Research Progress on Plant RING-Finger Proteins.

RING-finger proteins; adversity stress; plant development; Plant Proteins; Ubiquitin; Ubiquitin-Protein Ligases; Gene Expression Regulation, Developmental; Gene Expression Regulation, Plant; Plant Physiological Phenomena; Plant Proteins/chemistry; Plant Proteins/metabolism; RING Finger Domains; Stress, Physiological; Ubiquitin/metabolism; Ubiquitin-Protein Ligases/chemistry; Ubiquitin-Protein Ligases/metabolism; Genetics; Genetics (clinical)

Abstract :

[en] E3 ubiquitin ligases are the most expanded components of the ubiquitin proteasome system (UPS). They mediate the recognition of substrates and later transfer the ubiquitin (Ub) of the system. Really Interesting New Gene (RING) finger proteins characterized by the RING domain, which contains 40-60 residues, are thought to be E3 ubiquitin ligase. RING-finger proteins play significant roles in plant growth, stress resistance, and signal transduction. In this study, we mainly describe the structural characteristics, classifications, and subcellular localizations of RING-finger proteins, as well the physiological processes of RING-finger proteins in plant growth and development. We also summarize the functions of plant RING-finger proteins in plant stress resistance. Finally, further research on plant RING-finger proteins is suggested, thereby establishing a strong foundation for the future study of plant RING-finger proteins.

Disciplines :

Biochemistry, biophysics & molecular biology

Author, co-author :

Sun, Jinhao; Key Laboratory for Tobacco Gene Resources, Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao 266101, China ; Graduate School of Chinese Academy of Agricultural Science, Beijing 100081, China

Sun, Yuhe; Key Laboratory for Tobacco Gene Resources, Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao 266101, China

Ahmed, Rana Imtiaz; Key Laboratory for Tobacco Gene Resources, Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao 266101, China ; Graduate School of Chinese Academy of Agricultural Science, Beijing 100081, China ; Regional Agriculture Research Institute, Bahawalpur, Punjab 63100, Pakistan

Ren, Angyan ; Key Laboratory for Tobacco Gene Resources, Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao 266101, China ; Graduate School of Chinese Academy of Agricultural Science, Beijing 100081, China

Xie, Minmin ; Université de Liège - ULiège > TERRA Research Centre

Language :

English

Title :

Research Progress on Plant RING-Finger Proteins.

Publication date :

26 November 2019

Journal title :

Genes

ISSN :

2073-4425

Publisher :

MDPI AG, Basel, Switzerland

Volume :

Issue :

Pages :

973

Peer reviewed :

Peer Reviewed verified by ORBi

Additional URL :

https://www.mdpi.com/2073-4425/10/12/973/pdf

Funding text :

Funding: This work was supported by the Science Foundation for Young Scholars of the Tobacco Research Institute of the Chinese Academy of Agricultural Sciences (2018B02).This work was supported by the Science Foundation for Young Scholars of the Tobacco Research Institute of the Chinese Academy of Agricultural Sciences (2018B02).

Available on ORBi :

since 05 May 2023

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Bibliography

Glickman, M.H.; Ciechanover, A. The ubiquitin-proteasome proteolytic pathway: Destruction for the sake of construction. Physiol. Rev. 2002, 82, 373–428, doi:10.1152/physrev.00027.2001.
Borden, K.L. RING domains: Master builders of molecular scaffolds? J. Mol. Biol. 2000, 295, 1103–1112, doi:10.1006/jmbi.1999.3429.
Fleury, D.; Himanen, K.; Cnops, G.; Nelissen, H.; Boccardi, T.M.; Maere, S.; Beemster, G.T.; Neyt, P.; Anami, S.; Robles, P.; et al. The Arabidopsis thaliana homolog of yeast BRE1 has a function in cell cycle regulation during early leaf and root growth. Plant Cell 2007, 19, 417–432, doi:10.1105/tpc.106.041319.
Zeba, N.; Isbat, M.; Kwon, N.J.; Lee, M.O.; Kim, S.R.; Hong, C.B. Heat-inducible C3HC4 type RING zinc finger protein gene from Capsicum annuum enhances growth of transgenic tobacco. Planta 2009, 229, 861– 871, doi:10.1007/s00425-008-0884-0.
Yang, Y.; Fu, D.; Zhu, C.; He, Y.; Zhang, H.; Liu, T.; Li, X.; Wu, C. The RING-Finger Ubiquitin Ligase HAF1 Mediates Heading date 1 Degradation during Photoperiodic Flowering in Rice. Plant Cell 2015, 27, 2455– 2468, doi:10.1105/tpc.15.00320.
Li, W.T.; He, M.; Wang, J.; Wang, Y.P. Zinc finger protein (ZFP) in plants-A review. Plant Omics 2013, 6, 474–480, doi:10.3835/plantgenome2013.05.0018.
Kosarev, P.; Mayer, K.F.; Hardtke, C.S. Evaluation and classification of RING-finger domains encoded by the Arabidopsis genome. Genome Biol. 2002, 3, RESEARCH0016, doi:10.1186/gb-2002-3-4-research0016.
Metzger, M.B.; Pruneda, J.N.; Klevit, R.E.; Weissman, A.M. RING-type E3 ligases: Master manipulators of E2 ubiquitin-conjugating enzymes and ubiquitination. Biochim. Biophys. Acta 2014, 1843, 47–60, doi:10.1016/j.bbamcr.2013.05.026.
Stone, S.L.; Hauksdottir, H.; Troy, A.; Herschleb, J.; Kraft, E.; Callis, J. Functional analysis of the RING-type ubiquitin ligase family of Arabidopsis. Plant Physiol. 2005, 137, 13–30, doi:10.1104/pp.104.052423.
Freemont, P.S.; Hanson, I.M.; Trowsdale, J. A novel cysteine-rich sequence motif. Cell 1991, 64, 483–484, doi:10.1016/0092-8674(91)90229-r.
Borden, K.L.; Freemont, P.S. The RING finger domain: A recent example of a sequence-structure family. Curr. Opin. Struct. Biol. 1996, 6, 395–401, doi:10.1111/j.1432-1033.1993.tb18209.x.
Jimenez-Lopez, D.; Munoz-Belman, F.; Gonzalez-Prieto, J.M.; Aguilar-Hernandez, V.; Guzman, P. Repertoire of plant ring e3 ubiquitin ligases revisited: New groups counting gene families and single genes. PLoS ONE 2018, 13, e0203442, doi:10.1371/journal.pone.0203442.
Hong, J.K.; Choi, H.W.; Hwang, I.S.; Hwang, B.K. Role of a novel pathogen-induced pepper C3-H-C4 type RING-finger protein gene, CaRFPI, in disease susceptibility and osmotic stress tolerance. Plant Mol. Biol. 2007, 63, 571–588, doi:10.1007/s11103-006-9110-2.
Guzman, P. ATLs and BTLs, plant-specific and general eukaryotic structurally-related E3 ubiquitin ligases. Plant Sci. Int. J. Exp. Plant Biol. 2014, 215–216, 69–75, doi:10.1016/j.plantsci.2013.10.017.
Lim, S.D.; Yim, W.C.; Moon, J.C.; Kim, D.S.; Lee, B.M.; Jang, C.S. A gene family encoding RING finger proteins in rice: Their expansion, expression diversity, and co-expressed genes. Plant Mol. Biol. 2010, 72, 369–380, doi:10.1007/s11103-009-9576-9.
Lim, S.D.; Hwang, J.G.; Jung, C.G.; Hwang, S.G.; Moon, J.C.; Jang, C.S. Comprehensive analysis of the rice RING E3 ligase family reveals their functional diversity in response to abiotic stress. DNA Res. Int. J. Rapid Publ. Rep. Genes Genomes 2013, 20, 299–314, doi:10.1093/dnares/dst011.
Liu, Q.G.; Yang, J.L.; Wang, Z.C.; Xu, X.M.; Mao, X.L.; Li, D.D.; Hu, X.Q.; Jin, D.C.; Li, C.H. Genome-wide Classification, Identification and Expression Profile of the C3HC4-type RING Finger Gene Family in Poplar (Populus trichocarpa). Plant Mol. Biol. Rep. 2015, 33, 1740–1754, doi:10.1007/s11105-015-0870-1.
Alam, I.; Yang, Y.Q.; Wang, Y.; Zhu, M.L.; Wang, H.B.; Chalhoub, B.; Lu, Y.H. Genome-wide identification, evolution and expression analysis of RING finger protein genes in Brassica rapa. Sci. Rep. 2017, 7, doi:10.1038/Srep40690.
Yang, Y.Q.; Lu, Y.H. Genome-wide survey, characterization, and expression analysis of RING finger protein genes in Brassica oleracea and their syntenic comparison to Brassica rapa and Arabidopsis thaliana. Genome 2018, 61, 685–697, doi:10.1139/gen-2018-0046.
Li, Y.; Wu, B.; Yu, Y.; Yang, G.; Wu, C.; Zheng, C. Genome-wide analysis of the RING finger gene family in apple. Mol. Genet. Genom. MGG 2011, 286, 81–94, doi:10.1007/s00438-011-0625-0.
Yang, L.; Miao, M.; Lyu, H.; Cao, X.; Li, J.; Li, Y.; Li, Z.; Chang, W. Genome wide indentification, evolution and expression analysis of RING-finger gene family in Solanum lycopersicum. Int. J. Mol. Sci. 2019, 30, 4864, doi: 10.3390/ijms20194864.
Gao, Y.; Li, M.Y.; Zhao, J.; Zhang, Y.C.; Xie, Q.J.; Chen, D.H. Genome-wide analysis of RING finger proteins in the smallest free-living photosynthetic eukaryote Ostreococus tauri. Mar. Genom. 2016, 26, 51–61, doi:10.1016/j.margen.2015.12.008.
Chen, M.; Ni, M. RED AND FAR-RED INSENSITIVE 2, a RING-domain zinc finger protein, mediates phytochrome-controlled seedling deetiolation responses. Plant Physiol. 2006, 140, 457–465, doi:10.1104/pp.105.073163.
Liu, K.; Wang, L.; Xu, Y.; Chen, N.; Ma, Q.; Li, F.; Chong, K. Overexpression of OsCOIN, a putative cold inducible zinc finger protein, increased tolerance to chilling, salt and drought, and enhanced proline level in rice. Planta 2007, 226, 1007–1016, doi:10.1007/s00425-007-0548-5.
Xia, Z.; Liu, Q.; Wu, J.; Ding, J. ZmRFP1, the putative ortholog of SDIR1, encodes a RING-H2 E3 ubiquitin ligase and responds to drought stress in an ABA-dependent manner in maize. Gene 2012, 495, 146–153, doi:10.1016/j.gene.2011.12.028.
Lee, H.K.; Cho, S.K.; Son, O.; Xu, Z.; Hwang, I.; Kim, W.T. Drought stress-induced Rma1H1, a RING membrane-anchor E3 ubiquitin ligase homolog, regulates aquaporin levels via ubiquitination in transgenic Arabidopsis plants. Plant Cell 2009, 21, 622–641, doi:10.1105/tpc.108.061994.
Lim, S.D.; Cho, H.Y.; Park, Y.C.; Ham, D.J.; Lee, J.K.; Jang, C.S. The rice RING finger E3 ligase, OsHCI1, drives nuclear export of multiple substrate proteins and its heterogeneous overexpression enhances acquired thermotolerance. J. Exp. Bot. 2013, 64, 2899–2914, doi:10.1093/jxb/ert143.
Gao, W.; Liu, W.; Zhao, M.; Li, W.X. NERF encodes a RING E3 ligase important for drought resistance and enhances the expression of its antisense gene NFYA5 in Arabidopsis. Nucleic Acids Res. 2015, 43, 607–617, doi:10.1093/nar/gku1325.
Kim, J.H.; Lim, S.D.; Jang, C.S. Oryza sativa heat-induced RING finger protein 1 (OsHIRP1) positively regulates plant response to heat stress. Plant Mol. Biol. 2019, 99, 545–559, doi:10.1007/s11103-019-00835-9.
Ryu, M.Y.; Cho, S.K.; Kim, W.T. The Arabidopsis C3H2C3-type RING E3 ubiquitin ligase AtAIRP1 is a positive regulator of an abscisic acid-dependent response to drought stress. Plant Physiol. 2010, 154, 1983– 1997, doi:10.1104/pp.110.164749.
Yang, L.; Liu, Q.; Liu, Z.; Yang, H.; Wang, J.; Li, X.; Yang, Y. Arabidopsis C3HC4-RING finger E3 ubiquitin ligase AtAIRP4 positively regulates stress-responsive abscisic acid signaling. J. Integr. Plant Biol. 2016, 58, 67–80, doi:10.1111/jipb.12364.
Qin, X.M.; Huang, S.; Liu, Y.Q.; Bian, M.D.; Shi, W.L.; Zuo, Z.C.; Yang, Z.M. Overexpression of A RING finger ubiquitin ligase gene AtATRF1 enhances aluminium tolerance in Arabidopsis thaliana. J. Plant Biol. 2017, 60, 66–74, doi:10.1007/s12374-016-0903-9.
Berrocal-Lobo, M.; Stone, S.; Yang, X.; Antico, J.; Callis, J.; Ramonell, K.M.; Somerville, S. ATL9, a RING zinc finger protein with E3 ubiquitin ligase activity implicated in chitin-and NADPH oxidase-mediated defense responses. PLoS ONE 2010, 5, e14426.
Disch, S.; Anastasiou, E.; Sharma, V.K.; Laux, T.; Fletcher, J.C.; Lenhard, M. The E3 ubiquitin ligase BIG BROTHER controls arabidopsis organ size in a dosage-dependent manner. Curr. Biol. 2006, 16, 272–279, doi:10.1016/j.cub.2005.12.026.
Wang, X.; Chen, E.; Ge, X.; Gong, Q.; Butt, H.; Zhang, C.; Yang, Z.; Li, F.; Zhang, X. Overexpressed BRH1, a RING finger gene, alters rosette leaf shape in Arabidopsis thaliana. Sci. China Life Sci. 2018, 61, 79–87, doi:10.1007/s11427-017-9133-8.
Hardtke, C.S.; Okamoto, H.; Stoop-Myer, C.; Deng, X.W. Biochemical evidence for ubiquitin ligase activity of the Arabidopsis COP1 interacting protein 8 (CIP8). Plant J. Cell Mol. Biol. 2002, 30, 385–394, doi:10.1046/j.1365-313x.2002.01298.x.
Deng, X.W.; Caspar, T.; Quail, P.H. cop1: A regulatory locus involved in light-controlled development and gene expression in Arabidopsis. Genes Dev. 1991, 5, 1172–1182, doi:10.1101/gad.5.7.1172.
von Arnim, A.G.; Deng, X.W. Ring finger motif of Arabidopsis thaliana COP1 defines a new class of zinc-binding domain. J. Biol. Chem. 1993, 268, 19626–19631.
Qin, F.; Sakuma, Y.; Tran, L.S.; Maruyama, K.; Kidokoro, S.; Fujita, Y.; Fujita, M.; Umezawa, T.; Sawano, Y.; Miyazono, K.; et al. Arabidopsis DREB2A-interacting proteins function as RING E3 ligases and negatively regulate plant drought stress-responsive gene expression. Plant Cell 2008, 20, 1693–1707, doi:10.1105/tpc.107.057380.
Park, J.H.; Kang, C.H.; Nawkar, G.M.; Lee, E.S.; Paeng, S.K.; Chae, H.B.; Chi, Y.H.; Kim, W.Y.; Yun, D.J.; Lee, S.Y. EMR, a cytosolic-abundant ring finger E3 ligase, mediates ER-associated protein degradation in Arabidopsis. New Phytol. 2018, 220, 163–177, doi:10.1111/nph.15279.
Voiniciuc, C.; Dean, G.H.; Griffiths, J.S.; Kirchsteiger, K.; Hwang, Y.T.; Gillett, A.; Dow, G.; Western, T.L.; Estelle, M.; Haughn, G.W. Flying saucer1 is a transmembrane RING E3 ubiquitin ligase that regulates the degree of pectin methylesterification in Arabidopsis seed mucilage. Plant Cell 2013, 25, 944–959, doi:10.1105/tpc.112.107888.
Kim, J.H.; Lee, H.J.; Park, C.M. HOS1 acts as a key modulator of hypocotyl photomorphogenesis. Plant Signal. Behav. 2017, 12, e1315497, doi:10.1080/15592324.2017.1315497.
Lee, H.; Xiong, L.; Gong, Z.; Ishitani, M.; Stevenson, B.; Zhu, J.K. The Arabidopsis HOS1 gene negatively regulates cold signal transduction and encodes a RING finger protein that displays cold-regulated nucleo--cytoplasmic partitioning. Genes Dev. 2001, 15, 912–924, doi:10.1101/gad.866801.
Marino, D.; Froidure, S.; Canonne, J.; Ben Khaled, S.; Khafif, M.; Pouzet, C.; Jauneau, A.; Roby, D.; Rivas, S. Arabidopsis ubiquitin ligase MIEL1 mediates degradation of the transcription factor MYB30 weakening plant defence. Nat. Commun. 2013, 4, 1476, doi:10.1038/ncomms2479.
Chen, M.; Ni, M. RFI2, a RING-domain zinc finger protein, negatively regulates CONSTANS expression and photoperiodic flowering. Plant J. Cell Mol. Biol. 2006, 46, 823–833, doi:10.1111/j.1365-313X.2006.02740.x.
Cheng, M.C.; Hsieh, E.J.; Chen, J.H.; Chen, H.Y.; Lin, T.P. Arabidopsis RGLG2, functioning as a RING E3 ligase, interacts with AtERF53 and negatively regulates the plant drought stress response. Plant Physiol. 2012, 158, 363–375, doi:10.1104/pp.111.189738.
Zhang, Y.; Yang, C.; Li, Y.; Zheng, N.; Chen, H.; Zhao, Q.; Gao, T.; Guo, H.; Xie, Q. SDIR1 is a RING finger E3 ligase that positively regulates stress-responsive abscisic acid signaling in Arabidopsis. Plant Cell 2007, 19, 1912–1929, doi:10.1105/tpc.106.048488.
Xie, Q.; Guo, H.S.; Dallman, G.; Fang, S.; Weissman, A.M.; Chua, N.H. SINAT5 promotes ubiquitin-related degradation of NAC1 to attenuate auxin signals. Nature 2002, 419, 167–170, doi:10.1038/nature00998.
Tian, M.; Lou, L.; Liu, L.; Yu, F.; Zhao, Q.; Zhang, H.; Wu, Y.; Tang, S.; Xia, R.; Zhu, B.; et al. The RING finger E3 ligase STRF1 is involved in membrane trafficking and modulates salt-stress response in Arabidopsis thaliana. Plant J. Cell Mol. Biol. 2015, 82, 81–92, doi:10.1111/tpj.12797.
Ko, J.H.; Yang, S.H.; Han, K.H. Upregulation of an Arabidopsis RING-H2 gene, XERICO, confers drought tolerance through increased abscisic acid biosynthesis. Plant J. Cell Mol. Biol. 2006, 47, 343–355, doi:10.1111/j.1365-313X.2006.02782.x.
Liu, H.; Zhang, H.; Yang, Y.; Li, G.; Yang, Y.; Wang, X.; Basnayake, B.M.; Li, D.; Song, F. 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. 2008, 68, 17–30, doi:10.1007/s11103-008-9349-x.
Ning, Y.; Jantasuriyarat, C.; Zhao, Q.; Zhang, H.; Chen, S.; Liu, J.; Liu, L.; Tang, S.; Park, C.H.; Wang, X.; et al. The SINA E3 ligase OsDIS1 negatively regulates drought response in rice. Plant Physiol. 2011, 157, 242– 255, doi:10.1104/pp.111.180893.
Park, G.G.; Park, J.J.; Yoon, J.; Yu, S.N.; An, G. A RING finger E3 ligase gene, Oryza sativa Delayed Seed Germination 1 (OsDSG1), controls seed germination and stress responses in rice. Plant Mol. Biol. 2010, 74, 467–478, doi:10.1007/s11103-010-9687-3.
Hsu, K.H.; Liu, C.C.; Wu, S.J.; Kuo, Y.Y.; Lu, C.A.; Wu, C.R.; Lian, P.J.; Hong, C.Y.; Ke, Y.T.; Huang, J.H.; et al. Expression of a gene encoding a rice RING zinc-finger protein, OsRZFP34, enhances stomata opening. Plant Mol. Biol. 2014, 86, 125–137, doi:10.1007/s11103-014-0217-6.
Park, Y.C.; Chapagain, S.; Jang, C.S. The microtubule-associated RING finger protein 1 (OsMAR1) acts as a negative regulator for salt-stress response through the regulation of OCPI2 (O. sativa chymotrypsin protease inhibitor 2). Planta 2018, 247, 875–886, doi:10.1007/s00425-017-2834-1.
Bae, H.; Kim, S.K.; Cho, S.K.; Kang, B.G.; Kim, W.T. Overexpression of OsRDCP1, a rice RING domain-containing E3 ubiquitin ligase, increased tolerance to drought stress in rice (Oryza sativa L.). Plant Sci. Int. J. Exp. Plant Biol. 2011, 180, 775–782, doi:10.1016/j.plantsci.2011.02.008.
Liu, J.; Zhang, C.; Wei, C.; Liu, X.; Wang, M.; Yu, F.; Xie, Q.; Tu, J. The RING Finger Ubiquitin E3 Ligase OsHTAS Enhances Heat Tolerance by Promoting H2O2-Induced Stomatal Closure in Rice. Plant Physiol. 2016, 170, 429–443, doi:10.1104/pp.15.00879.
Park, Y.C.; Chapagain, S.; Jang, C.S. A Negative Regulator in Response to Salinity in Rice: Oryza sativa Salt-, ABA-and Drought-Induced RING Finger Protein 1 (OsSADR1). Plant Cell Physiol. 2018, 59, 575–589, doi:10.1093/pcp/pcy009.
Park, Y.C.; Lim, S.D.; Moon, J.C.; Jang, C.S. A rice really interesting new gene H2-type E3 ligase, OsSIRH2-14, enhances salinity tolerance via ubiquitin/26S proteasome-mediated degradation of salt-related proteins. Plant Cell Environ. 2019, 42, 3061–3076, doi:10.1111/pce.13619.
Hwang, S.G.; Kim, J.J.; Lim, S.D.; Park, Y.C.; Moon, J.C.; Jang, C.S. Molecular dissection of Oryza sativa salt-induced RING Finger Protein 1 (OsSIRP1): Possible involvement in the sensitivity response to salinity stress. Physiol. Plant. 2016, 158, 168–179, doi:10.1111/ppl.12459.
Lim, C.W.; Baek, W.; Lee, S.C. The Pepper RING-Type E3 Ligase CaAIRF1 Regulates ABA and Drought Signaling via CaADIP1 Protein Phosphatase Degradation. Plant Physiol. 2017, 173, 2323–2339, doi:10.1104/pp.16.01817.
Joo, H.; Lim, C.W.; Lee, S.C. A pepper RING-type E3 ligase, CaASRF1, plays a positive role in drought tolerance via modulation of CaAIBZ1 stability. Plant J. Cell Mol. Biol. 2019, 98, 5–18, doi:10.1111/tpj.14191.
Lim, C.W.; Baek, W.; Lee, S.C. Roles of pepper bZIP protein CaDILZ1 and its interacting partner RING-type E3 ligase CaDSR1 in modulation of drought tolerance. Plant J. Cell Mol. Biol. 2018, 96, 452–467, doi:10.1111/tpj.14046.
Brugiere, N.; Zhang, W.; Xu, Q.; Scolaro, E.J.; Lu, C.; Kahsay, R.Y.; Kise, R.; Trecker, L.; Williams, R.W.; Hakimi, S.; et al. Overexpression of RING Domain E3 Ligase ZmXerico1 Confers Drought Tolerance through Regulation of ABA Homeostasis. Plant Physiol. 2017, 175, 1350–1369, doi:10.1104/pp.17.01072.
Yu, Y.; Xu, W.; Wang, J.; Wang, L.; Yao, W.; Yang, Y.; Xu, Y.; Ma, F.; Du, Y.; Wang, Y. The Chinese wild grapevine (Vitis pseudoreticulata) E3 ubiquitin ligase Erysiphe necator-induced RING finger protein 1 (EIRP1) activates plant defense responses by inducing proteolysis of the VpWRKY11 transcription factor. New Phytol. 2013, 200, 834–846.
Wang, L.; Xie, X.; Yao, W.; Wang, J.; Ma, F.; Wang, C.; Yang, Y.; Tong, W.; Zhang, J.; Xu, Y.; et al. RING-H2-type E3 gene VpRH2 from Vitis pseudoreticulata improves resistance to powdery mildew by interacting with VpGRP2A. J. Exp. Bot. 2017, 68, 1669–1687.
Liu, Y.; Li, L.; Zhang, L.; Lv, Q.; Zhao, Y.; Li, X. Isolation and identification of wheat gene TaDIS1 encoding a RING finger domain protein, which negatively regulates drought stress tolerance in transgenic Arabidopsis. Plant Sci. Int. J. Exp. Plant Biol. 2018, 275, 49–59, doi:10.1016/j.plantsci.2018.07.017.
Kam, J.; Gresshoff, P.; Shorter, R.; Xue, G.P. 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. 2007, 173, 650–659, doi:10.1016/j.plantsci.2007.09.001.
Yang, X.; Sun, C.; Hu, Y.; Lin, Z. Molecular cloning and characterization of a gene encoding RING zinc finger ankyrin protein from drought-tolerant Artemisia desertorum. J. Biosci. 2008, 33, 103–112, doi:10.1007/s12038-008-0026-7.
Jung, Y.J.; Lee, I.H.; Nou, I.S.; Lee, K.D.; Rashotte, A.M.; Kang, K.K. BrRZFP1 a Brassica rapa C3HC4-type RING zinc finger protein involved in cold, salt and dehydration stress. Plant Biol. 2013, 15, 274–283, doi:10.1111/j.1438-8677.2012.00631.x.
Zhang, X.; Wang, N.; Chen, P.; Gao, M.; Liu, J.; Wang, Y.; Zhao, T.; Li, Y.; Gai, J. Overexpression of a soybean ariadne-like ubiquitin ligase gene GmARI1 enhances aluminum tolerance in Arabidopsis. PLoS ONE 2014, 9, e111120, doi:10.1371/journal.pone.0111120.
Cai, K.; Yin, J.; Chao, H.; Ren, Y.; Jin, L.; Cao, Y.; Duanmu, D.; Zhang, Z. A C3HC4-type RING finger protein regulates rhizobial infection and nodule organogenesis in Lotus japonicus. J. Integr. Plant Biol. 2018, 60, 878–896, doi:10.1111/jipb.12703.
Karlowski, W.M.; Hirsch, A.M. The over-expression of an alfalfa RING-H2 gene induces pleiotropic effects on plant growth and development. Plant Mol. Biol. 2003, 52, 121–133, doi:10.1023/a:1023916701669.
dos Reis, S.P.; Tavares Lde, S.; Costa Cde, N.; Brigida, A.B.; de Souza, C.R. Molecular cloning and characterization of a novel RING zinc-finger protein gene up-regulated under in vitro salt stress in cassava. Mol. Biol. Rep. 2012, 39, 6513–6519, doi:10.1007/s11033-012-1479-1.
Wu, W.X.; Cheng, Z.W.; Liu, M.J.; Yang, X.F.; Qiu, D.W. C3HC4-Type RING Finger Protein NbZFP1 Is Involved in Growth and Fruit Development in Nicotiana benthamiana. PLoS ONE 2014, 9, doi:10.1371/journal.pone.0099352.
Xia, Z.; Su, X.; Liu, J.; Wang, M. The RING-H2 finger gene 1 (RHF1) encodes an E3 ubiquitin ligase and participates in drought stress response in Nicotiana tabacum. Genetica 2013, 141, 11–21, doi:10.1007/s10709-013-9702-0.
Qi, S.L.; Lin, Q.F.; Zhu, H.S.; Gao, F.H.; Zhang, W.H.; Hua, X.J. The RING Finger E3 Ligase SpRing is a Positive Regulator of Salt Stress Signaling in Salt-Tolerant Wild Tomato Species. Plant Cell Physiol. 2016, 57, 528–539, doi:10.1093/pcp/pcw006.
Dong, C.H.; Agarwal, M.; Zhang, Y.; Xie, Q.; Zhu, J.K. 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 2006, 103, 8281–8286, doi:10.1073/pnas.0602874103.
Shinozaki, K.; Yamaguchi-Shinozaki, K. Gene Expression and Signal Transduction in Water-Stress Response. Plant Physiol. 1997, 115, 327–334.
Finkelstein, R.R.; Gampala, S.S.; Rock, C.D. Abscisic acid signaling in seeds and seedlings. Plant Cell 2002, 14, S15–S45.
Yamaguchi-Shinozaki, K.; Shinozaki, K. Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu. Rev. Plant Biol. 2006, 57, 781–803.