水稻E3泛素连接酶的功能研究进展

doi:10.16819/j.1001-7216.2026.250616

摘要/Abstract

摘要：

E3泛素连接酶决定底物特异性，在泛素化反应中发挥重要作用。水稻是重要的粮食作物之一，近年来的研究显示E3泛素连接酶参与调控水稻中的多方面生物学进程。本文总结了水稻中已报道的E3泛素连接酶基因，阐述了E3泛素连接酶调控水稻生长发育和胁迫响应的分子机制，并对E3泛素连接酶的进一步研究进行展望，旨在为水稻的高产及抗逆育种提供理论依据和实践指导。

关键词: 水稻, E3泛素连接酶, 生长发育, 胁迫响应

Abstract:

E3 ubiquitin ligases determine substrate specificity and therefore play important roles in the ubiquitination process. Rice is one of the most important cereal crops, and recent studies have shown that E3 ubiquitin ligases are involved in regulating various biological processes in rice. This manuscript summarizes the reported E3 ubiquitin ligase genes in rice, elucidates the molecular mechanisms of E3 ubiquitin ligases in regulating rice growth, development, and stress response, and outlines further research prospects on E3 ubiquitin ligases, aiming to provide a theoretical basis and practical guidance for high-yield and stress-resistant breeding of rice.

Key words: rice, E3 ubiquitin ligase, growth and development, stress response

郝栖贤, 周坤能, 云鹏, 张彩娟, 夏加发, 李泽福. 水稻E3泛素连接酶的功能研究进展[J]. 中国水稻科学, 2026, 40(6): 705-725.

HAO Qixian, ZHOU Kunneng, YUN Peng, ZHANG Caijuan, XIA Jiafa, LI Zefu. Research Progress of the Functions of E3 Ubiquitin Ligases in Rice[J]. Chinese Journal OF Rice Science, 2026, 40(6): 705-725.

图/表 10

参考文献 114

[1]	Morreale F E, Walden H. Types of ubiquitin ligases[J]. Cell, 2016, 165(1): 248-248.e1.
[2]	Zheng N, Shabek N. Ubiquitin ligases: Structure, function, and regulation[J]. Annual Review of Biochemistry, 2017, 86: 129-157.
[3]	吴比, 胡伟, 邢永忠. 中国水稻遗传育种历程与展望[J]. 遗传, 2018, 40(10): 841-857.
	Wu B, Hu W, Xing Y Z. The history and prospect of rice genetic breeding in China[J]. Hereditas (Beijing), 2018, 40(10): 841-857. (in Chinese with English abstract)
[4]	Berndsen C E, Wolberger C. New insights into ubiquitin E3 ligase mechanism[J]. Nature Structural & Molecular Biology, 2014, 21(4): 301-307.
[5]	Zhou B, Zeng L. Conventional and unconventional ubiquitination in plant immunity[J]. Molecular Plant Pathology, 2017, 18(9): 1313-1330.
[6]	Vijay-Kumar S, Bugg C E, Cook W J. Structure of ubiquitin refined at 1.8 Å resolution[J]. Journal of Molecular Biology, 1987, 194(3): 531-544.
[7]	Passmore L A, Barford D. Getting into position: The catalytic mechanisms of protein ubiquitylation[J]. The Biochemical Journal, 2004, 379(Pt 3): 513-525.
[8]	Vierstra R D. The ubiquitin-26S proteasome system at the nexus of plant biology[J]. Nature Reviews Molecular Cell Biology, 2009, 10(6): 385-397.
[9]	Vierstra R D. The expanding universe of ubiquitin and ubiquitin-like modifiers[J]. Plant Physiology, 2012, 160(1): 2-14.
[10]	Du Z, Zhou X, Li L, Su Z. plantsUPS: A database of plants' Ubiquitin Proteasome System[J]. BMC Genomics, 2009, 10(1): 227.
[11]	Toma-Fukai S, Shimizu T. Structural diversity of ubiquitin E3 ligase[J]. Molecules, 2021, 26(21): 6682.
[12]	Freemont P S, Hanson I M, Trowsdale J. A novel cysteine-rich sequence motif[J]. Cell, 1991, 64(3): 483-484.
[13]	Stone S L, Hauksdóttir H, Troy A, Herschleb J, Kraft E, Callis J. Functional analysis of the RING-type ubiquitin ligase family of Arabidopsis[J]. Plant Physiology, 2005, 137(1): 13-30.
[14]	Ohi M D, Vander Kooi C W, Rosenberg J A, Chazin W J, Gould K L. Structural insights into the U-box, a domain associated with multi-ubiquitination[J]. Nature Structural & Molecular Biology, 2003, 10(4): 250-255.
[15]	Ban Z, Estelle M. CUL3 E3 ligases in plant development and environmental response[J]. Nature Plants, 2021, 7(1): 6-16.
[16]	Lan W, Miao Y. New aspects of HECT-E3 ligases in cell senescence and cell death of plants[J]. Plants, 2019, 8(11): 483.
[17]	Callis J. The ubiquitination machinery of the ubiquitin system[J]. The Arabidopsis Book, 2014, 12: e0174.
[18]	Song X J, Huang W, Shi M, Zhu M Z, Lin H X. A QTL for rice grain width and weight encodes a previously unknown RING-type E3 ubiquitin ligase[J]. Nature Genetics, 2007, 39(5): 623-630.
[19]	Hao J, Wang D, Wu Y, Huang K, Duan P, Li N, Xu R, Zeng D, Dong G, Zhang B, Zhang L, Inzé D, Qian Q, Li Y. The GW2-WG1-OsbZIP47 pathway controls grain size and weight in rice[J]. Molecular Plant, 2021, 14(8): 1266-1280.
[20]	Choi B S, Kim Y J, Markkandan K, Koo Y J, Song J T, Seo H S. GW2 functions as an E3 ubiquitin ligase for rice expansin-like 1[J]. International Journal of Molecular Sciences, 2018, 19(7): 1904.
[21]	Sun S, Wang L, Mao H, Shao L, Li X, Xiao J, Ouyang Y, Zhang Q. A G-protein pathway determines grain size in rice[J]. Nature Communications, 2018, 9: 851.
[22]	Yang W, Wu K, Wang B, Liu H, Guo S, Guo X, Luo W, Sun S, Ouyang Y, Fu X, Chong K, Zhang Q, Xu Y. The RING E3 ligase CLG1 targets GS3 for degradation via the endosome pathway to determine grain size in rice[J]. Molecular Plant, 2021, 14(10): 1699-1713.
[23]	Bai C, Wang G J, Feng X H, Gao Q, Wang W Q, Xu R, Guo S J, Shen S Y, Ma M, Lin W H, Liu C M, Li Y, Song X J. OsMAPK6 phosphorylation and CLG1 ubiquitylation of GW6a non-additively enhance rice grain size through stabilization of the substrate[J]. Nature Communications, 2024, 15: 4300.
[24]	Tong H, Chu C. Brassinosteroid signaling and application in rice[J]. Journal of Genetics and Genomics, 2012, 39(1): 3-9.
[25]	Liu D, Zhang X, Li Q, Xiao Y, Zhang G, Yin W, Niu M, Meng W, Dong N, Liu J, Yang Y, Xie Q, Chu C, Tong H. The U-box ubiquitin ligase TUD1 promotes brassinosteroid-induced GSK2 degradation in rice[J]. Plant Communications, 2023, 4(2): 100450.
[26]	Zhu X, Zhang S, Chen Y, Mou C, Huang Y, Liu X, Ji J, Yu J, Hao Q, Yang C, Cai M, Nguyen T, Song W, Wang P, Dong H, Liu S, Jiang L, Wan J. Decreased grain size1, a C₃HC₄-type RING protein, influences grain size in rice (Oryza sativa L.)[J]. Plant Molecular Biology, 2021, 105(4/5): 405-417.
[27]	Li J, Zhang B, Duan P, Yan L, Yu H, Zhang L, Li N, Zheng L, Chai T, Xu R, Li Y. An endoplasmic reticulum-associated degradation-related E2-E3 enzyme pair controls grain size and weight through the brassinosteroid signaling pathway in rice[J]. The Plant Cell, 2023, 35(3): 1076-1091.
[28]	Hao Q, Zhu X, Huang Y, Song J, Mou C, Zhang F, Miao R, Ma T, Wang P, Zhu Z, Chen C, Tong Q, Hu C, Chen Y, Dong H, Liu X, Jiang L, Wan J. E3 ligase decreased grain size 1 promotes degradation of a g-protein subunit and positively regulates grain size in rice[J]. Plant Physiology, 2024, 196(2): 948-960.
[29]	Huang L, Hua K, Xu R, Zeng D, Wang R, Dong G, Zhang G, Lu X, Fang N, Wang D, Duan P, Zhang B, Liu Z, Li N, Luo Y, Qian Q, Yao S, Li Y. The LARGE2-APO1/APO2 regulatory module controls panicle size and grain number in rice[J]. The Plant Cell, 2021, 33(4): 1212-1228.
[30]	Yue Z, Wang Z, Yao Y, Liang Y, Li J, Yin K, Li R, Li Y, Ouyang Y, Xiong L, Hu H. Variation in width of leaf and grain contributes to grain and leaf size by controlling large2 stability in rice[J]. The Plant Cell, 2024, 36(9): 3201-3218.
[31]	杨得正, 付惠仙, 肖素勤, 雷凌云, 李天时, 程在全, 刘丽. 水稻株型的遗传基础与分子调控机理研究进展[J]. 生物技术进展, 2024, 14(3): 349-359.
	Yang D Z, Fu H X, Xiao S Q, Lei L Y, Li T S, Cheng Z Q, Liu L. Research progress on genetic basis and molecular regulation mechanism of rice plant architecture[J]. Current Biotechnology, 2024, 14(3): 349-359. (in Chinese with English abstract)
[32]	Jiao Y, Wang Y, Xue D, Wang J, Yan M, Liu G, Dong G, Zeng D, Lu Z, Zhu X, Qian Q, Li J. Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice[J]. Nature Genetics, 2010, 42(6): 541-544.
[33]	Lu Z, Yu H, Xiong G, Wang J, Jiao Y, Liu G, Jing Y, Meng X, Hu X, Qian Q, Fu X, Wang Y, Li J. Genome-wide binding analysis of the transcription activator ideal plant architecture1 reveals a complex network regulating rice plant architecture[J]. The Plant Cell, 2013, 25(10): 3743-3759.
[34]	Wang J, Yu H, Xiong G, Lu Z, Jiao Y, Meng X, Liu G, Chen X, Wang Y, Li J. Tissue-specific ubiquitination by IPA1 INTERACTING PROTEIN1 modulates IPA1 protein levels to regulate plant architecture in rice[J]. The Plant Cell, 2017, 29(4): 697-707.
[35]	Zhao J, Wang T, Wang M, Liu Y, Yuan S, Gao Y, Yin L, Sun W, Peng L, Zhang W, Wan J, Li X. DWARF3 participates in an SCF complex and associates with DWARF14 to suppress rice shoot branching[J]. Plant and Cell Physiology, 2014, 55(6): 1096-1109.
[36]	Zhou F, Lin Q, Zhu L, Ren Y, Zhou K, Shabek N, Wu F, Mao H, Dong W, Gan L, Ma W, Gao H, Chen J, Yang C, Wang D, Tan J, Zhang X, Guo X, Wang J, Jiang L, Liu X, Chen W, Chu J, Yan C, Ueno K, Ito S, Asami T, Cheng Z, Wang J, Lei C, Zhai H, Wu C, Wang H, Zheng N, Wan J. D14-SCF(D3)-dependent degradation of D53 regulates strigolactone signalling[J]. Nature, 2013, 504(7480): 406-410.
[37]	Ueguchi-Tanaka M, Ashikari M, Nakajima M, Itoh H, Katoh E, Kobayashi M, Chow T Y, Hsing Y C, Kitano H, Yamaguchi I, Matsuoka M. GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin[J]. Nature, 2005, 437(7059): 693-698.
[38]	Sasaki A, Itoh H, Gomi K, Ueguchi-Tanaka M, Ishiyama K, Kobayashi M, Jeong D H, An G, Kitano H, Ashikari M, Matsuoka M. Accumulation of phosphorylated repressor for gibberellin signaling in an F-box mutant[J]. Science, 2003, 299(5614): 1896-1898.
[39]	Liu F, Wang P, Zhang X, Li X, Yan X, Fu D, Wu G. The genetic and molecular basis of crop height based on a rice model[J]. Planta, 2018, 247(1): 1-26.
[40]	Lin Q, Wang D, Dong H, Gu S, Cheng Z, Gong J, Qin R, Jiang L, Li G, Wang J L, Wu F, Guo X, Zhang X, Lei C, Wang H, Wan J. Rice APC/CTE controls tillering by mediating the degradation of MONOCULM 1[J]. Nature Communications, 2012, 3: 752.
[41]	Zhou S, Zhu S, Cui S, Hou H, Wu H, Hao B, Cai L, Xu Z, Liu L, Jiang L, Wang H, Wan J. Transcriptional and post-transcriptional regulation of heading date in rice[J]. New Phytologist, 2021, 230(3): 943-956.
[42]	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[J]. The Plant Cell, 2015, 27(9): 2455-2468.
[43]	Yang Y, Peng Q, Chen G X, Li X H, Wu C Y. OsELF3 is involved in circadian clock regulation for promoting flowering under long-day conditions in rice[J]. Molecular Plant, 2013, 6(1): 202-215.
[44]	Zhu C, Peng Q, Fu D, Zhuang D, Yu Y, Duan M, Xie W, Cai Y, Ouyang Y, Lian X, Wu C. The E3 ubiquitin ligase HAF1 modulates circadian accumulation of EARLY FLOWERING3 to control heading date in rice under long-day conditions[J]. The Plant Cell, 2018, 30(10): 2352-2367.
[45]	Du Y, He W, Deng C, Chen X, Gou L, Zhu F, Guo W, Zhang J, Wang T. Flowering-related RING protein 1 (FRRP1) regulates flowering time and yield potential by affecting histone H2B monoubiquitination in rice (Oryza sativa)[J]. PLoS One, 2016, 11(3): e0150458.
[46]	Jiang P, Wang S, Zheng H, Li H, Zhang F, Su Y, Xu Z, Lin H, Qian Q, Ding Y. SIP1 participates in regulation of flowering time in rice by recruiting OsTrx1 to Ehd1[J]. New Phytologist, 2018, 219(1): 422-435.
[47]	Xu Z, Li E, Xue G, Zhang C, Yang Y, Ding Y. OsHUB2 inhibits function of OsTrx1 in heading date in rice[J]. The Plant Journal, 2022, 110(6): 1670-1680.
[48]	Zeng L R, Qu S, Bordeos A, Yang C, Baraoidan M, Yan H, Xie Q, Nahm B H, Leung H, Wang G L. Spotted leaf11, a negative regulator of plant cell death and defense, encodes a U-box/Armadillo repeat protein endowed with E3 ubiquitin ligase activity[J]. The Plant Cell, 2004, 16(10): 2795-2808.
[49]	Vega-Sánchez M E, Zeng L, Chen S, Leung H, Wang G L. SPIN1, a K homology domain protein negatively regulated and ubiquitinated by the E3 ubiquitin ligase SPL11, is involved in flowering time control in rice[J]. The Plant Cell, 2008, 20(6): 1456-1469.
[50]	葛城成, 肖欣蕊, 王子涵, 丁蓓, 耿好, 谭永泰, 方慧敏. 水稻E3泛素连接酶响应非生物胁迫的分子机制研究进展[J]. 植物生理学报, 2023, 59(3): 490-504.
	Ge C C, Xiao X R, Wang Z H, Ding B, Geng H, Tan Y T, Fang H M. Research progress on molecular mechanism of rice E3 ubiquitin ligase in response to abiotic stresses[J]. Plant Physiology Journal, 2023, 59(3): 490-504. (in Chinese with English abstract)
[51]	Ning Y, Jantasuriyarat C, Zhao Q, Zhang H, Chen S, Liu J, Liu L, Tang S, Park C H, Wang X, Liu X, Dai L, Xie Q, Wang G L. The SINA E3 ligase OsDIS1 negatively regulates drought response in rice[J]. Plant Physiology, 2011, 157(1): 242-255.
[52]	杨茂, 林宇丰, 戴阳朔, 潘素君, 彭伟业, 严明雄, 李魏, 王冰, 戴良英. OsDIS1通过抗氧化途径负调控水稻耐旱性[J]. 生物技术通报, 2023, 39(2): 88-95.
	Yang M, Lin Y F, Dai Y S, Pan S J, Peng W Y, Yan M X, Li W, Wang B, Dai L Y. OsDIS1 negatively regulates rice drought tolerance through antioxidant pathways[J]. Biotechnology Bulletin, 2023, 39(2): 88-95. (in Chinese with English abstract)
[53]	Chen S, Xu K, Kong D, Wu L, Chen Q, Ma X, Ma S, Li T, Xie Q, Liu H, Luo L. Ubiquitin ligase OsRINGzf1 regulates drought resistance by controlling the turnover of OsPIP2;1[J]. Plant Biotechnology Journal, 2022, 20(9): 1743-1755.
[54]	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.)[J]. Plant Science, 2011, 180(6): 775-782.
[55]	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[J]. The Plant Cell, 2009, 21(2): 622-641.
[56]	Wang Z, Tian X, Zhao Q, Liu Z, Li X, Ren Y, Tang J, Fang J, Xu Q, Bu Q. The E3 ligase DROUGHT HYPERSENSITIVE negatively regulates cuticular wax biosynthesis by promoting the degradation of transcription factor ROC4 in rice[J]. The Plant Cell, 2018, 30(1): 228-244.
[57]	Qin Q, Wang Y, Huang L, Du F, Zhao X, Li Z, Wang W, Fu B. A U-box E3 ubiquitin ligase OsPUB67 is positively involved in drought tolerance in rice[J]. Plant Molecular Biology, 2020, 102(1): 89-107.
[58]	Gao T, Wu Y, Zhang Y, Liu L, Ning Y, Wang D, Tong H, Chen S, Chu C, Xie Q. OsSDIR1 overexpression greatly improves drought tolerance in transgenic rice[J]. Plant Molecular Biology, 2011, 76(1): 145-156.
[59]	赵晴, 欧英卓, 胡诗钦, 周宇阳, 郭龙彪, 郝芷圻, 孟丽君, 刘长华. 水稻耐盐生理及分子机制研究进展[J]. 中国农学通报, 2024, 40(12): 94-103.
	Zhao Q, Ou Y Z, Hu S Q, Zhou Y Y, Guo L B, Hao Z Q, Meng L J, Liu C H. Physiological response and molecular mechanism of salt tolerance in rice: A review[J]. Chinese Agricultural Science Bulletin, 2024, 40(12): 94-103. (in Chinese with English abstract)
[60]	Xiao L, Shi Y, Wang R, Feng Y, Wang L, Zhang H, Shi X, Jing G, Deng P, Song T, Jing W, Zhang W. The transcription factor OsMYBc and an E3 ligase regulate expression of a K+ transporter during salt stress[J]. Plant Physiology, 2022, 190(1): 843-859.
[61]	Fang H, Meng Q, Xu J, Tang H, Tang S, Zhang H, Huang J. Knock-down of stress inducible OsSRFP1 encoding an E3 ubiquitin ligase with transcriptional activation activity confers abiotic stress tolerance through enhancing antioxidant protection in rice[J]. Plant Molecular Biology, 2015, 87(4): 441-458.
[62]	Ruan W, Guo M, Wang X, Guo Z, Xu Z, Xu L, Zhao H, Sun H, Yan C, Yi K. Two RING-finger ubiquitin E3 ligases regulate the degradation of SPX4, an internal phosphate sensor, for phosphate homeostasis and signaling in rice[J]. Molecular Plant, 2019, 12(8): 1060-1074.
[63]	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)[J]. Planta, 2018, 247(4): 875-886.
[64]	Tiwari L D, Mittal D, Chandra Mishra R, Grover A. Constitutive over-expression of rice chymotrypsin protease inhibitor gene OCPI2 results in enhanced growth, salinity and osmotic stress tolerance of the transgenic Arabidopsis plants[J]. Plant Physiology and Biochemistry, 2015, 92: 48-55.
[65]	Lim S D, Jung C G, Park Y C, Lee S C, Lee C, Lim C W, Kim D S, Jang C S. Molecular dissection of a rice microtubule-associated RING finger protein and its potential role in salt tolerance in Arabidopsis[J]. Plant Molecular Biology, 2015, 89(4): 365-384.
[66]	Kim J H, Lim S D, Jang C S. Oryza sativa drought-, heat-, and salt-induced RING finger protein 1 (OsDHSRP1) negatively regulates abiotic stress-responsive gene expression[J]. Plant Molecular Biology, 2020, 103(3): 235-252.
[67]	Wang S, Xu L, Li C, Zhu L, Fu Y, Guo Y. Imaging of cortical microtubules in plants under salt stress[J]. Methods in Molecular Biology, 2023, 2604: 257-261.
[68]	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[J]. Plant, Cell & Environment, 2019, 42(11): 3061-3076.
[69]	Kim J H, Kim J H, Jung K H, Jang C S. OsSIRH2-23, a rice salt-induced RING finger protein H2-23, contributes to insensitivity to salinity stress[J]. Environmental and Experimental Botany, 2022, 194: 104715.
[70]	Zhang H, Zhou J F, Kan Y, Shan J X, Ye W W, Dong N Q, Guo T, Xiang Y H, Yang Y B, Li Y C, Zhao H Y, Yu H X, Lu Z Q, Guo S Q, Lei J J, Liao B, Mu X R, Cao Y J, Yu J J, Lin Y, Lin H X. A genetic module at one locus in rice protects chloroplasts to enhance thermotolerance[J]. Science, 2022, 376(6599): 1293-1300.
[71]	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[J]. Plant Molecular Biology, 2019, 99(6): 545-559.
[72]	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]. Journal of Experimental Botany, 2013, 64(10): 2899-2914.
[73]	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[J]. Plant Physiology, 2016, 170(1): 429-443.
[74]	Kaur H, Salvi P, Chaurasia A, Mondal T K. PUB63, a novel early heat responsive ubiquitin E3 ligase from rice implicates heat stress tolerance[J]. Plant Stress, 2023, 10: 100291.
[75]	Zhang H, Zheng D, Song F, Jiang M. Expression patterns and functional analysis of 11 E3 ubiquitin ligase genes in rice[J]. Frontiers in Plant Science, 2022, 13: 840360.
[76]	Cui L H, Min H J, Yu S G, Byun M Y, Oh T R, Lee A, Yang H W, Kim W T. OsATL38 mediates mono-ubiquitination of the 14-3-3 protein OsGF14d and negatively regulates the cold stress response in rice[J]. Journal of Experimental Botany, 2022, 73(1): 307-323.
[77]	Nakamura J, Yuasa T, Huong T T, Harano K, Tanaka S, Iwata T, Phan T, Iwaya M. Rice homologs of inducer of CBF expression (OsICE) are involved in cold acclimation[J]. Plant Biotechnology, 2011, 28(3): 303-309.
[78]	Lourenço T, Sapeta H, Figueiredo D D, Rodrigues M, Cordeiro A, Abreu I A, Saibo N J, Oliveira M M. Isolation and characterization of rice (Oryza sativa L.) E3-ubiquitin ligase OsHOS1 gene in the modulation of cold stress response[J]. Plant Molecular Biology, 2013, 83(4/5): 351-363.
[79]	Zhang Z, Li J, Li F, Liu H, Yang W, Chong K, Xu Y. OsMAPK3 phosphorylates OsbHLH002/OsICE1 and inhibits its ubiquitination to activate OsTPP1 and enhances rice chilling tolerance[J]. Developmental Cell, 2017, 43(6): 731-743.e5.
[80]	Cui L H, Min H J, Byun M Y, Oh H G, Kim W T. OsDIRP1, a putative RING E3 ligase, plays an opposite role in drought and cold stress responses as a negative and positive factor, respectively, in rice (Oryza sativa L.)[J]. Frontiers in Plant Science, 2018, 9: 1797.
[81]	Byun M Y, Cui L H, Oh T K, Jung Y J, Lee A, Park K Y, Kang B G, Kim W T. Homologous U-box E3 ubiquitin ligases OsPUB2 and OsPUB3 are involved in the positive regulation of low temperature stress response in rice (Oryza sativa L.)[J]. Frontiers in Plant Science, 2017, 8: 16.
[82]	Yan Y, Wang H, Bi Y, Song F. Rice E3 ubiquitin ligases: From key modulators of host immunity to potential breeding applications[J]. Plant Communications, 2024, 5(12): 101128.
[83]	Wang J, Wang R, Fang H, Zhang C, Zhang F, Hao Z, You X, Shi X, Park C H, Hua K, He F, Bellizzi M, Xuan Vo K T, Jeon J S, Ning Y, Wang G L. Two VOZ transcription factors link an E3 ligase and an NLR immune receptor to modulate immunity in rice[J]. Molecular Plant, 2021, 14(2): 253-266.
[84]	Li W, Zhong S, Li G, Li Q, Mao B, Deng Y, Zhang H, Zeng L, Song F, He Z. Rice RING protein OsBBI1 with E3 ligase activity confers broad-spectrum resistance against Magnaporthe oryzae by modifying the cell wall defence[J]. Cell Research, 2011, 21(5): 835-848.
[85]	Liu Z, Qiu J, Shen Z, Wang C, Jiang N, Shi H, Kou Y. The E3 ubiquitin ligase OsRGLG5 targeted by the Magnaporthe oryzae effector AvrPi9 confers basal resistance against rice blast[J]. Plant Communications, 2023, 4(5): 100626.
[86]	Wang Y, Zheng C, Peng Y L, Chen Q. DGS1 improves rice disease resistance by elevating pathogen-associated molecular pattern-triggered immunity[J]. aBIOTECH, 2024, 5(1): 46-51.
[87]	Bi Y, Wang H, Yuan X, Yan Y, Li D, Song F. The NAC transcription factor ONAC083 negatively regulates rice immunity against Magnaporthe oryzae by directly activating transcription of the RING-H2 gene OsRFPH2-6[J]. Journal of Integrative Plant Biology, 2023, 65(3): 854-875.
[88]	Wang S, Han S, Zhou X, Zhao C, Guo L, Zhang J, Liu F, Huo Q, Zhao W, Guo Z, Chen X. Phosphorylation and ubiquitination of OsWRKY31 are integral to OsMKK10-2-mediated defense responses in rice[J]. The Plant Cell, 2023, 35(6): 2391-2412.
[89]	Chen X, Shang J, Chen D, Lei C, Zou Y, Zhai W, Liu G, Xu J, Ling Z, Cao G, Ma B, Wang Y, Zhao X, Li S, Zhu L. A B-lectin receptor kinase gene conferring rice blast resistance[J]. The Plant Journal, 2006, 46(5): 794-804.
[90]	Wang K, Li S, Chen L, Tian H, Chen C, Fu Y, Du H, Hu Z, Li R, Du Y, Li J, Zhao Q, Du C. E3 ubiquitin ligase OsPIE3 destabilises the B-lectin receptor-like kinase PID2 to control blast disease resistance in rice[J]. New Phytologist, 2023, 237(5): 1826-1842.
[91]	Zhou X, Liao H, Chern M, Yin J, Chen Y, Wang J, Zhu X, Chen Z, Yuan C, Zhao W, Wang J, Li W, He M, Ma B, Wang J, Qin P, Chen W, Wang Y, Liu J, Qian Y, Wang W, Wu X, Li P, Zhu L, Li S, Ronald P C, Chen X. Loss of function of a rice TPR-domain RNA-binding protein confers broad-spectrum disease resistance[J]. Proceedings of the National Academy of Sciences of the United States of America, 2018, 115(12): 3174-3179.
[92]	Wang R, You X, Zhang C, Fang H, Wang M, Zhang F, Kang H, Xu X, Liu Z, Wang J, Zhao Q, Wang X, Hao Z, He F, Tao H, Wang D, Wang J, Fang L, Qin M, Zhao T, Zhang P, Xing H, Xiao Y, Liu W, Xie Q, Wang G L, Ning Y. An ORFeome of rice E3 ubiquitin ligases for global analysis of the ubiquitination interactome[J]. Genome Biology, 2022, 23(1): 154.
[93]	Wang Y S, Pi L Y, Chen X, Chakrabarty P K, Jiang J, de Leon A L, Liu G Z, Li L, Benny U, Oard J, Ronald P C, Song W Y. Rice XA21 binding protein 3 is a ubiquitin ligase required for full Xa21-mediated disease resistance[J]. The Plant Cell, 2006, 18(12): 3635-3646.
[94]	Choi C, Im J H, Lee J, Kwon S I, Kim W Y, Park S R, Hwang D J. OsDWD1 E3 ligase-mediated OsNPR1 degradation suppresses basal defense in rice[J]. The Plant Journal, 2022, 112(4): 966-981.
[95]	Kachewar N R, Gupta V, Ranjan A, Patel H K, Sonti R V. Overexpression of OsPUB41, a rice E3 ubiquitin ligase induced by cell wall degrading enzymes, enhances immune responses in rice and Arabidopsis[J]. BMC Plant Biology, 2019, 19(1): 530.
[96]	Ishikawa K, Yamaguchi K, Sakamoto K, Yoshimura S, Inoue K, Tsuge S, Kojima C, Kawasaki T. Bacterial effector modulation of host E3 ligase activity suppresses PAMP-triggered immunity in rice[J]. Nature Communications, 2014, 5: 5430.
[97]	Gao M, He Y, Yin X, Zhong X, Yan B, Wu Y, Chen J, Li X, Zhai K, Huang Y, Gong X, Chang H, Xie S, Liu J, Yue J, Xu J, Zhang G, Deng Y, Wang E, Tharreau D, Wang G L, Yang W, He Z. Ca²⁺ sensor-mediated ROS scavenging suppresses rice immunity and is exploited by a fungal effector[J]. Cell, 2021, 184(21): 5391-5404.e17.
[98]	Park C H, Chen S, Shirsekar G, Zhou B, Khang C H, Songkumarn P, Afzal A J, Ning Y, Wang R, Bellizzi M, Valent B, Wang G L. TheMagnaporthe oryzaeEffector AvrPiz-t targets the RING E3 ubiquitin ligase APIP6 to suppress pathogen-associated molecular pattern-triggered immunity in rice[J]. The Plant Cell, 2012, 24(11): 4748-4762
[99]	You X, Zhang F, Liu Z, Wang M, Xu X, He F, Wang D, Wang R, Wang Y, Wang G, Chu C, Wang G L, Ning Y. Rice catalase OsCATC is degraded by E3 ligase APIP6 to negatively regulate immunity[J]. Plant Physiology, 2022, 190(2): 1095-1099.
[100]	You X, Zhu S, Sheng H, Liu Z, Wang D, Wang M, Xu X, He F, Fang H, Zhang F, Wang D, Hao Z, Wang R, Xiao Y, Wan J, Wang G L, Ning Y. The rice peroxisomal receptor PEX5 negatively regulates resistance to rice blast fungus Magnaporthe oryzae[J]. Cell Reports, 2023, 42(10): 113315.
[101]	Yi H, Shi H, Mao W, Yin J, Ma Y, Xu L, Jing L, He M, Zhu X, Lu X, Xiong Q, Tang Y, Hou Q, Song L, Wang L, Li W, Yu H, Chen X, Li J, Wang J. E3 ubiquitin ligase IPI1 controls rice immunity and flowering via both E3 ligase-dependent and-independent pathways[J]. Developmental Cell, 2024, 59(20): 2719-2730.e4.
[102]	Fu S, Wang K, Ma T, Liang Y, Ma Z, Wu J, Xu Y, Zhou X. An evolutionarily conserved C₄HC₃-type E3 ligase regulates plant broad-spectrum resistance against pathogens[J]. The Plant Cell, 2022, 34(5): 1822-1843
[103]	Zhang C, Fang H, Wang J, Tao H, Wang D, Qin M, He F, Wang R, Wang G L, Ning Y. The rice E3 ubiquitin ligase-transcription factor module targets two trypsin inhibitors to enhance broad-spectrum disease resistance[J]. Developmental Cell, 2024, 59(15): 2017-2033.e5.
[104]	You Q, Zhai K, Yang D, Yang W, Wu J, Liu J, Pan W, Wang J, Zhu X, Jian Y, Liu J, Zhang Y, Deng Y, Li Q, Lou Y, Xie Q, He Z. An E3 ubiquitin ligase-BAG protein module controls plant innate immunity and broad-spectrum disease resistance[J]. Cell Host & Microbe, 2016, 20(6): 758-769.
[105]	Fan J, Bai P, Ning Y, Wang J, Shi X, Xiong Y, Zhang K, He F, Zhang C, Wang R, Meng X, Zhou J, Wang M, Shirsekar G, Park C H, Bellizzi M, Liu W, Jeon J S, Xia Y, Shan L, Wang G L. The monocot-specific receptor-like kinase SDS2 controls cell death and immunity in rice[J]. Cell Host & Microbe, 2018, 23(4): 498-510.e5.
[106]	Liu J, Park C H, He F, Nagano M, Wang M, Bellizzi M, Zhang K, Zeng X, Liu W, Ning Y, Kawano Y, Wang G L. The RhoGAP SPIN6 associates with SPL11 and OsRac1 and negatively regulates programmed cell death and innate immunity in rice[J]. PLoS Pathogens, 2015, 11(2): e1004629.
[107]	Wang G, Chen X, Yu C, Shi X, Lan W, Gao C, Yang J, Dai H, Zhang X, Zhang H, Zhao B, Xie Q, Yu N, He Z, Zhang Y, Wang E. Release of a ubiquitin brake activates OsCERK1-triggered immunity in rice[J]. Nature, 2024, 629(8014): 1158-1164.
[108]	Hao Z, Tian J, Fang H, Fang L, Xu X, He F, Li S, Xie W, Du Q, You X, Wang D, Chen Q, Wang R, Zuo S, Yuan M, Wang G L, Xia L, Ning Y. A VQ-motif-containing protein fine-tunes rice immunity and growth by a hierarchical regulatory mechanism[J]. Cell Reports, 2022, 40(7): 111235.
[109]	Liu Q, Ning Y, Zhang Y, Yu N, Zhao C, Zhan X, Wu W, Chen D, Wei X, Wang G L, Cheng S, Cao L. OsCUL3a negatively regulates cell death and immunity by degrading OsNPR1 in rice[J]. The Plant Cell, 2017, 29(2): 345-359.
[110]	Yang D L, Yao J, Mei C S, Tong X H, Zeng L J, Li Q, Xiao L T, Sun T P, Li J, Deng X W, Lee C M, Thomashow M F, Yang Y, He Z, He S Y. Plant hormone jasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade[J]. Proceedings of the National Academy of Sciences of the United States of America, 2012, 109(19): E1192-E1200.
[111]	Zhang Y, Chen M, Zhou S, Lou Y, Lu J. Silencing an E3 ubiquitin ligase gene OsJMJ715 enhances the resistance of rice to a piercing-sucking herbivore by activating ABA and JA signaling pathways[J]. International Journal of Molecular Sciences, 2021, 22(23): 13020.
[112]	Ma F, Yang X, Shi Z, Miao X. Novel crosstalk between ethylene- and jasmonic acid-pathway responses to a piercing-sucking insect in rice[J]. New Phytologist, 2020, 225(1): 474-487.
[113]	Li S, Zhang Y, Liu Y, Zhang P, Wang X, Chen B, Ding L, Nie Y, Li F, Ma Z, Kang Z, Mao H. The E3 ligase TaGW2 mediates transcription factor TaARR12 degradation to promote drought resistance in wheat[J]. Plant Cell, 2024, 36(3): 605-625.
[114]	Liu X, Song L, Zhang H, Lin Y, Shen X, Guo J, Su M, Shi G, Wang Z, Lu G D. Rice ubiquitin-conjugating enzyme OsUBC26 is essential for immunity to the blast fungus Magnaporthe oryzae[J]. Molecular Plant Pathology, 2021, 22(12): 1613-1623.