AtRGS1胞吞动态调控G蛋白参与拟南芥生长发育和抗性反应

doi:10.13560/j.cnki.biotech.bull.1985.2021-0849

摘要/Abstract

摘要：

异源三聚体G蛋白由Gα、Gβ和Gγ 3个亚基组成,是普遍存在于真核细胞中的跨膜信号转导因子。植物细胞通过定位于细胞质膜的G蛋白信号调节子RGS蛋白（regulator of G protein signaling）,调控异源三聚体G蛋白的活性,进而参与生长发育、激素和糖信号转导以及抗病反应等多个重要生物学过程。膜蛋白可通过胞吞循环调控其在细胞质膜上的数量,以响应外界环境因子和自身发育信号。近年来,研究表明多种外界信号诱导拟南芥AtRGS1蛋白的胞吞,进而促进其与Gα亚基的解离,游离的Gα-GTP、Gβγ亚基和定位于内含体的AtRGS1蛋白均可能调控下游信号转导,进而影响相应生物学过程。本文综述了AtRGS1通过胞吞作用调控G蛋白参与的生长发育和抗性反应的分子细胞学机制研究进展,以期为深入理解G蛋白信号调节子影响植物发育进程和抗性反应的作用机制提供理论参考,为植物膜蛋白胞吞调控信号转导提供新的视角。

关键词: 拟南芥, AtRGS1, G蛋白, 胞吞作用, 生长发育, 抗性反应

Abstract:

Heterotrimeric G protein complex, classically consisting of Gα,Gβ,and Gγ subunits, mediates an essential signaling pathway across the PM (plasma membrane) in most eukaryotes. In plants, heterotrimeric G proteins regulate multiple biological processes such as plant growth and development, hormones and sugar signal transduction, and defense processes via RGS（regulator of G-protein signaling protein）protein in PM. The endocytosis of PM-localized proteins is involved in the control of their quantity on the PM in response to environmental stimuli and development signals. In Arabidopsis, several studies recently revealed that various external signals induced the endocytosis of AtRGS1, thus promoted the dissociation of AtRGS1 from Gα. Free Gα-GTP,Gβγ subgroup, and internalized AtRGS1 protein could regulate downstream signal transduction, thus affect the corresponding biological processes. In this review, we give an overview of the molecular cytological mechanism of AtRGS1 endocytosis in G-protein-mediated plant development and stress responses in Arabidopsis, aiming to provide a theoretical reference for deep understanding how RGS affects the plants development process and stress responses, as well as shed a new insight on the regulation of signal transduction by endocytosis of PM proteins.

Key words: Arabidopsis, AtRGS1, G proteins, endocytosis, growth and development, stress responses

古盼, 齐学影, 李莉, 张曦, 单晓昳. AtRGS1胞吞动态调控G蛋白参与拟南芥生长发育和抗性反应[J]. 生物技术通报, 2022, 38(6): 34-42.

GU Pan, QI Xue-ying, LI Li, ZHANG Xi, SHAN Xiao-yi. Endocytosis of AtRGS1 Involved in the Regulation of G-protein-mediated Arabidopsis Development and Stress Responses[J]. Biotechnology Bulletin, 2022, 38(6): 34-42.

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参考文献 43

[1]	Urano D, Chen JG, Botella JR, et al. Heterotrimeric G protein signalling in the plant kingdom[J]. Open Biol, 2013, 3(3):120186.
[2]	Gilman AG. G proteins:transducers of receptor-generated signals[J]. Annu Rev Biochem, 1987, 56:615-649. pmid: 3113327
[3]	Ma H, Yanofsky MF, Huang H. Isolation and sequence analysis of TGA1 cDNAs encoding a tomato G protein alpha subunit[J]. Gene, 1991, 107(2):189-195. pmid: 1748292
[4]	Weiss CA, Garnaat CW, Mukai K, et al. Isolation of cDNAs encoding guanine nucleotide-binding protein beta-subunit homologues from maize(ZGB1)and Arabidopsis(AGB1)[J]. PNAS, 1994, 91(20):9554-9558. pmid: 7937804
[5]	Mason MG, Botella JR. Completing the heterotrimer:isolation and characterization of an Arabidopsis thaliana G protein gamma-subunit cDNA[J]. PNAS, 2000, 97(26):14784-14788. pmid: 11121078
[6]	Mason MG, Botella JR. Isolation of a novel G-protein gamma-subunit from Arabidopsis thaliana and its interaction with Gbeta[J]. Biochim et Biophys Acta, 2001, 1520(2):147-153.
[7]	Lee YR, Assmann SM. Arabidopsis thaliana ‘extra-large GTP-binding protein’(AtXLG1):a new class of G-protein[J]. Plant Mol Biol, 1999, 40(1):55-64. pmid: 10394945
[8]	Seo HS, Kim HY, Jeong JY, et al. Molecular cloning and characterization of RGA1 encoding a G protein alpha subunit from rice(Oryza sativa L. IR-36)[J]. Plant Mol Biol, 1995, 27(6):1119-1131. pmid: 7766894
[9]	Kato C, Mizutani T, Tamaki H, et al. Characterization of heterotrimeric G protein complexes in rice plasma membrane[J]. Plant J, 2004, 38(2):320-331. doi: 10.1111/j.1365-313X.2004.02046.x URL
[10]	Ishikawa A, Iwasaki Y, Asahi T. Molecular cloning and characterization of a cDNA for the beta subunit of a G protein from rice[J]. Plant Cell Physiol, 1996, 37(2):223-228. pmid: 8665097
[11]	Li JH, Liu YQ, Lü P, et al. A signaling pathway linking nitric oxide production to heterotrimeric G protein and hydrogen peroxide regulates extracellular calmodulin induction of stomatal closure in Arabidopsis[J]. Plant Physiol, 2009, 150(1):114-124. doi: 10.1104/pp.109.137067 URL
[12]	Chen JG, Willard FS, Huang JR, et al. A seven-transmembrane RGS protein that modulates plant cell proliferation[J]. Science, 2003, 301(5640):1728-1731. doi: 10.1126/science.1087790 URL
[13]	Johnston CA, Taylor JP, Gao Y, et al. GTPase acceleration as the rate-limiting step in Arabidopsis G protein-coupled sugar signaling[J]. PNAS, 2007, 104(44):17317-17322. doi: 10.1073/pnas.0704751104 URL
[14]	Zappel NF, Panstruga R. Heterogeneity and lateral compartmentalization of plant plasma membranes[J]. Curr Opin Plant Biol, 2008, 11(6):632-640. doi: 10.1016/j.pbi.2008.07.002 URL
[15]	Denisov IG, Sligar SG. Nanodiscs for structural and functional studies of membrane proteins[J]. Nat Struct Mol Biol, 2016, 23(6):481-486. doi: 10.1038/nsmb.3195 pmid: 27273631
[16]	Grant BD, Donaldson JG. Pathways and mechanisms of endocytic recycling[J]. Nat Rev Mol Cell Biol, 2009, 10(9):597-608.
[17]	Doherty GJ, McMahon HT. Mechanisms of endocytosis[J]. Annu Rev Biochem, 2009, 78(1):857-902. doi: 10.1146/annurev.biochem.78.081307.110540 URL
[18]	Paez Valencia J, Goodman K, Otegui MS. Endocytosis and endosomal trafficking in plants[J]. Annu Rev Plant Biol, 2016, 67:309-335. doi: 10.1146/annurev-arplant-043015-112242 pmid: 27128466
[19]	Urano D, Phan N, Jones JC, et al. Endocytosis of the seven-transmembrane RGS1 protein activates G-protein-coupled signalling in Arabidopsis[J]. Nat Cell Biol, 2012, 14(10):1079-1088. doi: 10.1038/ncb2568 URL
[20]	Zhang X, Cui Y, Yu M, et al. Phosphorylation-mediated dynamics of nitrate transceptor NRT1. 1 regulate auxin flux and nitrate signaling in lateral root growth[J]. Plant Physiol, 2019, 181(2):480-498. doi: 10.1104/pp.19.00346 pmid: 31431511
[21]	Fan L, Li R, Pan J, et al. Endocytosis and its regulation in plants[J]. Trends Plant Sci, 2015, 20(6):388-397. doi: 10.1016/j.tplants.2015.03.014 URL
[22]	Chen X, Irani NG, Friml J. Clathrin-mediated endocytosis:the gateway into plant cells[J]. Curr Opin Plant Biol, 2011, 14(6):674-682. doi: 10.1016/j.pbi.2011.08.006 pmid: 21945181
[23]	Li R, Liu P, Wan Y, et al. A membrane microdomain-associated protein, Arabidopsis Flot1, is involved in a clathrin-independent endocytic pathway and is required for seedling development[J]. Plant Cell, 2012, 24(5):2105-2122. doi: 10.1105/tpc.112.095695 URL
[24]	Offringa R, Huang F. Phosphorylation-dependent trafficking of plasma membrane proteins in animal and plant cells[J]. J Integr Plant Biol, 2013, 55(9):789-808. doi: 10.1111/jipb.12096
[25]	Prak S, Hem S, Boudet J, et al. Multiple phosphorylations in the C-terminal tail of plant plasma membrane aquaporins:role in subcellular trafficking of AtPIP2;1 in response to salt stress[J]. Mol Cell Proteom, 2008, 7(6):1019-1030. doi: 10.1074/mcp.M700566-MCP200 URL
[26]	Erwig J, Ghareeb H, Kopischke M, et al. Chitin-induced and chitin elicitor receptor kinase1(CERK1)phosphorylation-dependent endocytosis of Arabidopsis thaliana lysin motif-containing receptor-like kinase5(LYK5)[J]. New Phytol, 2017, 215(1):382-396. doi: 10.1111/nph.14592 pmid: 28513921
[27]	Xue Y, Xing J, Wan Y, et al. Arabidopsis blue light receptor phototropin 1 undergoes blue light-induced activation in membrane microdomains[J]. Mol Plant, 2018, 11(6):846-859. doi: 10.1016/j.molp.2018.04.003 URL
[28]	Ullah H, Chen JG, Wang S, et al. Role of a heterotrimeric G protein in regulation of Arabidopsis seed germination[J]. Plant Physiol, 2002, 129(2):897-907. doi: 10.1104/pp.005017 URL
[29]	Pandey S, Chen JG, Jones AM, et al. G-protein complex mutants are hypersensitive to abscisic acid regulation of germination and postgermination development[J]. Plant Physiol, 2006, 141(1):243-256. doi: 10.1104/pp.106.079038 pmid: 16581874
[30]	Chen JG, Jones AM. AtRGS1 function in Arabidopsis thaliana[J]. Methods Enzymol, 2004, 389:338-350.
[31]	Fu Y, Lim S, Urano D, et al. Reciprocal encoding of signal intensity and duration in a glucose-sensing circuit[J]. Cell, 2014, 156(5):1084-1095. doi: 10.1016/j.cell.2014.01.013 URL
[32]	Thomma BPHJ, Nürnberger T, Joosten MHAJ. Of PAMPs and effectors:the blurred PTI-ETI dichotomy[J]. Plant Cell, 2011, 23(1):4-15. doi: 10.1105/tpc.110.082602 URL
[33]	Wang W, Feng B, Zhou JM, et al. Plant immune signaling:Advancing on two frontiers[J]. J Integr Plant Biol, 2020, 62(1):2-24. doi: 10.1111/jipb.12898 URL
[34]	Tunc-Ozdemir M, Jones AM. Ligand-induced dynamics of heterotrimeric G protein-coupled receptor-like kinase complexes[J]. PLoS One, 2017, 12(2):e0171854.
[35]	Xue J, Gong BQ, Yao X, et al. BAK1-mediated phosphorylation of canonical G protein alpha during flagellin signaling in Arabidopsis[J]. J Integr Plant Biol, 2020, 62(5):690-701. doi: 10.1111/jipb.12824 URL
[36]	Tunc-Ozdemir M, Urano D, Jaiswal DK, et al. Direct modulation of heterotrimeric G protein-coupled signaling by a receptor kinase complex[J]. J Biol Chem, 2016, 291(27):13918-13925. doi: 10.1074/jbc.C116.736702 pmid: 27235398
[37]	Liang X, Ding P, Lian K, et al. Arabidopsis heterotrimeric G proteins regulate immunity by directly coupling to the FLS2 receptor[J]. eLife, 2016, 5:e13568.
[38]	Liang X, Ma M, Zhou Z, et al. Ligand-triggered de-repression of Arabidopsis heterotrimeric G proteins coupled to immune receptor kinases[J]. Cell Res, 2018, 28(5):529-543. doi: 10.1038/s41422-018-0027-5 URL
[39]	Li L, Su BD, Qi XY, et al. JA-induced endocytosis of AtRGS1 is involved in G-protein mediated JA responses[J]. Int J Mol Sci, 2019, 20(15):E3779.
[40]	Colaneri AC, Tunc-Ozdemir M, Huang JP, et al. Growth attenuation under saline stress is mediated by the heterotrimeric G protein complex[J]. BMC Plant Biol, 2014, 14:129. doi: 10.1186/1471-2229-14-129 URL
[41]	Chen Y, Ji F, Xie H, et al. Overexpression of the regulator of G-protein signalling protein enhances ABA-mediated inhibition of root elongation and drought tolerance in Arabidopsis[J]. J Exp Bot, 2006, 57(9):2101-2110. pmid: 16714312
[42]	Chen Y, Ji F, Xie H, et al. The regulator of G-protein signaling proteins involved in sugar and abscisic acid signaling in Arabidopsis seed germination[J]. Plant Physiol, 2006, 140(1):302-310. pmid: 16361523
[43]	Choudhury SR, Pandey S. Phosphorylation-dependent regulation of G-protein cycle during nodule formation in soybean[J]. Plant Cell, 2015, 27(11):3260-3276. doi: 10.1105/tpc.15.00517 URL