Abstract
The proteins harboring RING finger motif(s) have been shown to mediate protein–protein interactions that are relevant to a variety of cellular processes. In an effort to elucidate the evolutionary dynamics of the rice RING finger protein family, we have attempted to determine their genomic locations, expression diversity, and co-expressed genes via in silico analysis and semi-quantitative RT–PCR. A total of 425 retrieved genes appear to be distributed over all 12 of the chromosomes of rice with different distributions, and are reflective of the evolutionary dynamics of the rice genome. A genome-wide dataset harboring 155 gene expression omnibus sample plates evidenced some degree of differential evolutionary fates between members of RING-H2 and RING-HC types. Additionally, responses to abiotic stresses, such as salinity and drought, demonstrated that some degree of expression diversity existed between members of the RING finger protein genes. Interestingly, we determined that one RING-H2 finger protein gene (Os04g51400) manifested striking differences in expression patterns in response to abiotic stresses between leaf and culm-node tissues, further revealing responses highly similar to the majority of randomly selected co-expressed genes. The gene network of genes co-expressed with Os04g51400 may suggest some role in the salt response of the gene. These findings may shed further light on the evolutionary dynamics and molecular functional diversity of these proteins in complex cellular regulations.
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References
Baumberger N, Doesseger B, Guyot R, Diet A, Parsons RL, Clark MA, Simmons MP, Bedinger P, Goff SA, Ringli C, Keller B (2003) Whole-genome comparison of leucine-rich repeat extensions in Arabidopsis and rice. A conserved family of cell wall proteins form a vegetative and a reproductive clade. Plant Physiol 131:1313–1326
Borden KL, Boddy MN, Lally J, O’Reilly NJ, Martin S, Howe KL (1995) The solution structure of the RING finger domain from the acute promyelocytic leukaemia proto-oncoprotein PML. EMBO J 14:1532–1541
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 seedling development. Plant Physiol 150:463–481
Buljan M, Bateman A (2009) The evolution of protein domain families. Biochem Soc Trans 37:751–755
Chapman BA, Bowers JE, Feltus FA, Paterson AH (2006) Buffering of crucial functions by paleologous duplicate genes may contribute cyclicality to angiosperm genome duplication. Proc Natl Acad Sci USA 103:2730–2735
Cooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: a sequence log generator. Genome Res 14:1188–1190
Deng XW, Matsui M, Wei N, Wagner D, Chu AM, Feldmann KA, Quail PH (1992) COP1, an Arabidopsis regulatory gene, encodes a protein with both a zinc-binding motif and a G beta homologus domain. Cell 71:791–801
Deng L, Wang C, Spencer E, Yang L, Braun A, You J, Slaughter C, Pickart C, Chen ZJ (2000) Activation of the IkappaB kinase complex by TRAF6 requires a dimeric ubiquitin-conjugating enzyme complex and a unique polyubiquitin chain. Cell 103:351–361
Feuerstein R, Wang X, Song D, Cooke NE, Liebhaber SA (1994) The LIM/double zinc-finger motif functions as a protein dimerization domain. Proc Natl Acad Sci USA 91:10655–10659
Glickman MH, Ciechanover A (2002) The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol Rev 82:373–428
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acides Symp Ser 41:95–98
Hashizume R, Fukuda M, Maeda I, Nishikawa H, Oyake D, Yabuki Y, Ogata H, Ohta T (2001) The RING heterodimer BRCA1-BARD1 is a ubiquitin ligase inactivated by a breast cancer-derived mutation. J Biol Chem 276:14537–14540
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
Indorf M, Cordero J, Neuhaus G, Rodríguez-Franco M (2007) Salt tolerance (STO), a stress-related protein, has a major role in light signaling. Plant J 51:563–574
Jackson PK, Eldridge AG, Freed E, Furstenthal L, Hsu JY, Kaiser BK, Reimann JDR (2000) The lore of the RINGs: substrate recognition and catalysis by ubiquitin ligases. Trends Cell Biol 10:429–439
Jain M, Nijhawan A, Arora R, Agrwal P, Ray S, Sharma P, Kapoor S, Tyagi AK, Khurana JP (2007) F-box proteins in rice. Geome-wide analysis, classification, temporal and spatial gene expression during panicle and seed development, and regulation by light and abiotic stress. Plant Physiol 143:1467–1483
Jang CS, Jung JH, Yim WC, Lee B-M, Seo YW, Kim W (2007) Divergence of genes encoding non-specific lipid transfer proteins in the Poaceae family. Mol Cells 24:215–223
Jang CS, Yim WC, Moon SC, Jung JH, Lee TG, Lim SD, Cho SH, Kim W, Seo YW, Lee BM (2008) Evolution of non-specific lipid transfer protein (nsLTP) genes in the Poaceae family: their duplication and diversity. Mol Genet Genomics 279:481–497
Kaiser P, Flick K, Wittenberg C, Reed SI (2000) Regulation of transcription by Ubiquitination without proteolysis: Cdc34/SCF(Met30)-mediated inactivation of the transcription factor Met4. Cell 102:303–314
Keiko UT, Timothy W, McNellis TW, Deng XW (1998) Functional dissection of Arabidopsis COP1 reveals specific roles of its three structural modules in light control of seedling development. EMBO J 19:5577–5587
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
Koiwai H, Tagiri A, Katoh S, Katoh E, Ichikawa H, Minami E, Nishizawa Y (2007) RING-H2 type ubiqutin ligase EL5 is involved in root development through the maintenance of cell viability in rice. Plant J 51:92–104
Kosarev P, Mayer KF, Hardtke CS (2002) Evaluation and classification of RING-finger domains encoded by the Arabidopsis genome. Genome Biol 3: RESEARCH0016
Krzywinski MI, Schein JE, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA (2009) Circos : an information aesthetic for comparative genomics. Genome Res (in press)
Kuras L, Rouillon A, Lee T, Barbey R, Tyers M, Thomas D (2002) Dual regulation of the met4 transcription factor by ubiquitin-dependent degradation and inhibition of promoter recruitment. Mol Cell 10:69–80
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947
Linares LK, Hengstermann A, Ciechanover A, Muller S, Scheffner M (2003) HdmX stimulates Hdm2-mediated ubiquitination and degradation of p53. Proc Natl Acad Sci USA 100:12009–12014
Lippuner V, Cyert MS, Gasser CS (1996) Two classes of plant cDNA clones differentially complement yeast calcineurin mutants and increase salt tolerance of wild-type yeast. J Biol Chem 271:12859–12866
Liu Y, Koornneef M, Soppe JJ (2007) 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
Liu H, Zhang H, Yang Y, Li G, Yang Y, Wang X, Basnayake BMVS, 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 Mol Biol 68:17–30
Lovering R, Hanson IM, Borden KL, Martin S, O’Reilly NJ, Evan GI, Raman 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
McNellis TW, von Arnim AG, Deng XW (1994) Overexpression of Arabidopsis COP1 results in partial suppression of light-mediated development: evidence for a light-inactivable repressor of photomorphogenesis. Plant Cell 6:1391–1400
McNellis TW, Torii KU, Deng XW (1996) Expression of an N-terminal fragment of COP1 confers a dominant-negative effect on light-regulated seedling development in Arabidopsis. Plant Cell 8:1491–1503
Nagaoka S, Takano T (2003) Salt tolerance-related protein STO binds to a Myb transcription factor homologue and confers salt tolerance in Arabidopsis. J Exp Bot 54:2231–2237
Nijhawan A, Jain M, Tyagi AK, Khurana JP (2008) Genomic survey and gene expression analysis of the basic leucine zipper transcription factor family in rice. Plant Physiol 146:333–350
Ohno S (1970) Evolution by gene duplication. Springer, New York
Paterson AH, Bowers JE, Chapman BA (2004) Ancient polyploidization prediating divergence of the cereals, and its consequences for comparative genomics. Proc Natl Acad Sci USA 101:9903–9908
Pavletich N, Pabo C (1991) Zinc finger-DNA recognition: crystal structure of a Zif268-DNA complex at 2.1 A. Science 252:809–817
Pevny L, Simon MC, Robertson E, Klein WH, Tsai SF, D’Agati V (1991) Erythroid differentiation in chimaeric mice blocked by a targeted mutation in the gene for transcription factor GATA-1. Nature 349:257–260
Qin F, Sakuma Y, Phan Tran L-S, 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
Quevillon E, Silventoinen V, Pillai S, Harte N, Mulder N, Apweiler R, Lopez R (2008) InterProScan: protein domains identifier. Nucleic Acids Res 33:116–120
Rice chromosomes 11, 12 sequencing consortia (2005) The sequence of rice chromosomes 11 and 12, rich in disease resistance genes and recent gene duplications. BMC Biol 3:20. doi:10.1186/174-7007-8-20
Ruqiang X, Qingshun QL (2003) A RING-H2 zinc-finger protein gene RIE1 is essential for seed development in Arabidopsis. Plant Mol Biol 53:37–50
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
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 chloroplast. Proc Natl Acad Sci 104:1069–1074
Sémon M, Wolfe KH (2007) Consequences of genome duplication. Curr Opin Genet Dev 17:505–512
Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504
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
Stuart JM, Segal E, Koller D, Kim SK (2003) A gene-coexpression network for global discovery of conserved genetic modules. Science 302:249–255
Takatsuji H (1998) Zinc-finger transcription factors in plants. Cell Mol Life Sci 54:582–596
von Arnim AG, Deng XW (1993) Ring finger motif of Arabidopsis thaliana COP1 defines a new class of zinc-binding domain. J Biol Chem 268:19626–19631
Wang H, Wang L, Erdjument-Bromage H, Vidal M, Tempst P, Jones RS, Zhang Y (2004) Role of histone H2A ubiquitination in Polycomb silencing. Nature 431:873–878
Wang D, Guo Y, Wu C, Yang G, Li Y, Zheng C (2008) Genome-wide analysis of CCCH zinc finger family in Arabidopsis and rice. BMC genomic 9:44. doi:10.1186/1471-2164-9-44
Yim WC, Jang CS (2007) Discovery of gene regulatory networks via in silico analysis and their application in abiotic stress responses. Korean J Breed Sci 39:464–472
Yim WC, Lee B-M, Jang CS (2009) Expression diversity and evolutionary dynamics of rice duplicate genes. Mol Genet Genomics 281:483–493
Yu J, Wang J, Lin W, Li S, Li H et al (2005) The genomes of Oryza sativa: a history of duplications. PLoS Biol 3(2):e38
Zeba N, Isbat M, Kwon N-J, Lee MO, Kim SR, Hong CB (2009) Heat-inducible C3HC4 type RING zinc finger protein gene from Capsicum annuum enhances growth of transgenic tobacco. Planta (in press) doi: 10.1007/s00425-008-0884-0
Zhang S, Chen C, Li L, Meng L, Singh J, Jiang N, Deng X-W, He Z-H, Lemaux PG (2005) Evolutionary expansion, gene structure, and expression in the rice wall-associated kinase gene family. Plant Physiol 139:1107–1124
Acknowledgments
This work was supported by a grant from the BioGreen21 Program (no. 20080401034015), Rural Development Administration, Republic of Korea and a research program of Oriental Bio-herb Research Institute, Kangwon National University to CSJ and a research program of Dongguk University to BML.
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11103_2009_9576_MOESM4_ESM.png
Supplemental Fig. 1 Phylogenetic relationship among the 425 RING finger protein genes in rice. The phylogenetic tree was constructed via the neighbor-joining algorithm with 1,000 bootstrap replicates. (PNG 902 kb)
11103_2009_9576_MOESM5_ESM.pptx
Supplemental Fig. 2 Expression profiles of 369 RING finger protein genes in rice. Clustering analysis was conducted using the average linkage hierarchical clustering via uncentered Pearson’s correlation. The expression values of each RING finger protein genes were retrieved from 155 GSM samples of the Affymetrix GeneChip rice genome array. (PPTX 521 kb)
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Lim, S.D., Yim, W.C., Moon, JC. et al. A gene family encoding RING finger proteins in rice: their expansion, expression diversity, and co-expressed genes. Plant Mol Biol 72, 369–380 (2010). https://doi.org/10.1007/s11103-009-9576-9
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DOI: https://doi.org/10.1007/s11103-009-9576-9