8:213–217

    Article  CAS  PubMed  Google Scholar 

  • Oh EY, Kang HJ, Yamaguchi S, Park JM, Lee DH, Kamiya Y, Choi GS (2009) Genome-wide analysis of genes targeted by PHYTOCHROME INTERACTING FACTOR 3-LIKE5 during seed germination in Arabidopsis. Plant Cell 21:403–419

    Article  CAS  PubMed  Google Scholar 

  • Peters JM (1998) SCF and APC: the Yin and Yang of cell cycle regulated proteolysis. Curr Opin Cell Biol 10:759–768

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez PL, Benning G, Grill E (1998) ABI2, a second protein phosphatase 2C involved in abscisic acid signal transduction in Arabidopsis. FEBS Lett 421:185–190

    Article  CAS  PubMed  Google Scholar 

  • Seol JH, Feldman RM, Zachariae W, Shevchenko A, Correll CC, Lyapina S, Chi Y, Galova M, Claypool J, Sandmeyer S, Nasmyth K, Deshaies RJ (1999) Cdc53/cullin and the essential Hrt1 RING-H2 subunit of SCF define a ubiquitin ligase module that activates the E2 enzyme Cdc34. Genes Dev 13:1614–1626

    Article  CAS  PubMed  Google Scholar 

  • Sun TP, Gubler F (2004) Molecular mechanism of gibberellin signaling in plants. Annu Rev Plant Biol 55:197–223

    Article  CAS  PubMed  Google Scholar 

  • Teng FY, Tang BL (2005) APC/C regulation of axonal growth and synaptic functions in postmitotic neurons: The Liprin-alpha connection. Cell Mol Life Sci 62:1571–1578

    Article  CAS  PubMed  Google Scholar 

  • Thomann A, Dieterle M, Genschik P (2005) Plant CULLIN-based E3s: phytohormones come first. FEBS Lett 579:3239–3245

    Article  CAS  PubMed  Google Scholar 

  • Tokunori H, Yasuo K, Tsukaho H (1999) A bZIP factor, TRAB1, interacts with VP1 and mediates abscisic acid-induced transcription. Proc Natl Acad Sci USA 96:15348–15353

    Article  Google Scholar 

  • Vieira AR, Vieira MDGGC, Fraga AC, Oliveira JA, Santos CDD (2002) Action of gibberellic acid (GA3) on dormancy and activity of α-amylase in rice seeds. Rev Bras Sementes 24:43–48

    Article  Google Scholar 

  • Vierstra RD (2003) The ubiquitin/26S proteasome pathway, the complex last chapter in the life of many plant proteins. Trends Plant Sci 8:135–142

    Article  CAS  PubMed  Google Scholar 

  • Wang Q, Guan Y, Yaorong Wu, Chen H, Chen F, Chu C (2008) Overexpression of a rice OsDREB1F gene increases salt, drought, and low temperature tolerance in both Arabidopsis and rice. Plant Mol Biol 67:589–602

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank Kyungsook An for plant transformation, Priscilla Licht for English editing, Gihwan Yi for providing the rice seeds and Jongjin Park, Sungryul Kim and Songlim Kim for helpful discussion. This work was supported, in part, by grants from the Crop Functional Genomic Center, the 21st Century Frontier Program (Grant CG1111); from the Biogreen 21 Program, Rural Development Administration (20070401-034-001-007-03-00); from the Korea Research Foundation Grant (MOEHRD, Basic Research Promotion Fund (KRF-2007-341-C00028); and from Kyoung Hee University (20100791).

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Authors and Affiliations

  1. Crop Biotech Institute & Department of Plant Molecular Systems Biotechnology, Kyung Hee University, Yongin, 446-701, Republic of Korea

    Gi-Gyeong Park & Gynheung An

  2. Department of Plant Genetic Engineering, Catholic University of Daegu, Gyeongsan, 712-702, Republic of Korea

    Gi-Gyeong Park & Sun-Nam Yu

  3. Department of Life Science, Pohang University of Science and Technology (POSTECH), Pohang, 790-784, Republic of Korea

    Jong-Jin Park & Jinmi Yoon

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  1. Gi-Gyeong Park
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Correspondence to Gynheung An.

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Supplemental Figure S1.

Alignment of OsDSG1 with AIP2, via ClustalW and BoxShade programs. Conserved protein positions and RING finger motif (∇) are marked. (PPTX 79 kb)

Supplemental Figure S2.

Seed germination rates for various rice cultivars. (PPTX 85 kb)

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Park, GG., Park, JJ., Yoon, J. et al. A RING finger E3 ligase gene, Oryza sativa Delayed Seed Germination 1 (OsDSG1), controls seed germination and stress responses in rice. Plant Mol Biol 74, 467–478 (2010). https://doi.org/10.1007/s11103-010-9687-3

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