Advances in the Studies of Plant Protein Post-translational Modification

doi:10.13560/j.cnki.biotech.bull.1985.2020-0946

Abstract

Abstract:

Protein post-translational modification（PTMs）is an important cellular regulatory mechanism. It regulates the activity,structure,positioning and interaction between proteins by covalently binding some chemical small molecular groups on the amino acid side chains of proteins,thereby fine-tuning the dynamic changes of protein’s biological functions. PTMs are one of the fastest and earliest responses of plants to environmental changes. They are the key mechanism of plant proteome diversity and play an important role in plant growth and development and environmental adaptation. This article mainly introduces the research progress of plant PTMs such as phosphorylation,acetylation,succinylation,glycosylation,ubiquitination,crotonylation,S-nitrosylation,2-hydroxyisobutylation,etc. in recent years,aiming to provide references for understanding the key biological functions and research prospects of plant PTMs.

Key words: post-translational modification, proteome, phosphorylation, acetylation, ubiquitination

LIU Jing, LI Ya-chao, ZHOU Meng-yan, WU Peng-fei, MA Xiang-qing, LI Ming. Advances in the Studies of Plant Protein Post-translational Modification[J]. Biotechnology Bulletin, 2021, 37(1): 67-76.

Figures/Tables 1

References 65

[1]	Millar AH, Heazlewood JL, Giglione C, et al. The scope, functions, and dynamics of posttranslational protein modifications[J]. Annual Review of Plant Biology, 2019,70:119-151.
[2]	阮班军, 代鹏, 王伟, 等. 蛋白质翻译后修饰研究进展[J]. 中国细胞生物学学报, 2014(7):1027-1037.
	Ruan BJ, Dai P, Wang W, et al. Progress on post-translational modifi cation of proteins[J]. Chinese Journal of Cell Biology, 2014(7):1027-1037.
[3]	Zhu JK. Abiotic stress signaling and responses in plants[J]. Cell, 2016,167(2):313-324. URL pmid: 27716505
[4]	Withers J, Dong X. Post-translational regulation of plant immunity[J]. Current Opinion in Plant Biology, 2017,38:124-132.
[5]	刘雅琼, 侯岁稳. 蛋白磷酸化修饰在植物-病原微生物互作中的作用研究进展[J]. 植物学报, 2019,54(2):168-184.
	Liu YQ, Hou SW. Research progress on the role of protein phosphorylation modification in plant-pathogen microorganism interaction[J]. Chinese Bulletin of Botany, 2019,54(2):168-184.
[6]	Moulinier-Anzola J, Schwihla M, De-Araujo L, et al. TOLs function as ubiquitin receptors in the early steps of the ESCRT pathway in higher plants[J]. Molecular Plant, 2020,13(5):717-731.
[7]	Nagashima Y, von Schaewen A, Koiwa H. Function of N-glycosylation in plants[J]. Plant Science, 2018,274:70-79.
[8]	Liu W, Zhang B, He W, et al. Characterization of in vivo phosphorylation modification of differentially accumulated proteins in cotton fiber-initiation process[J]. Acta Biochimica et Biophysica Sinica, 2016,48(8):756-761.
[9]	Mizoi J, Kanazawa N, Kidokoro S, et al. Heat-induced inhibition of phosphorylation of the stress-protective transcription factor DREB2A promotes thermotolerance of Arabidopsis thaliana[J]. Journal of Biological Chemistry, 2019,294(3):902-917.
[10]	Furuya T, Matsuoka D, Nanmori T. Phosphorylation of Arabidopsis thaliana MEKK1 via Ca ²⁺ signaling as a part of the cold stress response [J]. Journal of Plant Research, 2013,126(6):833-840. doi: 10.1007/s10265-013-0576-0 URL pmid: 23857079
[11]	Yu X, Dong J, Deng Z, et al. Arabidopsis PP6 phosphatases dephosphorylate PIF proteins to repress photomorphogenesis[J]. Proceedings of the National Academy of Sciences of the United States of America, 2019,116(40):20218-20225. doi: 10.1073/pnas.1907540116 URL pmid: 31527236
[12]	Pi E, Qu L, Hu J, et al. Mechanisms of soybean roots’ tolerances to salinity revealed by proteomic and phosphoproteomic comparisons between two cultivars[J]. Molecular & Cellular Proteomics, 2016,15(1):266-288. doi: 10.1074/mcp.M115.051961 URL pmid: 26407991
[13]	常丽丽, 王力敏, 郭安平, 等. 木薯叶片响应干旱胁迫的磷酸化蛋白质组差异分析[J]. 植物生理学报, 2018,54(1):133-144.
	Chang LL, Wang LM, Guo AP, et al. Difference analysis of phosphorylated proteome in cassava leaves in response to drought stress[J]. Plant Physiology Journal, 2018,54(1):133-144.
[14]	Yang J, Xie M, Yang X, et al. Phosphoproteomic profiling reveals the importance of CK2, MAPKs and CDPKs in response to phosphate starvation in rice[J]. Plant and Cell Physiology, 2019,60(12):2785-2796.
[15]	Zhou Y, Zhang Z, Zheng C, et al. Nitrogen regulates CRY1 phosphorylation and circadian clock input pathways[J]. Plant Signaling & Behavior, 2016,11(9):e1219830. URL pmid: 27617369
[16]	Wang Q, Qin G, Cao M, et al. A phosphorylation-based switch controls TAA1-mediated auxin biosynjournal in plants[J]. Nature Communications, 2020,11(1):679. URL pmid: 32015349
[17]	Wang J, Liu X, Zhang A, et al. A cyclic nucleotide-gated channel mediates cytoplasmic calcium elevation and disease resistance in rice[J]. Cell Research, 2019,29(10):820-831. doi: 10.1038/s41422-019-0219-7 URL pmid: 31444468
[18]	Zhang Y, Song L, Liang W, et al. Comprehensive profiling of lysine acetylproteome analysis reveals diverse functions of lysine acetylation in common wheat[J]. Scientific Reports, 2016,6:21069. doi: 10.1038/srep21069 URL pmid: 26875666
[19]	王峰, 闫家榕, 陈雪玉, 等. 光调控植物叶绿素生物合成的研究进展[J]. 园艺学报, 2019,46(5):164-183.
	Wang F, Yan JR, Chen XY, et al. Research progress of light regulation of plant chlorophyll biosynjournal[J]. Journal of Horticulture, 2019,46(5):164-183.
[20]	Li X, Ye J, Ma H, et al. Proteomic analysis of lysine acetylation provides strong evidence for involvement of acetylated proteins in plant meiosis and tapetum function[J]. The Plant Journal, 2018,93(1):142-154.
[21]	Xue C, Liu S, Chen C, et al. Global proteome analysis links lysine acetylation to diverse functions in Oryza sativa[J]. Proteomics, 2018,18(1):17000361.
[22]	Lu Y, Xu Q, Liu Y, et al. Dynamics and functional interplay of histone lysine butyrylation, crotonylation, and acetylation in rice under starvation and submergence[J]. Genome Biology, 2018,19:144. URL pmid: 30253806
[23]	Liao CJ, Lai Z, Lee S, et al. Arabidopsis HOOKLESS1 regulates responses to pathogens and abscisic acid through interaction with MED18 and acetylation of WRKY33 and ABI5 chromatin[J]. The Plant Cell, 2016,28(7):1662-1681. doi: 10.1105/tpc.16.00105 URL pmid: 27317674
[24]	李蓉, 陈雪岚. 蛋白质赖氨酸残基的琥珀酰化修饰[J]. 中国生物化学与分子生物学报, 2018,34(12):1272-1279.
	Li R, Chen XL. Succinylation modification of protein lysine residues[J]. Chinese Journal of Biochemistry and Molecular Biology, 2018,34(12):1272-1279.
[25]	Meng X, Mujahid H, Zhang Y, et al. Comprehensive analysis of the lysine succinylome and protein co-modifications in developing rice seeds[J]. Molecular & Cellular Proteomics, 2019,18(12):2359-2372. doi: 10.1074/mcp.RA119.001426 URL pmid: 31492684
[26]	Zhang Y, Wang G, Song L. et al. Global analysis of protein lysine succinylation profiles in common wheat[J]. BMC Genomics, 2017,18(1):309. doi: 10.1186/s12864-017-3698-2 URL pmid: 28427325
[27]	Xu Y, Shen C, Ma J, et al. Quantitative succinyl-proteome profiling of Camellia sinensis cv. ‘Anji Baicha’ during periodic albinism[J]. Scientific Reports, 2017,7(1):1873. doi: 10.1038/s41598-017-02128-x URL pmid: 28500349
[28]	Yuan H, Chen J, Yang Y, et al. Quantitative succinyl-proteome profiling of Chinese hickory(Carya cathayensis)during the grafting process[J]. BMC Plant Biology, 2019,19(1):467. doi: 10.1186/s12870-019-2072-8 URL pmid: 31684873
[29]	王晓龙, 王秀然, 卢天成. 蛋白质糖基化修饰的研究进展[J]. 基因组学与应用生物学, 2017,36(10):4380-4384.
	Wang XL, Wang XR, Lu TC. Research progress of protein glycosylation modification[J]. Genomics and Applied Biology, 2017,36(10):4380-4384.
[30]	Strasser R. Plant protein glycosylation[J]. Glycobiology, 2016,26(9):926-939. doi: 10.1093/glycob/cww023 URL
[31]	Ying J, Zhao J, Hou Y, et al. Mapping the N-linked glycosites of rice(Oryza sativa L.)germinating embryos[J]. PLoS One, 2017,12(3):e0173853. doi: 10.1371/journal.pone.0173853 URL pmid: 28328971
[32]	Wang J, Wen H, Li M, et al. N-Glycoproteome reveals that N-Glycosylation plays crucial roles in photosynjournal and carbon metabolism in young rice leaves[J]. Journal of Plant Biology, 2020,63(3):165-175. doi: 10.1007/s12374-020-09243-9 URL
[33]	Xing L, Liu Y, Xu S, et al. Arabidopsis O-GlcNAc transferase SEC activates histone methyltransferase ATX1 to regulate flowering[J]. EMBO Journal, 2018,37:e9811519.
[34]	Chen L, Huang X, Zhao S, et al. IPyA glucosylation mediates light and temperature signaling to regulate auxin-dependent hypocotyl elongation in Arabidopsis[J]. Proceedings of the National Academy of Sciences of the United States of America, 2020,117(12):6910-6917. doi: 10.1073/pnas.2000172117 URL pmid: 32152121
[35]	王志凤. 小黑杨花芽和叶芽糖基化蛋白质组学研究[D]. 哈尔滨:东北林业大学, 2014.
	Wang ZF. Glycosylation proteomics research of flower bud and leaf bud from P. simonii×P. nigra[D]. Harbin:Northeast Forestry University, 2014.
[36]	Chen X, Liu C, Tang B, et al. Quantitative proteomics analysis reveals important roles of N-glycosylation on ER quality control system for development and pathogenesis in Magnaporthe oryzae[J]. PLoS Pathogens, 2020,16(2):e1008355. doi: 10.1371/journal.ppat.1008355 URL pmid: 32092131
[37]	Liu C, Xing J, Cai X, et al. GPI7-mediated glycosylphosphatidylinositol anchoring regulates appressorial penetration and immune evasion during infection of Magnaporthe oryzae[J]. Environmental Microbiology, 2020,22(7):2581-2595. doi: 10.1111/1462-2920.14941 URL pmid: 32064718
[38]	Chen X, Shi T, Yang J, et al. N-glycosylation of effector proteins by an alpha-1, 3-mannosyltransferase is required for the rice blast fungus to evade host innate immunity[J]. The Plant Cell, 2014,26(3):1360-1376. doi: 10.1105/tpc.114.123588 URL pmid: 24642938
[39]	于菲菲, 谢旗. 泛素化修饰调控脱落酸介导的信号途径[J]. 遗传, 2017,39(8):692-706. pmid: 28903897
	Yu FF, Xie Q. Ubiquitination modification regulates abscisic acid-mediated signaling pathway[J]. Hereditas, 2017,39(8):692-706. doi: 10.16288/j.yczz.17-043 URL pmid: 28903897
[40]	Romero-Barrios N, Monachello D, Dolde U, et al. Advanced cataloging of lysine-63 polyubiquitin networks by genomic, interactome, and sensor-based proteomic analyses[J]. The Plant Cell, 2020,32(1):123-138. doi: 10.1105/tpc.19.00568 URL pmid: 31712406
[41]	Xie H, Wang Y, Ding Y, et al. Global ubiquitome profiling revealed the roles of ubiquitinated proteins in metabolic pathways of tea leaves in responding to drought stress[J]. Scientific Reports, 2019,9(1):4286. URL pmid: 30862833
[42]	He D, Li M, Damaris RN, et al. Quantitative ubiquitylomics approach for characterizing the dynamic change and extensive modulation of ubiquitylation in rice seed germination[J]. The Plant Journal, 2020,101(6):1430-1447. URL pmid: 31677306
[43]	Guo J, Liu J, Wei Q, et al. Proteomes and ubiquitylomes analysis reveals the involvement of ubiquitination in protein degradation in petunias[J]. Plant Physiology, 2017,173(1):668-687. doi: 10.1104/pp.16.00795 URL pmid: 27810942
[44]	Pan W, Wu Y, Xie Q. Regulation of ubiquitination is central to the phosphate starvation response[J]. Trends in Plant Science, 2019,24(8):755-769. doi: 10.1016/j.tplants.2019.05.002 URL pmid: 31176527
[45]	Suen D, Tsai Y, Cheng Y, et al. The deubiquitinase OTU5 regulates root responses to phosphate starvation[J]. Plant Physiology, 2018,176(3):2441-2455. doi: 10.1104/pp.17.01525 URL pmid: 29301952
[46]	胡婷丽, 李魏, 刘雄伦, 等. 泛素化在植物抗病中的作用[J]. 微生物学通报, 2014,41(6):1175-1179.
	Hu TL, Li W, Liu XL, et al. The role of ubiquitination in plant disease resistance[J]. Microbiology Bulletin, 2014,41(6):1175-1179.
[47]	Tan M, Luo H, Lee S, et al. Identification of 67 histone marks and histone lysine crotonylation as a new type of histone modification[J]. Cell, 2011,146(6):1015-1027.
[48]	Liu S, Xue C, Fang Y, et al. Global involvement of lysine crotonylation in protein modification and transcription regulation in rice[J]. Molecular & Cellular Proteomics, 2018,17(10):1922-1936. URL pmid: 30021883
[49]	Sun H, Liu X, Li F, et al. First comprehensive proteome analysis of lysine crotonylation in seedling leaves of Nicotiana tabacum[J]. Scientific Reports, 2017,7(1):3013.
[50]	Sun J, Qiu C, Qian W, et al. Ammonium triggered the response mechanism of lysine crotonylome in tea plants[J]. BMC Genomics, 2019,20(1):340. doi: 10.1186/s12864-019-5716-z URL pmid: 31060518
[51]	Liu K, Yuan C, Li H, et al. A qualitative proteome-wide lysine crotonylation profiling of papaya(Carica papaya L.)[J]. Scientific Reports, 2018,8(1):8230. URL pmid: 29844531
[52]	Feng J, Chen L, Zuo J. Protein S-Nitrosylation in plants:Current progresses and challenges[J]. Journal of Integrative Plant Biology, 2019,61(12):1206-1223. doi: 10.1111/jipb.12780 URL pmid: 30663237
[53]	陈立超, 詹妮, 李彦莎, 等. 植物蛋白质S-亚硝基化修饰的检测与分析[J]. 植物学报, 2019,54(4):497-502.
	Chen LC, Zhan N, Li YS, et al. Detection and analysis of protein S-nitrosylation in plants[J]. Chinese Bulletin of Botany, 2019,54(4):497-502.
[54]	Lin A, Wang Y, Tang J, et al. Nitric oxide and protein S-nitrosylation are integral to hydrogen peroxide-induced leaf cell death in rice[J]. Plant Physiology, 2012,158(1):451-464. doi: 10.1104/pp.111.184531 URL pmid: 22106097
[55]	Yang H, Mu J, Chen L, et al. S-Nitrosylation positively regulates ascorbate peroxidase activity during plant stress responses[J]. Plant Physiology, 2015,167(4):1604-1753. doi: 10.1104/pp.114.255216 URL pmid: 25667317
[56]	Hu J, Huang X, Chen L, et al. Site-specific Nitrosoproteomic identification of endogenously S-Nitrosylated proteins in Arabidopsis[J]. Plant Physiology, 2015,167(4):1731-1746. doi: 10.1104/pp.15.00026 URL pmid: 25699590
[57]	Gong B, Yan Y, Zhang L, et al. Unravelling GSNOR-mediated S-nitrosylation and multiple developmental programs in tomato plants[J]. Plant and Cell Physiology, 2019,60(11):2523-2537.
[58]	Dai L, Peng C, Montellier E, et al. Lysine 2-hydroxyisobutyrylation is a widely distributed active histone mark[J]. Nature Chemical Biology, 2014,10(5):365-373. URL pmid: 24681537
[59]	Yu Z, Ni J, Sheng W, et al. Proteome-wide identification of lysine 2-hydroxyisobutyrylation reveals conserved and novel histone modifications in Physcomitrella patens[J]. Scientific Reports, 2017,7(1):15553.
[60]	Meng X, Xing S, Perez LM, et al. Proteome-wide analysis of Lysine 2-hydroxyisobutyrylation in developing rice(Oryza sativa)seeds[J]. Scientific Reports, 2017,7(1):17486. doi: 10.1038/s41598-017-17756-6 URL pmid: 29235492
[61]	Liu S, Liu G, Cheng P, et al. Genome-wide profiling of histone lysine butyrylation reveals its role in the positive regulation of gene transcription in rice[J]. Rice, 2019,12(1):1-12. URL pmid: 30631971
[62]	Yang M, Huang H, Ge F. Lysine propionylation is a widespread post-translational modification involved in regulation of photosynjournal and metabolism in cyanobacteria[J]. International Journal of Molecular Sciences, 2019,20(19):4792.
[63]	Cao Y, Fan G, Wang Z, et al. Phytoplasma-induced changes in the acetylome and succinylome of paulownia tomentosa provide evidence for involvement of acetylated proteins in witches’ broom disease[J]. Molecular & Cellular Proteomics, 2019,18(6):1210-1226. doi: 10.1074/mcp.RA118.001104 URL pmid: 30936209
[64]	He D, Wang Q, Li M, et al. Global proteome analyses of lysine acetylation and succinylation reveal the widespread involvement of both modification in metabolism in the embryo of germinating rice seed[J]. Journal of Proteome Research, 2016,15(3):879-890. doi: 10.1021/acs.jproteome.5b00805 URL pmid: 26767346
[65]	张玉梅. 小麦苗期盐胁迫相关转录组表达谱及蛋白质乙酰化和琥珀酰化修饰研究[D]. 沈阳:沈阳农业大学, 2016.
	Zhang YM. Transcriptome analysis and protein acetylation and succinylation study of wheat seedling in response to salt stress[D]. Shenyang:Shenyang Agricultural University, 2016.

修饰类型	蛋白数量	位点数量
磷酸化	89 022	326 848
赖氨酸乙酰化	10 518	21 235
赖氨酸泛素化	6 622	14 131
N端蛋白水解	5 884	1 021
赖氨酸2-羟基异丁酰化	4 554	19 256
N末端乙酰化	4 266	4 572
S-亚磺酰化	3 875	6 496
可逆半胱氨酸氧化	2 963	4 302
赖氨酸丙二酸化	2 938	5 772
N-糖基化	2 821	5 027
亚硝基化	2 176	2 942
赖氨酸琥珀酰化	2 170	4 662
蛋氨酸氧化	921	1 287
N-乙酰葡萄糖胺	430	838
羰基化	223	404
肉豆蔻酰化	166	166
赖氨酸类泛素化	140	173
S-氰基化	132	148
S-谷胱甘肽酰化	46	66
N端泛素化	24	24
赖氨酸甲基化	11	17

修饰类型	蛋白数量	位点数量
磷酸化	89 022	326 848
赖氨酸乙酰化	10 518	21 235
赖氨酸泛素化	6 622	14 131
N端蛋白水解	5 884	1 021
赖氨酸2-羟基异丁酰化	4 554	19 256
N末端乙酰化	4 266	4 572
S-亚磺酰化	3 875	6 496
可逆半胱氨酸氧化	2 963	4 302
赖氨酸丙二酸化	2 938	5 772
N-糖基化	2 821	5 027
亚硝基化	2 176	2 942
赖氨酸琥珀酰化	2 170	4 662
蛋氨酸氧化	921	1 287
N-乙酰葡萄糖胺	430	838
羰基化	223	404
肉豆蔻酰化	166	166
赖氨酸类泛素化	140	173
S-氰基化	132	148
S-谷胱甘肽酰化	46	66
N端泛素化	24	24
赖氨酸甲基化	11	17