Roles of Histone H2B Monoubiquitination in the Growth and Stress Responses of Plants
LIU Shan-He1, PAN Yan-Yun1*, LI Jun1,2*
1 College of Life Sciences/Key Laboratory of Hebei Province for Plant Physiology and Molecular Pathology, Hebei Agricultural University, Baoding 071000, China; 2 State Key Laboratory of North China Crop Improvement and Regulation, Baoding 071000, China
Abstract：Histone monoubiquitination (H2Bub1) is conserved among eukaryotes, and is one of known histone modifications. H2Bub1 is essential for the growth and development of organisms. In recent years, a great number of studies have shown that H2Bub1 is widely involved in plant growth, development and stress response. In this review, diverse roles of H2Bub1 in regulating developmental processes were introduced, including seed dormancy, photomorphogenesis, and flowering time, and the biological function of H2Bub1 in response to biotic and abiotic stress were discussed. This review provides reference for the crop genetic improvement.
刘善贺, 潘延云, 李君. 组蛋白 H2B 单泛素化在植物生长发育和胁迫应答中的作用[J]. 农业生物技术学报, 2023, 31(5): 1064-1073.
LIU Shan-He, PAN Yan-Yun, LI Jun. Roles of Histone H2B Monoubiquitination in the Growth and Stress Responses of Plants. 农业生物技术学报, 2023, 31(5): 1064-1073.
[1] 欧斯艳, 张亚楠, 王金祥. 2020. 植物响应低磷胁迫的蛋白质泛素化途径研究进展[J]. 植物营养与肥料学报, 26(11): 2060-2069. (OU S Y, Zhang Y N, Wang J X. 2020. Advances in protein ubiquitination in response to low phosphorus stress in plants[J]. Journal of Plant Nutrition and Fertilizers, 26(11): 2060-2069.) [2] 薛满德, 赵峰月, 李洁等. 2022. 组蛋白变体在植物表观遗传调控中的研究进展[J]. 生物技术通报, 38(7): 1-12. (Xue M D, Zhao F Y, Li J et al., Histone variants in plant epigenetic regulation[J]. Biotechnology Bulletin, 38(7): 1-12.) [3] 杨柳, 杨洁舒, 孙睿聪等. 2017. 拟南芥 DNA 去甲基化候选突变体 rll2 的鉴定与功能分析[J]. 农业生物技术学报, 25(8): 1207-1216. (Yang L,Yang S J, Sun R et al., Identification and functional analysis of a candidate mutant rll2 associated with DNA demethylation processes in Arabidopsis thaliana[J]. Journal of Agricultural Biotechnology, 25(8): 1207-1216.) [4] 赵添羽, 韩成贵. 2022. 去泛素化修饰在病毒侵染中的作用研究进展[J]. 农业生物技术学报 30(10): 2025-2035. (Zhao T Y, Han C G, 2022. Research progress on the role of deubiquitination modification in viral infection[J]. Journal of Agricultural Biotechnology, 30(10): 2025-2035.) [5] Adli M. 2018. The CRISPR tool kit for genome editing and beyond[J]. Nature Communications, 9(1): 1911. [6] Allis C D, Jenuwein T. 2016. The molecular hallmarks of epigenetic control[J]. Nature Reviews Genetics, 17(8): 487-500. [7] Andrews A J, Luger K. 2011. Nucleosome Structure(s) and stability: Variations on a theme[J]. Annual Review of Biophysics, 40: 99-117. [8] Bard J A, Goodall E A, Greene E R, et al. 2018. Structure and function of the 26S proteasome[J]. Annual Review of Biochemistry, 87(1): 697-724. [9] Berr A, Shafiq S, Shen W H. 2011. Histone modifications in transcriptional activation during plant development[J]. Biochimica et Biophysica Acta, 1809(10): 567-576. [10] Bourbousse C, Ahmed I, Roudier F, et al. 2012. Histone H2B monoubiquitination facilitates the rapid modulation of gene expression during Arabidopsis photomorphogenesis[J]. PLoS Genetics, 8(7): e1002825. [11] Braun S, Madhani H D. 2012. Shaping the landscape: Mechanistic consequences of ubiquitin modification of chromatin[J]. EMBO Reports, 13(7): 619-630. [12] Bray S, Musisi H, Bienz M. 2005. Bre1 is required for Notch signaling and histone modification[J]. Developmental Cell, 8(2): 279-286. [13] Cao H, Li X Y, Wang Z, et al. 2015. Histone H2B monoubiquitination mediated by HISTONE MONOUBIQUITINATION1 and HISTONE MONOUBIQUITINATION2 is involved in anther development by regulating tapetum degradation-related genes in rice[J]. Plant Physiology, 168(4): 1389-1514. [14] Cao Y, Dai Y, Cui S, et al. 2008. Histone H2B monoubiquitination in the chromatin of FLOWERING LOCUS C regulates flowering time in Arabidopsis[J]. Plant Cell, 20(10): 2586-2602. [15] Chen H, Feng H, Zhang X, et al. 2019. An Arabidopsis E3 ligase HUB2 increases histone H2B monoubiquitination and enhances drought tolerance in transgenic cotton[J]. Plant Biotechnology Journal, 17(3): 556-568. [16] Chen K, Tang W S, Zhou Y B, et al. 2020. Overexpression of GmUBC9 gene enhances plant drought resistance and affects flowering time via histone H2B monoubiquitination[J]. Frontiers in Plant Science, 11: 555794. [17] Daniel J A, Torok M S, Sun Z W, et al. 2004. Deubiquitination of histone H2B by a yeast acetyltransferase complex regulates transcription[J]. Journal of Biological Chemistry, 279(3): 1867-1871. [18] Deng Z H, Ai H S, Lu C P, et al. 2020. The Bre1/Rad6 machinery: Writing the central histone ubiquitin mark on H2B and beyond[J]. Chromosome Research, 28(3-4): 247-258. [19] Dhawan R, Luo H L, Foerster A M, et al. 2009. HISTONE MONOUBIQUITINATION1 interacts with a subunit of the mediator complex and regulates defense against necrotrophic fungal pathogens in Arabidopsis[J]. Plant Cell, 21(3): 1000-1019. [20] Duan C G, Zhu J K, Cao X. 2018. Retrospective and perspective of plant epigenetics in China[J]. Journal of Genetics and Genomics, 45(11): 621-638. [21] Feng J, Shen W H. 2014. Dynamic regulation and function of histone monoubiquitination in plants[J]. Frontiers in Plant Science, 5: 83. [22] Fleury D, Himanen K, Cnops G, et al. 2007. The Arabidopsis thaliana homolog of yeast BRE1 has a function in cell cycle regulation during early leaf and root growth[J]. Plant Cell, 19(2): 417-432. [23] Gagne J M, Downes B P, Shiu S H, et al. 2002. The F-box subunit of the SCF E3 complex is encoded by a diverse superfamily of genes in Arabidopsis[J]. Proceedings of the National Academy of Sciences of the USA, 99(17): 11519-11524. [24] Gao C. 2021. Genome engineering for crop improvement and future agriculture[J]. Cell, 184(6): 1621-1635. [25] Gazzarrini S, Tsai A Y. 2015. Hormone cross-talk during seed germination[J]. Plant Hormone Signalling, 58: 151-164. [26] Han Y G, Yun M, Choi M, et al. 2019. TRAIP regulates Histone H2B monoubiquitination in DNA damage response pathways[J]. Oncology Reports, 41(6): 3305-3312. [27] He K, Cao X, Deng X. 2021. Histone methylation in epigenetic regulation and temperature responses[J]. Current Opinion in Plant Biology, 61: 102001. [28] Himanen K, Woloszynska M, Boccardi T M, et al. 2012. Histone H2B monoubiquitination is required to reach maximal transcript levels of circadian clock genes in Arabi- dopsis[J]. The Plant Journal, 72(2): 249-260. [29] Hsu P L, Shi H, Leonen C, et al. 2019. Structural basis of H2B ubiquitination-dependent H3K4 methylation by COMPASS[J]. Molecular Cell, 76(5): 712-723. [30] Hu M, Pei B L, Zhang L F, et al. 2014. Histone H2B monoubiquitination is involved in regulating the dynamics of microtubules during the defense response to Verticillium dahliae toxins in Arabidopsis[J]. Plant Physiology, 164(4): 1857-1865. [31] Hu Y, Zhang L, Zhao L, et al. 2011. Trichostatin a selectively suppresses the cold-induced transcription of the Zm- DREB1 gene in Maize[J]. PLoS One, 6(7): e22132. [32] Hwang W W, Venkatasubrahmanyam S, Ianculescu A G, et al. 2003. A conserved RING finger protein required for histone H2B monoubiquitination and cell size control[J]. Molecular Cell, 11(1): 261-266. [33] Kao C F, Hillyer C, Tsukuda T, et al. 2004. Rad6 plays a role in transcriptional activation through ubiquitylation of histone H2B[J]. Genes & Development, 18(2): 184-195. [34] Kim J, Guermah M, McGinty R K, et al. 2009. RAD6-mediated transcription-coupled H2B ubiquitylation directly stimulates H3K4 Methylation in human cells[J]. Cell, 137(3): 459-471. [35] Köhler C, Springer N. 2017. Plant epigenomics-deciphering the mechanisms of epigenetic inheritance and plasticity in plants[J]. Genome Biology, 18(1): 132. [36] Kouzarides T. 2007. Chromatin modifications and their function[J]. Cell, 128(4): 693-705. [37] Kushwaha N K, Mansi, Chakraborty S. 2017. The replication initiator protein of a geminivirus interacts with host monoubiquitination machinery and stimulates transcription of the viral genome[J]. PLOS Pathogens, 13(8): 1-41. [38] Lee J S, Shukla A, Schneider J, et al. 2007. Histone crosstalk between H2B monoubiquitination and H3 methylation mediated by COMPASS[J]. Cell, 131(6): 1084-1096. [39] Leo M, Fanelli G, Di Vito S, et al. 2018. Ubiquitin protease Ubp8 is necessary for S. cerevisiae respiration[J]. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, 1865(10), 1491-1500. [40] Liu B, Ruan J, Chen M, et al. 2022. Deubiquitinating enzymes (DUBs): Decipher underlying basis of neurodegenerative diseases[J]. Molecular Psychiatry, 27(1): 259-268. [41] Liu Y X, Koornneef M, Soppe W J. 2007. The absence of histone H2B monoubiquitination in the Arabidopsis hub1 (rdo4) mutant reveals a role for chromatin remodeling in seed dormancy[J]. Plant Cell, 19(2): 433-444. [42] Ma S Q, Tang N, Li X, et al. 2019. Reversible histone H2B monoubiquitination fine-tunes abscisic acid signaling and drought response in rice[J]. Molecular Plant, 12(2): 263-277. [43] Marsh D J, Dickson K A. 2019. Writing histone monoubiquitination in human malignancy-the role of RING finger E3 ubiquitin ligases[J]. Genes (Basel), 10(1): 67. [44] Menard R, Verdier G, Ors M, et al. 2014. Histone H2B monoubiquitination is involved in the regulation of cutin and wax composition in Arabidopsis thaliana[J]. Plant and Cell Physiology, 55(2): 455-466. [45] Nassrallah A, Rougée M, Bourbousse C, et al. 2018. DET1- mediated degradation of a SAGA-like deubiquitination module controls H2Bub homeostasis[J]. Elife, 7: e37892. [46] Nelissen H, De Groeve S, Fleury D, et al. 2010. Plant elongator regulates auxin-related genes during RNA polymerase II transcription elongation[J]. Proceedings of the National Academy of Sciences of the USA, 107(4): 1678-1683. [47] Nguyen K M, Busino L. 2020. The biology of F-box proteins: the SCF family of E3 ubiquitin ligases[J]. Advances in Experimental Medicine and Biology, 1217: 111-122. [48] Nijman S M, Luna-Vargas M P, Velds A, et al. 2005. A genomic and functional inventory of deubiquitinating enzymes[J]. Cell, 123(5): 773-786. [49] Nune M, Morgan M T, Connell Z, et al. 2019. FACT and Ubp10 collaborate to modulate H2B deubiquitination and nucleosome dynamics[J]. Elife, 8: e40988. [50] Pavri R, Zhu B, Li G H, et al. 2006. Histone H2B monoubiquitination functions cooperatively with FACT to regulate elongation by RNA polymerase II[J]. Cell, 125(4): 703-717. [51] Pickart C M. 2004. Back to the future with ubiquitin[J]. Cell, 116(2): 181-190. [52] Roudier F, Ahmed I, Bérard C, et al. 2011. Integrative epigenomic mapping defines four main chromatin states in Arabidopsis[J]. The EMBO Journal, 30(10): 1928-1938. [53] Schmitz R J, Tamada Y, Doyle M R, et al. 2009. Histone H2B deubiquitination is required for transcriptional activation of FLOWERING LOCUS C and for proper control of flowering in Arabidopsis[J]. Plant Physiology, 149(2): 1196-1204. [54] Selth L A, Sigurdsson S, Svejstrup J Q. 2010. Transcript elongation by RNA polymerase II[J]. Annual Review of Biochemistry, 79: 271-293. [55] Shilatifard A. 2006. Chromatin modifications by methylation and ubiquitination: Implications in the regulation of gene expression[J]. Annual Review of Biochemistry, 75: 243-269. [56] Song L, Luo Z Q. 2019. Post-translational regulation of ubiquitin signaling[J]. The Journal of Cell Biology, 218(6): 1776-1786. [57] Sun Y, Zhao J, Li X, et al. 2020. E2 conjugases UBC1 and UBC2 regulate MYB42-mediated SOS pathway in response to salt stress in Arabidopsis[J]. New Phytologist, 227(2): 455-472. [58] Suskiewicz M J, Zobel F, Ogden T E, et al. 2020. HPF1 completes the PARP active site for DNA damage-induced ADP-ribosylation[J]. Nature, 579(7800): 598-602. [59] Tanny J C, Erdjument-Bromage H, Tempst P, et al. 2007. Ubiquitylation of histone H2B controls RNA polymerase II transcription elongation independently of histone H3 methylation[J]. Genes & Development, 21(7): 835-847. [60] Wang L, Brown J L, Cao R, et al. 2004. Hierarchical recruitment of polycomb group silencing complexes[J]. Molecular Cell, 14(5): 637-646. [61] Wang P, Guo K, Su Q, et al. 2022. Histone ubiquitination controls organ size in cotton (Gossypium hirsutum)[J]. The Plant Journal, 110(4): 1005-1020. [62] Weake V M, Workman J L. 2008. Histone ubiquitination: Triggering gene activity[J]. Molecular Cell, 29(6): 653-663. [63] Woloszynska M, Le Gall S, Neyt P, et al. 2019. Histone 2B monoubiquitination complex integrates transcript elongation with RNA processing at circadian clock and flowering regulators[J]. Proceedings of the National Academy of Sciences of the USA, 116(16): 8060-8069. [64] Wood A, Krogan N J, Dover J, et al. 2003a. Bre1, an E3 ubiquitin ligase required for recruitment and substrate selection of Rad6 at a promoter[J]. Molecular Cell, 11(1): 267-274. [65] Wood A, Schneider J, Dover J, et al. 2003b. The PAF1 complex is essential for histone monoubiquitination by the Rad6-Bre1 complex, which signals for histone methylation by COMPASS and Dot1p[J]. Journal of Biological Chemistry, 278(37): 34739-34742. [66] Wood A, Schneider J, Dover J, et al. 2005. The Bur1/Bur2 complex is required for histone H2B monoubiquitination by Rad6/Bre1 and histone methylation by COMPASS[J]. Molecular Cell, 20(4): 589-599. [67] Xiao T, Kao C F, Krogan N J, et al. 2005. Histone H2B ubiquitylation is associated with elongating RNA polymerase II[J]. Molecular and Cellular Biology, 25(2): 637-651. [68] Xiao X, Liu C, Pei Y, et al. 2020. Histone H2A ubiquitination reinforces mechanical stability and asymmetry at the single-nucleosome level[J]. Journal of the American Chemical Society, 142(7): 3340-3345. [69] Xie J, Wooten M, Tran V, et al. 2015. Histone H3 threonine phosphorylation regulates asymmetric histone inheritance in the Drosophila male germline[J]. Cell, 163(4): 920-933. [70] Xu Z, Li E, Xue G, et al. 2022. OsHUB2 inhibits function of OsTrx1 in heading date in rice[J]. The Plant Journal, 110(6): 1670-1680. [71] Yang Q, Zhao J, Chen D, et al. 2021. E3 ubiquitin ligases: styles, structures and functions[J]. Molecular Biomedicine, 2(1): 23. [72] Yao T, Jing W, Hu Z, et al. 2019. Structural basis of the crosstalk between histone H2B monoubiquitination and H3 lysine 79 methylation on nucleosome[J]. Cell Research, 29(4): 330-333. [73] Zarreen F, Karim M J, Chakraborty S. 2022. The diverse roles of Histone 2b monoubiquitination in the life of plants[J]. Journal of Experimental Botany, 73(12): 3854-3865. [74] Zhang L, Luo P, Bai J, et al. 2021. Function of histone H2B monoubiquitination in transcriptional regulation of auxin biosynthesis in Arabidopsis[J]. Communications Biology, 4(1): 206. [75] Zhang Y F, Li D Y, Zhang H J, et al. 2015. Tomato histone H2B monoubiquitination enzymes SlHUB1 and SlHUB2 contribute to disease resistance against Botrytis ci- nerea through modulating the balance between SA- and JA/ET-mediated signaling pathways[J]. BMC Plant Biology, 15: 252. [76] Zhao J, Chen Q H, Zhou S, et al. 2020. H2Bub1 regulates rbohD-dependent hydrogen peroxide signal pathway in the defense responses to Verticillium dahliae toxins[J]. Plant Physiology, 182(1): 640-657. [77] Zhao T, Zhan Z, Jiang D.2019a. Histone modifications and their regulatory roles in plant development and environmental memory[J]. Journal of Genetics and Genomics, 46(10): 467-476. [78] Zhao W, Neyt P, Van Lijsebettens M, et al. 2019b. Interactive and noninteractive roles of histone H2B monoubiquitination and H3K36 methylation in the regulation of active gene transcription and control of plant growth and development[J]. New Phytologist, 221(2): 1101-1116. [79] Zheng H, Zhang F, Wang S, et al. 2018. MLK1 and MLK2 coordinate RGA and CCA1 activity to regulate hypocotyl elongation in Arabidopsis thaliana[J]. Plant Cell, 30(1): 67-82. [80] Zheng Y, Zhang S, Luo Y, et al. 2022. Rice OsUBR7 modulates plant height by regulating histone H2B monoubiquitination and cell proliferation[J]. Plant Community, 100412. [81] Zhou S, Chen Q H, Sun Y H, et al. 2017. Histone H2B monoubiquitination regulates salt stress-induced microtubule depolymerization in Arabidopsis[J]. Plant Cell and Environment, 40(8): 1512-1530. [82] Zhu B, Zheng Y, Pham A D, et al. 2005. Monoubiquitination of human histone H2B: The factors involved and their roles in HOX gene regulation[J]. Molecular Cell, 20(4): 601-611. [83] Zou B H, Yang D L, Shi Z Y, et al. 2014. Monoubiquitination of histone 2B at the disease resistance gene locus regulates its expression and impacts immune responses in Arabidopsis[J]. Plant Physiology, 165(1): 309-318.
