SPINDLY和SECRET AGENT介导的蛋白糖基化调控植物发育与逆境响应

doi:10.13560/j.cnki.biotech.bull.1985.2024-0916

摘要/Abstract

摘要：

蛋白糖基化修饰调控诸多生物学过程，尤其是在动植物发育与非生物/生物逆境胁迫响应方面，取得了很多重要的进展。O-乙酰氨基葡萄糖基化（O-GlcNAc）及O-岩藻糖基化（O-Fuc）是两类重要的蛋白翻译后修饰。其中，SECRET AGENT（SEC）和SPINDLY（SPY）作为重要的O-乙酰氨基葡萄糖转移酶（OGT）同源蛋白，分别负责O-GlcNAc和O-Fuc修饰，其在植物生长发育和逆境胁迫响应过程中发挥了重要的作用。本文系统总结了植物中蛋白的O-GlcNAc和O-Fuc修饰过程及相关酶类，分析了SEC和SPY的进化特点，重点聚焦它们参与植物发育及逆境响应的调控机制，并探讨了未来植物蛋白糖基化修饰的研究热点和挑战。

关键词: O-乙酰氨基葡萄糖基化, O-岩藻糖基化, 植物发育, 逆境响应

Abstract:

Protein glycosylation modifications play a crucial role in regulating numerous biological processes, with significant advancements made, particularly in the areas of plant and animal development as well as responses to abiotic and biotic stressors. O-GlcNAcylation (O-GlcNAc) and O-Fucosylation (O-Fuc) are two important types of protein modifications. Among them, SECRET AGENT (SEC) and SPINDLY (SPY) are key homologous proteins of O-GlcNAc transferase (OGT), responsible for O-GlcNAc modification and O-Fuc modification, respectively. They play crucial roles in plant growth, development, and stress response processes. This review provides a comprehensive overview of the O-GlcNAc and O-Fuc modification processes of proteins and their associated enzymes. It analyses the evolutionary characteristics of SEC and SPY, highlights their regulatory mechanisms in plant development and stress responses, and discusses future research hotspots and challenges in plant protein glycosylation modifications.

Key words: O-GlcNAcylation, O-Fucosylation, plant development, response to adversity

樊玥妮, 仙保山, 师艺萍, 任梦圆, 徐佳慧, 魏绍巍, 许晓敬, 罗晓峰, 舒凯. SPINDLY和SECRET AGENT介导的蛋白糖基化调控植物发育与逆境响应[J]. 生物技术通报, 2025, 41(4): 1-8.

FAN Yue-ni, XIAN Bao-shan, SHI Yi-ping, REN Meng-yuan, XU Jia-hui, WEI Shao-wei, XU Xiao-jing, LUO Xiao-feng, SHU Kai. SPINDLY and SECRET AGENT-mediated Protein Glycosylation Regulates Plant Development and Stress Response[J]. Biotechnology Bulletin, 2025, 41(4): 1-8.

图/表 2

图1 植物中SPY介导的O-岩藻糖基化及SEC介导的O-乙酰氨基葡萄糖基化示意图A：O-Fuc修饰通过O连接的岩藻糖基转移酶（protein O-fucosyltransferase， POFUT）的催化，将GDP-Fucose中的Fucose与蛋白质的丝氨酸（Ser）或苏氨酸（Thr）残基侧链羟基氧相连接；B：O-GlcNAc修饰通过O连接的N-乙酰氨基葡萄糖转移酶（O-GlcNAc transferase， OGT）的催化，将UDP-GlcNAc中的GlcNAc与蛋白质的丝氨酸（Ser）或苏氨酸（Thr）残基侧链羟基氧相连接。在动物中O-乙酰氨基葡萄糖苷酶（O-GlcNAcases， OGA）将GlcNAc移除，目前在植物中仅发现OGA类似物

Fig. 1 Schematic illustration of SPY-mediated O-Fucosylation and SEC-mediated O-GlcNAcylation in plantsA: O-Fuc modification is catalyzed by protein O-fucosyltransferase (POFUT) to link the fucose of GDP-Fucose to the hydroxyl oxygen of the serine (Ser) or threonine (Thr) residue side chain of the protein. B: O-GlcNAc modification is catalyzed by O-GlcNAc transferase (OGT) to link GlcNAc in UDP-GlcNAc to serine (Ser) or threonine (Thr) residue side-chain hydroxyl oxygen of proteins. In animals, O-GlcNAcases (OGA) can remove GlcNAc, and only OGA analogues are currently found in plants

图2 拟南芥SPY及SEC蛋白结构域示意图A：利用SMART： Main page预测拟南芥SPY和SEC的蛋白结构域；SPY及SEC均包括TPR结构域及催化结构域；灰框表示低复杂性；B：利用SWISS MODEL预测拟南芥SPY的蛋白结构域，局部放大区域为GDP-Fucose的结合位点；SPY能形成头尾二聚体构象，进行自身岩藻糖基化［24］；C：利用SWISS MODEL预测拟南芥SEC的蛋白结构域

Fig. 2 Schematic representation of the protein domains of SPY and SEC in Arabidopsis thalianaA: Protein domains of SPY and SEC in Arabidopsis thaliana were predicted using the SMART: Main page. Both SPY and SEC include the TPR domain and catalytic domain. Gray boxes indicate low complexity. B: SWISS-MODEL was used to predict the protein domain ofSPY in in A. thaliana, and the local amplification region was the binding site of GDP-Fucose. SPY can form a head-to-tail dimer conformation and fucosylate itself. C: SWISS MODEL was utilized to predict the protein domain of SEC in in A. thaliana

参考文献 61

1	Ramazi S, Allahverdi A, Zahiri J. Evaluation of post-translational modifications in histone proteins: a review on histone modification defects in developmental and neurological disorders [J]. J Biosci, 2020, 45: 135.
2	Ramazi S, Zahiri J. Posttranslational modifications in proteins: resources, tools and prediction methods [J]. Database, 2021, 2021: baab012.
3	Eichler J. Protein glycosylation [J]. Curr Biol, 2019, 29(7): R229-R231.
4	王婷, 羊欢欢, 赵弘巍, 等. 蛋白质N-糖基化在拟南芥生长周期中的变化规律及去糖基化对根发育的影响 [J]. 植物学报, 2021, 56(3): 262-274.
	Wang T, Yang HH, Zhao HW, et al. Changes of protein N-glycosylation in the growth of Arabidopsis thaliana and effects of enzymatic deglycosylation on root development [J]. Chin Bull Bot, 2021, 56(3): 262-274.
5	Joshi HJ, Narimatsu Y, Schjoldager KT, et al. SnapShot: O-glycosylation pathways across Kingdoms [J]. Cell, 2018, 172(3): 632-632.e2.
6	Mulagapati S, Koppolu V, Shantha Raju T. Decoding of O-linked glycosylation by mass spectrometry [J]. Biochemistry, 2017, 56(9): 1218-1226.
7	Aquino-Gil MO, Kupferschmid M, Shams-Eldin H, et al. Apart from rhoptries, identification of Toxoplasma gondii's O-GlcNAcylated proteins reinforces the universality of the O-GlcNAcome [J]. Front Endocrinol, 2018, 9: 450.
8	Torres-Gutiérrez E, Pérez-Cervera Y, Camoin L, et al. Identification of O-glcnacylated proteins in Trypanosoma cruzi [J]. Front Endocrinol, 2019, 10: 199.
9	Holt GD, Hart GW. The subcellular distribution of terminal N-acetylglucosamine moieties. Localization of a novel protein-saccharide linkage, O-linked GlcNAc [J]. J Biol Chem, 1986, 261(17): 8049-8057.
10	Lopaticki S, Yang ASP, John A, et al. Protein O-fucosylation in Plasmodium falciparum ensures efficient infection of mosquito and vertebrate hosts [J]. Nat Commun, 2017, 8(1): 561.
11	Haltiwanger RS, Holt GD, Hart GW. Enzymatic addition of O-GlcNAc to nuclear and cytoplasmic proteins. Identification of a uridine diphospho-N-acetylglucosamine: peptide beta-N-acetylglucosaminyltransferase [J]. J Biol Chem, 1990, 265(5): 2563-2568.
12	Dong DL, Hart GW. Purification and characterization of an O-GlcNAc selective N-acetyl-beta-D-glucosaminidase from rat spleen cytosol [J]. J Biol Chem, 1994, 269(30): 19321-19330.
13	Hart GW, Housley MP, Slawson C. Cycling of O-linked beta-N-acetylglucosamine on nucleocytoplasmic proteins [J]. Nature, 2007, 446(7139): 1017-1022.
14	Hartweck LM, Genger RK, Grey WM, et al. SECRET AGENT and SPINDLY have overlapping roles in the development of Arabidopsis thaliana L. Heyn [J]. J Exp Bot, 2006, 57(4): 865-875.
15	Zhu L, Wei XT, Cong JM, et al. Structural insights into mechanism and specificity of the plant protein O-fucosyltransferase SPINDLY [J]. Nat Commun, 2022, 13(1): 7424.
16	Iyer SPN, Hart GW. Roles of the tetratricopeptide repeat domain in O-GlcNAc transferase targeting and protein substrate specificity [J]. J Biol Chem, 2003, 278(27): 24608-24616.
17	Banerjee S, Robbins PW, Samuelson J. Molecular characterization of nucleocytosolic O-GlcNAc transferases of Giardia Lamblia and Cryptosporidium parvum [J]. Glycobiology, 2009, 19(4): 331-336.
18	Butkinaree C, Cheung WD, Park S, et al. Characterization of beta-N-acetylglucosaminidase cleavage by caspase-3 during apoptosis [J]. J Biol Chem, 2008, 283(35): 23557-23566.
19	Rao FV, Schüttelkopf AW, Dorfmueller HC, et al. Structure of a bacterial putative acetyltransferase defines the fold of the human O-GlcNAcase C-terminal domain [J]. Open Biol, 2013, 3(10): 130021.
20	He Y, Roth C, Turkenburg JP, et al. Three-dimensional structure of a Streptomyces sviceus GNAT acetyltransferase with similarity to the C-terminal domain of the human GH84 O-GlcNAcase [J]. Acta Crystallogr D Biol Crystallogr, 2014, 70(Pt 1): 186-195.
21	Yang XY, Qian K. Protein O-GlcNAcylation: emerging mechanisms and functions [J]. Nat Rev Mol Cell Biol, 2017, 18(7): 452-465.
22	Olszewski NE, West CM, Sassi SO, et al. O-GlcNAc protein modification in plants: Evolution and function [J]. Biochim Biophys Acta, 2010, 1800(2): 49-56.
23	Sun TP. Novel nucleocytoplasmic protein O-fucosylation by SPINDLY regulates diverse developmental processes in plants [J]. Curr Opin Struct Biol, 2021, 68: 113-121.
24	Kumar S, Wang Y, Zhou Y, et al. Structure and dynamics of the Arabidopsis O-fucosyltransferase SPINDLY [J]. Nat Commun, 2023, 14(1): 1538.
25	Shen A, Kamp HD, Gründling A, et al. A bifunctional O-GlcNAc transferase governs flagellar motility through anti-repression [J]. Genes Dev, 2006, 20(23): 3283-3295.
26	Hart GW. Dynamic O-linked glycosylation of nuclear and cytoskeletal proteins [J]. Annu Rev Biochem, 1997, 66: 315-335.
27	Lazarus MB, Nam Y, Jiang JY, et al. Structure of human O-GlcNAc transferase and its complex with a peptide substrate [J]. Nature, 2011, 469(7331): 564-567.
28	Zentella R, Sui N, Barnhill B, et al. The Arabidopsis O-fucosyltransferase SPINDLY activates nuclear growth repressor DELLA [J]. Nat Chem Biol, 2017, 13(5): 479-485.
29	Jacobsen SE, Binkowski KA, Olszewski NE. SPINDLY, a tetratricopeptide repeat protein involved in gibberellin signal transduction in Arabidopsis [J]. Proc Natl Acad Sci USA, 1996, 93(17): 9292-9296.
30	Cui HC, Benfey PN. Interplay between scarecrow, ga and like heterochromatin protein 1 in ground tissue patterning in the Arabidopsis root [J]. Plant J, 2009, 58(6): 1016-1027.
31	Cui HC, Kong DY, Wei PC, et al. SPINDLY, ERECTA, and its ligand STOMAGEN have a role in redox-mediated cortex proliferation in the Arabidopsis root [J]. Mol Plant, 2014, 7(12): 1727-1739.
32	Masucci JD, Rerie WG, Foreman DR, et al. The homeobox gene GLABRA2 is required for position-dependent cell differentiation in the root epidermis of Arabidopsis thaliana [J]. Development, 1996, 122(4): 1253-1260.
33	Lee MM, Schiefelbein J. WEREWOLF, a MYB-related protein in Arabidopsis, is a position-dependent regulator of epidermal cell patterning [J]. Cell, 1999, 99(5): 473-483.
34	Mutanwad KV, Zangl I, Lucyshyn D. The Arabidopsis O-fucosyltransferase SPINDLY regulates root hair patterning independently of gibberellin signaling [J]. Development, 2020, 147(19): dev192039.
35	Achard P, Renou JP, Berthomé R, et al. Plant DELLAs restrain growth and promote survival of adversity by reducing the levels of reactive oxygen species [J]. Curr Biol, 2008, 18(9): 656-660.
36	Tseng TS, Salomé PA, Robertson McClung C, et al. SPINDLY and GIGANTEA interact and act in Arabidopsis thaliana pathways involved in light responses, flowering, and rhythms in Cotyledon movements [J]. Plant Cell, 2004, 16(6): 1550-1563.
37	Xing LJ, Liu Y, Xu SJ, et al. Arabidopsis O-GlcNAc transferase SEC activates histone methyltransferase ATX1 to regulate flowering [J]. EMBO J, 2018, 37(19): e98115.
38	Xiao J, Xu SJ, Li CH, et al. O-GlcNAc-mediated interaction between VER2 and TaGRP2 elicits TaVRN1 mRNA accumulation during vernalization in winter wheat [J]. Nat Commun, 2014, 5: 4572.
39	Xing LJ, Li J, Xu YY, et al. Phosphorylation modification of wheat lectin VER2 is associated with vernalization-induced O-GlcNAc signaling and intracellular motility [J]. PLoS One, 2009, 4(3): e4854.
40	Xu SL, Chalkley RJ, Maynard JC, et al. Proteomic analysis reveals O-GlcNAc modification on proteins with key regulatory functions in Arabidopsis [J]. Proc Natl Acad Sci USA, 2017, 114(8): E1536-E1543.
41	Bi Y, Deng ZP, Ni WM, et al. Arabidopsis ACINUS is O-glycosylated and regulates transcription and alternative splicing of regulators of reproductive transitions [J]. Nat Commun, 2021, 12(1): 945.
42	Quilichini TD, Friedmann MC, Lacey Samuels A, et al. ATP-binding cassette transporter G26 is required for male fertility and pollen exine formation in Arabidopsis [J]. Plant Physiol, 2010, 154(2): 678-690.
43	Qin F, Kodaira KS, Maruyama K, et al. SPINDLY, a negative regulator of gibberellic acid signaling, is involved in the plant abiotic stress response [J]. Plant Physiol, 2011, 157(4): 1900-1913.
44	Phokas A, Coates JC. Evolution of DELLA function and signaling in land plants [J]. Evol Dev, 2021, 23(3): 137-154.
45	Shimada A, Ueguchi-Tanaka M, Sakamoto T, et al. The rice SPINDLY gene functions as a negative regulator of gibberellin signaling by controlling the suppressive function of the DELLA protein, SLR1 and modulating brassinosteroid synthesis [J]. Plant J, 2006, 48(3): 390-402.
46	Sarnowska EA, Rolicka AT, Bucior E, et al. DELLA-interacting SWI3C core subunit of switch/sucrose nonfermenting chromatin remodeling complex modulates gibberellin responses and hormonal cross talk in Arabidopsis [J]. Plant Physiol, 2013, 163(1): 305-317.
47	Steiner E, Efroni I, Gopalraj M, et al. The Arabidopsis O-linked N-acetylglucosamine transferase SPINDLY interacts with class I TCPs to facilitate cytokinin responses in leaves and flowers [J]. Plant Cell, 2012, 24(1): 96-108.
48	Greenboim-Wainberg Y, Maymon I, Borochov R, et al. Cross talk between gibberellin and cytokinin: the Arabidopsis GA response inhibitor SPINDLY plays a positive role in cytokinin signaling [J]. Plant Cell, 2005, 17(1): 92-102.
49	Liang L, Yang J, Gao ZX, et al. SPINDLY is involved in ABA signaling bypassing the PYR/PYLs/RCARs-mediated pathway and partly through functional ABAR [J]. Environ Exp Bot, 2018, 151: 43-54.
50	Liang L, Wang Q, Song ZH, et al. O- fucosylation of CPN20 by SPINDLY derepresses abscisic acid signaling during seed germination and seedling development [J]. Front Plant Sci, 2021, 12: 724144.
51	Xu J, Liu SD, Cai LC, et al. SPINDLY interacts with EIN2 to facilitate ethylene signalling-mediated fruit ripening in tomato [J]. Plant Biotechnol J, 2023, 21(1): 219-231.
52	Wang Y, He YQ, Su C, et al. Nuclear localized O-fucosyltransferase SPY facilitates PRR5 proteolysis to fine-tune the pace of Arabidopsis circadian clock [J]. Mol Plant, 2020, 13(3): 446-458.
53	Cui HC. Cortex proliferation in the root is a protective mechanism against abiotic stress [J]. Plant Signal Behav, 2015, 10(5): e1011949.
54	Sakuma Y, Liu Q, Dubouzet JG, et al. DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold-inducible gene expression [J]. Biochem Biophys Res Commun, 2002, 290(3): 998-1009.
55	Kang HG, Kim J, Kim B, et al. Overexpression of FTL1/DDF1, an AP2 transcription factor, enhances tolerance to cold, drought, and heat stresses in Arabidopsis thaliana [J]. Plant Sci, 2011, 180(4): 634-641.
56	Xu J, Huang ZL, Du HY, et al. SEC1-C3H39 module fine-tunes cold tolerance by mediating its target mRNA degradation in tomato [J]. New Phytol, 2023, 237(3): 870-884.
57	Filardo F, Robertson M, Singh DP, et al. Functional analysis of HvSPY, a negative regulator of GA response, in barley aleurone cells and Arabidopsis [J]. Planta, 2009, 229(3): 523-537.
58	Rodamilans B, Valli A, García JA. Molecular plant-plum pox virus interactions [J]. Mol Plant Microbe Interact, 2020, 33(1): 6-17.
59	Pérez JD, Udeshi ND, Shabanowitz J, et al. O-GlcNAc modification of the coat protein of the potyvirus Plum pox virus enhances viral infection [J]. Virology, 2013, 442(2): 122-131.
60	Chen D, Juárez S, Hartweck L, et al. Identification of secret agent as the O-GlcNAc transferase that participates in Plum pox virus infection [J]. J Virol, 2005, 79(15): 9381-9387.
61	Li XL, Lei C, Song QT, et al. Chemoproteomic profiling of O-GlcNAcylated proteins and identification of O-GlcNAc transferases in rice [J]. Plant Biotechnol J, 2023, 21(4): 742-753.

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[10]	华明;杨先慈. 受体蛋白激酶和植物发育[J]. , 2000, 0(02): 23-27.
[11]	王伟. 植物发育研究进展及前景[J]. , 1996, 0(06): 5-7.
[12]	邵宏波;初立业. 组织培养和用于研究植物发育的转基因植物[J]. , 1992, 0(12): 1-4.
[13]	王璋瑜;. “自杀基因”能在植物中倒戈[J]. , 1989, 0(03): 23-23.