水稻泛素结合酶E2的生物学功能研究进展

doi:10.16819/j.1001-7216.2025.250316

摘要/Abstract

摘要：

泛素化是一种重要的蛋白质翻译后修饰，承担了真核生物中蛋白质降解任务的80%~85%，并影响蛋白的活性、定位和功能，从而广泛参与各种生命活动的调控。泛素结合酶E2是泛素化级联反应中的第二个酶，不仅作为泛素载体，还决定着泛素链的连接方式和长度。水稻中预测存在48个E2基因，所编码蛋白均含有一个高度保守的泛素结合(UBC)结构域。该结构域通过硫酯键与泛素分子结合，同时与泛素连接酶E3形成特异性互作界面，确保泛素转移的精确性。研究表明E2广泛参与调控水稻生长发育与生物/非生物胁迫应答。

关键词: 泛素结合酶, 泛素化, 蛋白修饰, 水稻

Abstract:

Ubiquitination is a critical post-translational modification, accounting for 80%-85% of protein degradation in eukaryotes. It regulates protein activity, localization, and function, thereby playing extensive roles in modulating diverse biological processes. The ubiquitin-conjugating enzyme E2, the second key enzyme in the ubiquitination cascade, acts not only as a ubiquitin carrier but also determines the type of ubiquitin linkages and the length of ubiquitin chains. A total of 48 E2 genes have been identified in rice, all encoding proteins that contain a highly conserved UBC (ubiquitin-conjugating) domain. This domain binds to ubiquitin via a thioester bond and forms a specific interaction interface with ubiquitin ligase E3, ensuring the precision of ubiquitin transfer. Studies have shown that E2 enzymes are widely involved in regulating rice growth and development, as well as responses to biotic stresses such as pathogen infection and abiotic stresses including drought and cold.

Key words: ubiquitin-conjugating enzyme, ubiquitination, protein modification, rice

王娟, 吴丽娟, 洪海波, 姚志文, 王磊, 鄂志国. 水稻泛素结合酶E2的生物学功能研究进展[J]. 中国水稻科学, 2025, 39(6): 744-750.

WANG Juan, WU Lijuan, HONG Haibo, YAO Zhiwen, WANG Lei, E Zhiguo. Research Progress on Biological Functions of Ubiquitin-conjugating Enzymes in Rice[J]. Chinese Journal OF Rice Science, 2025, 39(6): 744-750.

图/表 2

参考文献 38

[1]	Wang J, Jiang J, Oard J H. Structure, expression and promoter activity of two polyubiquitin genes from rice (Oryza sativa L.)[J]. Plant Science, 2000, 156(2): 201-211.
[2]	Morreale F E, Walden H. Types of ubiquitin ligases[J]. Cell, 2016, 165(1): 248-248.e1.
[3]	Yang Q, Zhao J, Chen D, Wang Y. E3 ubiquitin ligases: Styles, structures and functions[J]. Molecular Biomedicine, 2021, 2(1): 23.
[4]	Mevissen T E T, Hospenthal M K, Geurink P P, Elliott P R, Akutsu M, Arnaudo N, Ekkebus R, Kulathu Y, Wauer T, El Oualid F, Freund S M V, Ovaa H, Komander D. OTU deubiquitinases reveal mechanisms of linkage specificity and enable ubiquitin chain restriction analysis[J]. Cell, 2013, 154(1): 169-184.
[5]	Zhang Y, Li T, Wang L, Zhao H. Characterization of the ubiquitin-conjugating enzyme gene family in rice and evaluation of expression profiles under abiotic stresses and hormone treatments[J]. PLoS One, 2015, 10(4): e0122621.
[6]	Bae H, Kim W T. Classification and interaction modes of 40 rice E 2 ubiquitin-conjugating enzymes with 17 rice ARM-U-box E3 ubiquitin ligases[J]. Biochemical and Biophysical Research Communications, 2014, 444(4): 575-580.
[7]	Zang Y, Wang Q, Xue C, Li M, Wen R, Xiao W. Rice UBC13 a candidate housekeeping gene, is required for K63-linked polyubiquitination and tolerance to DNA damage[J]. Rice, 2012, 5(1): 24.
[8]	Wang Q, Zang Y, Zhou X, Xiao W. Characterization of four rice UEV1 genes required for Lys63-linked polyubiquitination and distinct functions[J]. BMC Plant Biology, 2017, 17(1): 126.
[9]	Wang F, Deng M, Chen J, He Q, Jia X, Guo H, Xu J, Liu Y, Zhang S, Shou H, Mao C. CASEIN KINASE2-dependent phosphorylation of PHOSPHATE2 fine-tunes phosphate homeostasis in rice[J]. Plant Physiology, 2020, 183(1): 250-262.
[10]	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.
[11]	Liu H, Liu S, Yu H, Huang X, Wang Y, Jiang L, Meng X, Liu G, Chen M, Jing Y, Yu F, Wang B, Li J. An engineered platform for reconstituting functional multisubunit SCF E3 ligase in vitro[J]. Molecular Plant, 2022, 15(8): 1285-1299.
[12]	Swatek K N, Komander D. Ubiquitin modifications[J]. Cell Research, 2016, 26(4): 399-422.
[13]	Han Y, Zhang C, Sha H, Wang X, Yu Y, Liu J, Zhao G, Wang J, Qiu G, Xu X, Fang J. Ubiquitin-conjugating enzyme OsUBC11 affects the development of roots via auxin pathway[J]. Rice, 2023, 16(1): 9.
[14]	Zhang C, Wang H, Tian X, Lin X, Han Y, Han Z, Sha H, Liu J, Liu J, Zhang J, Bu Q, Fang J. A transposon insertion in the promoter of OsUBC12 enhances cold tolerance during japonica rice germination[J]. Nature Communications, 2024, 15(1): 2211
[15]	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.
[16]	Zheng Y, Zhang S, Luo Y, Li F, Tan J, Wang B, Zhao Z, Lin H, Zhang T, Liu J, Liu X, Guo J, Xie X, Chen L, Liu Y G, Chu Z. Rice OsUBR7 modulates plant height by regulating histone H2B monoubiquitination and cell proliferation[J]. Plant Communications, 2022, 3(6): 100412.
[17]	Liu J, Liao W, Nie B, Zhang J, Xu W. OsUEV1B, an Ubc enzyme variant protein, is required for phosphate homeostasis in rice[J]. The Plant Journal, 2021, 106(3): 706-719.
[18]	Hu B, Zhu C, Li F, Tang J, Wang Y, Lin A, Liu L, Che R, Chu C. LEAF TIP NECROSIS1 plays a pivotal role in the regulation of multiple phosphate starvation pesponses in rice[J]. Plant Physiology, 2011, 156(3): 1101-1115.
[19]	Cao Y, Yan Y, Zhang F, Wang H D, Gu M, Wu X N, Sun S B, Xu G H. Fine characterization of OsPHO2 knockout mutants reveals its key role in Pi utilization in rice[J]. Journal of Plant Physiology, 2014, 171(3-4): 340-348.
[20]	Hu B, Wang W, Deng K, Li H, Zhang Z, Zhang L, Chu C. MicroRNA399 is involved in multiple nutrient starvation responses in rice[J]. Frontiers in Plant Science, 2015, 6: 188.
[21]	Yamamoto T, Mori Y, Ishibashi T, Uchiyama Y, Sakaguchi N, Furukawa T, Hashimoto J, Kimura S, Sakaguchi K. Characterization of Rad 6 from a higher plant, rice (Oryza sativa L.) and its interaction with Sgt1, a subunit of the SCF ubiquitin ligase complex[J]. Biochemical and Biophysical Research Communications, 2004, 314(2): 434-439.
[22]	Zang G, Zou H, Zhang Y, Xiang Z, Huang J, Luo L, Wang C, Lei K, Li X, Song D, Din A U, Wang G. The de-etiolated 1 homolog of Arabidopsis modulates the ABA signaling pathway and ABA biosynthesis in rice[J]. Plant Physiology, 2016, 171(2): 1259-1276.
[23]	Kim B, Lee Y, Nam J Y, Lee G, Seo J, Lee D, Cho Y H, Kwon S W, Koh H J. Mutations in OsDET1, OsCOP10, and OsDDB1 confer embryonic lethality and alter flavonoid accumulation in rice (Oryza sativa L.) seed[J]. Frontiers in Plant Science, 2022, 13: 952856.
[24]	Wei Z, Zhang Y, Yuan Y, Li L, Li T, Guan Y, Wang D, Gao Y, Gao Q, Ji J, Nguyen T, Liu X. Ubiquitin-conjugated enzyme OsUBC16 negatively regulates grain size and grain weight in rice[J]. Journal of Plant Biology, 2024, 67(5): 409-418.
[25]	Xie Y, Fan Z, Liang X, Teng K, Huang Z, Huang M, Zhao H, Xu K, Li J. OsPUB9 modulates leaf angle and grain size through the brassinosteroid signaling pathway in rice[J]. The Plant Journal, 2025, 121(3): e17230.
[26]	Ma J, Wang Y, Ma X, Meng L, Jing R, Wang F, Wang S, Cheng Z, Zhang X, Jiang L, Wang J, Wang J, Zhao Z, Guo X, Lin Q, Wu F, Zhu S, Wu C, Ren Y, Lei C, Zhai H, Wan J. Disruption of gene SPL35 encoding a novel CUE domain-containing protein, leads to cell death and enhanced disease response in rice[J]. Plant Biotechnology Journal, 2019, 17(8): 1679-1693.
[27]	Takai R, Matsuda N, Nakano A, Hasegawa K, Akimoto C, Shibuya N, Minami E. 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[J]. The Plant Journal, 2002, 30(4): 447-455.
[28]	Liu J, Nie B, Yu B, Xu F, Zhang Q, Wang Y, Xu W. Rice ubiquitin-conjugating enzyme OsUbc13 negatively regulates immunity against pathogens by enhancing the activity of OsSnRK1a[J]. Plant Biotechnology Journal, 2023, 21(8): 1590-1610.
[29]	Filipe O, De Vleesschauwer D, Haeck A, Demeestere K, Höfte M. The energy sensor OsSnRK1a confers broad-spectrum disease resistance in rice[J]. Scientific Reports, 2018, 8(1): 3864.
[30]	Cao Y, Lu M, Chen J, Li W, Wang M, Chen F. Identification of Ossnrk1a-1 regulated genes associated with rice immunity and seed set[J]. Plants, 2024, 13(5): 596.
[31]	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.
[32]	Phan H, Schläppi M. The RAD6-like ubiquitin conjugase gene OsUBC7 has a positive role in the early cold stress tolerance response of rice[J]. Genes, 2025, 16(1): 66.
[33]	Pathak B, Maurya C, Faria M C, Alizada Z, Nandy S, Zhao S, Jamsheer K M, Srivastava V. Targeting TOR and SnRK1 genes in rice with CRISPR/Cas9[J]. Plants, 2022, 11(11): 1453.
[34]	Ghimire S, Tang X, Liu W, Fu X, Zhang H, Zhang N, Si H. SUMO conjugating enzyme: A vital player of SUMO pathway in plants[J]. Physiology and Molecular Biology of Plants, 2021, 27(10): 2421-2431.
[35]	Joo J, Choi D H, Lee Y H, Seo H S, Song S I. The rice SUMO conjugating enzymes OsSCE1 and OsSCE3 have opposing effects on drought stress[J]. Journal of Plant Physiology, 2019, 240 : 152993.
[36]	Nurdiani D, Widyajayantie D, Nugroho S. OsSCE1 encoding SUMO E2-conjugating enzyme involves in drought stress response of Oryza sativa[J]. Rice Science, 2018, 25(2): 73-81.
[37]	Nigam N, Singh A, Sahi C, Chandramouli A, Grover A. SUMO-conjugating enzyme (Sce) and FK506-binding protein (FKBP) encoding rice (Oryza sativa L.) genes: Genome-wide analysis, expression studies and evidence for their involvement in abiotic stress response[J]. Molecular Genetics and Genomics, 2008, 279(4): 371-383.
[38]	Yuan X, Luan Y, Liu D, Wang J, Peng J, Zhao J, Li L, Su J, Xiao Y, Li Y, Ma X, Zhu X, Tan L, Liu F, Sun H, Gu P, Xu R, Zhang P, Zhu Z, Sun C, Fu Y, Zhang K. The SUMO-conjugating enzyme OsSCE1a from wild rice regulates the functional stay-green trait in rice[J]. Plant Biotechnology Journal, 2025, 23(2): 615-631.

基因名称 Gene name	别名 Gene alias	基因号 Gene ID	染色体 Chromosome	生物学功能 Biological function	参考文献 Reference
OsUBC1	OsSCE1	Os10g0536000	10	影响粒重和结实率，负调控耐旱性 Negatively regulates grain weight, seed-setting rate, and drought tolerance	[35]
OsUBC2	OsSCE1a; OsSCE2	Os03g0123100	3	负调控氮素利用率和光合效率，延长抽穗期 Negatively regulates nitrogen use efficiency and photosynthetic efficiency, and delays heading date	[38]
OsUBC3	OsSCE3	Os04g0580400	4	正调控耐旱性 Positively regulates drought tolerance	[35]
OsUBC7	qMT7-3	Os07g0166800	7	正调控籼稻幼苗的耐寒性 Positively regulates cold tolerance in indica rice seedlings	[32]
OsUBC9	OsRad6	Os03g0791800	3	与SCF泛素连接酶亚基OsSGT1互作 Interacts with the SCF ubiquitin ligase subunit OsSGT1	[21]
OsUBC11		Os01g0839700	1	负调控根系、节间和穗发育 Negatively regulates root, internode, and panicle development	[13]
OsUBC12		Os05g0460200	5	增强粳稻的低温下发芽能力 Enhances germination ability under low temperature conditions in japonica rice	[14]
OsUBC13		Os02g0120600	2	与OsPUB9互作使其稳定 Interacts with and stabilizes OsPUB9	[25]
OsUBC14	OsUBC5a	Os01g0658400	1	负调控细胞死亡和免疫反应 Negatively regulates cell death and immune responses	[26]
OsUBC16		Os04g0667800	4	负调控水稻籽粒大小和重量 Negatively regulates grain size and weight in rice	[24]
OsUBC18		Os09g0293400	9	与OsUBR7配对催化组蛋白H2B单泛素化 Pairs with OsUBR7 to catalyze histone H2B monoubiquitination	[16]
OsUBC24		Os07g0577400	7	调节水稻胚发生和类黄酮生物合成 Regulates rice embryogenesis and flavonoid biosynthesis	[23]
OsUBC26		Os12g0636800	12	正调控稻瘟病抗性 Positively regulates resistance to rice blast	[31]
OsUBC30	OsUEV1B	Os12g0605400	12	调节磷酸盐稳态 Regulates phosphate homeostasis	[17]
OsUBC35	LTN1; OsPHO2	Os05g0557700	5	调节磷酸盐稳态 Regulates phosphate homeostasis	[9,18-20]
OsUBC45	SMG3	Os03g0308000	3	调控穗和籽粒发育 Regulates panicle and grain development	[15]
OsUBC47	OsUBC13	Os01g0673600	1	负调控稻瘟病和白叶枯病抗性 Negatively regulates resistance to rice blast and bacterial blight	[28]

基因名称 Gene name	别名 Gene alias	基因号 Gene ID	染色体 Chromosome	生物学功能 Biological function	参考文献 Reference
OsUBC1	OsSCE1	Os10g0536000	10	影响粒重和结实率，负调控耐旱性 Negatively regulates grain weight, seed-setting rate, and drought tolerance	[35]
OsUBC2	OsSCE1a; OsSCE2	Os03g0123100	3	负调控氮素利用率和光合效率，延长抽穗期 Negatively regulates nitrogen use efficiency and photosynthetic efficiency, and delays heading date	[38]
OsUBC3	OsSCE3	Os04g0580400	4	正调控耐旱性 Positively regulates drought tolerance	[35]
OsUBC7	qMT7-3	Os07g0166800	7	正调控籼稻幼苗的耐寒性 Positively regulates cold tolerance in indica rice seedlings	[32]
OsUBC9	OsRad6	Os03g0791800	3	与SCF泛素连接酶亚基OsSGT1互作 Interacts with the SCF ubiquitin ligase subunit OsSGT1	[21]
OsUBC11		Os01g0839700	1	负调控根系、节间和穗发育 Negatively regulates root, internode, and panicle development	[13]
OsUBC12		Os05g0460200	5	增强粳稻的低温下发芽能力 Enhances germination ability under low temperature conditions in japonica rice	[14]
OsUBC13		Os02g0120600	2	与OsPUB9互作使其稳定 Interacts with and stabilizes OsPUB9	[25]
OsUBC14	OsUBC5a	Os01g0658400	1	负调控细胞死亡和免疫反应 Negatively regulates cell death and immune responses	[26]
OsUBC16		Os04g0667800	4	负调控水稻籽粒大小和重量 Negatively regulates grain size and weight in rice	[24]
OsUBC18		Os09g0293400	9	与OsUBR7配对催化组蛋白H2B单泛素化 Pairs with OsUBR7 to catalyze histone H2B monoubiquitination	[16]
OsUBC24		Os07g0577400	7	调节水稻胚发生和类黄酮生物合成 Regulates rice embryogenesis and flavonoid biosynthesis	[23]
OsUBC26		Os12g0636800	12	正调控稻瘟病抗性 Positively regulates resistance to rice blast	[31]
OsUBC30	OsUEV1B	Os12g0605400	12	调节磷酸盐稳态 Regulates phosphate homeostasis	[17]
OsUBC35	LTN1; OsPHO2	Os05g0557700	5	调节磷酸盐稳态 Regulates phosphate homeostasis	[9,18-20]
OsUBC45	SMG3	Os03g0308000	3	调控穗和籽粒发育 Regulates panicle and grain development	[15]
OsUBC47	OsUBC13	Os01g0673600	1	负调控稻瘟病和白叶枯病抗性 Negatively regulates resistance to rice blast and bacterial blight	[28]