Role of the plant heterotrimeric G-proteins in the signal pathways regulation

Abstract

Animal and fungal heterotrimeric G-proteins are among the well-known regulators of signaling pathways. Plant studies have shown that G-proteins may also be involved in the regulation of many processes. G-proteins are involved in hormonal regulation, control of cell proliferation, response to abiotic factors, control of biotic interactions and many others. It turned out that with a smaller variety of subunits, G-proteins of plants can have a greater variety of mechanisms for activating and transmitting signals. However, for most processes in plants the mechanisms of operation of heterotrimeric G-proteins remain poorly understood. This review is devoted to the analysis of modern ideas about the structure and functioning of heterotrimeric plant G proteins.

Keywords

heterotrimeric GTP-Binding proteins / plants / receptors / signal transduction

References

[1] Urano D, Jones AM. Heterotrimeric G protein-coupled signaling in plants. Annu Rev Plant Biol. 2014;65:365-384. https://doi.org/10.1146/annurev-arplant-050213-040133.

[2] Scherer GF. Stimulation of growth and phospholipase A, by the peptides mastoparan and melittin and by the auxin 2, 4-dichlorophenoxyacetic acid. Plant Growth Regulation. 1992;11(2):153-157. https://doi.org/10.1007/bf00024069.

[3] White I, Wise A, Millner P. Evidence for G-protein-linked receptors in higher plants: stimulation of GTP-gamma-S binding to membrane fractions by the mastoparan analogue mas 7. Planta. 1993;191(2):285-288. https://doi.org/10.1007/bf00199762.

[4] Legendre L, Yueh YG, Crain R, et al. Phospholipase C activation during elicitation of the oxidative burst in cultured plant cells. J Biol Chem. 1993;268(33):24559-24563.

[5] Aharon GS, Gelli A, Snedden WA, Blumwald E. Activation of a plant plasma membrane Ca2+ channel by TGα1, a heterotrimeric G protein α-subunit homologue. FEBS Lett. 1998;424(1-2):17-21. https://doi.org/10.1016/s0014-5793(98)00129-x.

[6] Zaina S, Reggiani R, Bertani A. Preliminary evidence for involvement of GTP-binding protein(s) in auxin signal transduction in rice (Oryza sativa L.) coleoptile. J Plant Physiol. 1990;136(6):653-658. https://doi.org/10.1016/s0176-1617(11)81339-8.

[7] Warpeha KM, Hamm HE, Rasenick MM, Kaufman LS. A blue-light-activated GTP-binding protein in the plasma membranes of etiolated peas. Proc Natl Acad Sci USA. 1991;88(20):8925-9. https://doi.org/10.1073/pnas.88.20.8925.

[8] Warpeha KM, Kaufman LS, Briggs WR. A flavoprotein may mediate the blue light-activated binding of guanosine 5’-triphosphate to isolated plasma membranes of Pisum sativum L. Photochem Photobiol. 1992;55(4):595-603. https://doi.org/10.1111/j.1751-1097.1992.tb04282.x.

[9] Romero LC, Sommer D, Gotor C, Song PS. G-proteins in etiolated Avena seedlings. Possible phytochrome regulation. FEBS Lett. 1991;282(2):341-346. https://doi.org/10.1016/0014-5793(91)80509-2.

[10] Perfus-Barbeoch L, Jones AM, Assmann SM. Plant heterotrimeric G protein function: Insights from Arabidopsis and rice mutants. Curr Opin Plant Biol. 2004;7(6): 719-31. https://doi.org/10.1016/j.pbi.2004.09.013.

[11] Lease KA, Wen J, Li J, et al. A mutant Arabidopsis heterotrimeric G-protein beta subunit affects leaf, flower, and fruit development. Plant Cell. 2001;13(12):2631-41. https://doi.org/10.1105/tpc.010315.

[12] Liang X, Ding P, Lian K, et al. Arabidopsis heterotrimeric G proteins regulate immunity by directly coupling to the FLS2 receptor. Elife. 2016;5:e13568. https://doi.org/10.7554/eLife.13568.

[13] Ishikawa A. The Arabidopsis G-protein beta-subunit is required for defense response against Agrobacterium tumefaciens. Biosci Biotechnol Biochem. 2009;73(1):47-52. https://doi.org/10.1271/bbb.80449.

[14] Maruta N, Trusov Y, Brenya E, et al. Membrane-localized extra-large G proteins and Gβγ of the heterotrimeric G proteins form functional complexes engaged in plant immunity in Arabidopsis. Plant Physiol. 2015;167(3):1004-1016. https://doi.org/10.1104/pp.114.255703.

[15] Pingret J-L. Rhizobium nod factor signaling: evidence for a G protein mediated transduction mechanism. Plant Cell. 1998;10(5):659-672. https://doi.org/10.1105/tpc.10.5.659.

[16] Rogato A, Valkov VT, Alves LM, et al. Down-regulated Lotus japonicus GCR1 plants exhibit nodulation signalling pathways alteration. Plant Sci. 2016;247:71-82. https://doi.org/10.1016/j.plantsci.2016.03.007.

[17] Choudhury SR, Pandey S. Phosphorylation-dependent regulation of G-protein cycle during nodule formation in soybean. Plant Cell. 2015;27(11):3260-3276. https://doi.org/10.1105/tpc.15.00517.

[18] Hebe G, Hager A, Salzer P. Initial signalling processes induced by elicitors of ectomycorrhiza-forming fungi in spruce cells can also be triggered by G-protein-activating mastoparan and protein phosphatase-inhibiting cantharidin. Planta. 1999;207(3):418-425. https://doi.org/10.1007/s004250050500.

[19] Aranda-Sicilia MN, Trusov Y, Maruta N, et al. Heterotrimeric G proteins interact with defense-related receptor-like kinases in Arabidopsis. J Plant Physiol. 2015;188: 44-48. https://doi.org/10.1016/j.jplph.2015.09.005.

[20] Neer EJ. G proteins: critical control points for transmembrane signals. Protein Sci. 2008;3(1):3-14. https://doi.org/10.1002/pro.5560030102.

[21] Iismaa TP, Biden TJ, Shine J. G protein-coupled receptors. Berlin, Heidelberg: Springer Berlin Heidelberg; 1995. P. 135-136.

[22] Oldham WM, Hamm HE. Heterotrimeric G protein activation by G-protein-coupled receptors. Nat Rev Mol Cell Biol. 2008;9(1):60-71. https://doi.org/10.1038/nrm2299.

[23] Siderovski DP, Willard FS. The GAPs, GEFs, and GDIs of heterotrimeric G-protein alpha subunits. Int J Biol Sci. 2005;1(2):51-66. https://doi.org/10.7150/ijbs.1.51.

[24] Stateczny D, Oppenheimer J, Bommert P. G-protein signaling in plants: minus times minus equals plus. Curr Opin Plant Biol. 2016;34:127-135. https://doi.org/ 10.1016/j.pbi.2016.11.001.

[25] Brown NA, Schrevens S, van Dijck P, Goldman GH. Fungal G-protein-coupled receptors: Mediators of pathogenesis and targets for disease control. Nat Microbiol. 2018;3(4):402-414. https://doi.org/10.1038/s41564-018-0127-5.

[26] Li L, Wright SJ, Krystofova S, et al. Heterotrimeric G protein signaling in filamentous fungi. Annu Rev Microbiol. 2007;61:423-452. https://doi.org/10.1146/annurev.micro.61.080706.093432.

[27] Hoffman CS. Except in every detail: comparing and contrasting G-protein signaling in Saccharomyces cerevisiae and Schizosaccharomyces pombe. Eukaryot Cell. 2005;4(3):495-503. https://doi.org/10.1128/EC.4.3.495-503.2005.

[28] Moretti M, Wang L, Grognet P, et al. Three regulators of G protein signaling differentially affect mating, morphology and virulence in the smut fungus Ustilago maydis. Mol Microbiol. 2017;105(6):901-921. https://doi.org/ 10.1111/mmi.13745.

[29] Xue C, Hsueh Y-P, Heitman J. Magnificent seven: roles of G protein-coupled receptors in extracellular sensing in fungi. FEMS Microbiol Rev. 2008;32(6):1010-1032. https://doi.org/10.1111/j.1574-6976.2008.00131.x.

[30] Krishnan A, Almén MS, Fredriksson R, Schiöth HB. The origin of GPCRs: identification of mammalian like Rhodopsin, Adhesion, Glutamate and Frizzled GPCRs in fungi. PLoS One. 2012;7(1):e29817. https://doi.org/10.1371/journal.pone.0029817.

[31] Lafon A, Han K, Seo J, et al. G-protein and cAMP-mediated signaling in aspergilli: a genomic perspective. Fungal Genet Biol. 2006;43(7):490-502. https://doi.org/10.1016/j.fgb.2006.02.001.

[32] Chen J-G, Willard FS, Huang J, et al. A seven-transmembrane RGS protein that modulates plant cell proliferation. Science. 2003;301(5640):1728-1731. https://doi.org/10.1126/science.1087790.

[33] Trusov Y, Botella JR. Plant G-proteins come of age: breaking the bond with animal models. Front Chem. 2016;4:24. https://doi.org/10.3389/fchem.2016.00024.

[34] Urano D, Jones JC, Wang H, et al. G protein activation without a GEF in the plant kingdom. PLoS Genet. 2012;8(6):e1002756. https://doi.org/10.1371/journal.pgen.1002756.

[35] Johnston CA, Taylor JP, Gao Y, et al. GTPase acceleration as the rate-limiting step in Arabidopsis G protein-coupled sugar signaling. Proc Natl Acad Sci USA. 2007;104(44):17317-17322. https://doi.org/10.1073/pnas.0704751104.

[36] Urano D, Phan N, Jones JC, et al. Endocytosis of the seven-transmembrane RGS1 protein activates G-protein-coupled signalling in Arabidopsis. Nat Cell Biol. 2012;14(10):1079-1088. https://doi.org/10.1038/ncb2568.

[37] Hackenberg D, McKain MR, Lee SG, et al. Gα and regulator of G-protein signaling (RGS) protein pairs maintain functional compatibility and conserved interaction interfaces throughout evolution despite frequent loss of RGS proteins in plants. New Phytol. 2017;216(2):562-75. https://doi.org/10.1111/nph.14180.

[38] Ullah H, Chen J, Temple B, et al. The beta-subunit of the Arabidopsis G protein negatively regulates auxin-induced cell division and affects multiple developmental processes. Plant Cell. 2003;15(2):393-409. https://doi.org/10.1105/tpc.006148.

[39] Pfeuffer T, Helmreich EJ. Activation of pigeon erythrocyte membrane adenylate cyclase by guanylnucleotide analogues and separation of a nucleotide binding protein. J Biol Chem. 1975;250(3):867-876.

[40] Sunahara RK. Isoforms of mammalian adenylyl cyclase: multiplicities of signaling. Mol Interv. 2002;2(3):168-184. https://doi.org/10.1124/mi.2.3.168.

[41] McCudden CR, Hains MD, Kimple RJ, et al. G-protein signaling: back to the future. Cell Mol Life Sci. 2005;62(5):551-577. https://doi.org/10.1007/s00018-004-4462-3.

[42] Kadamur G, Ross EM. Mammalian phospholipase C. Annu Rev Physiol. 2013;75(1):127-154. https://doi.org/10.1146/annurev-physiol-030212-183750.

[43] Berridge MJ. The inositol trisphosphate/calcium signaling pathway in health and disease. Physiol Rev. 2016;96(4):1261-1296. https://doi.org/10.1152/physrev.00006.2016.

[44] Dhanasekaran DN, Kashef K, Lee CM, et al. Scaffold proteins of MAP-kinase modules. Oncogene. 2007;26(22):3185-3202. https://doi.org/10.1038/sj.onc.1210411.

[45] Liu R, Wong W, IJzerman AP. Human G protein-coupled receptor studies in Saccharomyces cerevisiae. Biochem Pharmacol. 2016;114:103-115. https://doi.org/10.1016/j.bcp.2016.02.010.

[46] Lomovatskaya LA, Kuzakova OV, Romanenko AS, Goncharova AM. Activities of adenylate cyclase and changes in camp concentration in root cells of pea seedlings infected with Mutualists and Phytopathogens. Russ J Plant Physiol. 2018;65(4):588-597. https://doi.org/10.1134/S1021443718030056.

[47] Chatukuta P, Dikobe TB, Kawadza DT, et al. An arabidopsis clathrin assembly protein with a predicted role in plant defense can function as an adenylate cyclase. Biomolecules. 2018;8(2). pii: E15. https://doi.org/10.3390/biom8020015.

[48] Isner JC, Maathuis FJ. cGMP signalling in plants: from enigma to main stream. Funct Plant Biol. 2018;45(1-2): 93-101. https://doi.org/10.1071/fp16337.

[49] den Hartog M, Musgrave A, Munnik T. Nod factor-induced phosphatidic acid and diacylglycerol pyrophosphate formation: a role for phospholipase C and D in root hair deformation. Plant J. 2001;25(1):55-65. https://doi.org/10.1046/j.1365-313x.2001.00931.x.

[50] Sun J, Liu X, Pan Y. The physical interaction between LdPLCs and Arabidopsis G beta in a yeast two-hybrid system. Front Agric China. 2011;5(1):64-71. https://doi.org/10.1007/s11703-011-1063-9.

[51] Zhao J, Wang X. Arabidopsis phospholipase dalpha 1 interacts with the heterotrimeric G-protein α-subunit through a motif analogous to the DRY motif in G-protein-coupled receptors. J Biol Chem. 2004;279(3):1794-1800. https://doi.org/10.1074/jbc.M309529200.

[52] Zheng L, Krishnamoorthi R, Zolkiewski M, Wang X. Distinct Ca2+ binding properties of novel C2 domains of plant phospholipase dalpha and β. J Biol Chem. 2000;275(26):19700-19706.

[53] Cheng Z, Li JF, Niu Y, et al. Pathogen-secreted proteases activate a novel plant immune pathway. Nature. 2015;521(7551):213-216. https://doi.org/10.1038/nature14243.

[54] Yuan GL, Li HJ, Yang WC. The integration of Gβ and MAPK signaling cascade in zygote development. Sci Rep. 2017;7(1):8732. https://doi.org/10.1038/s41598-017-08230-4.

[55] Nakashima A, Chen L, Thao NP, et al. RACK1 Functions in rice innate immunity by interacting with the Rac1 immune complex. Plant Cell. 2008;20(8):2265-79. https://doi.org/10.1105/tpc.107.054395.

[56] Suharsono U, Fujisawa Y, Kawasaki T, et al. The heterotrimeric G protein alpha subunit acts upstream of the small GTPase Rac in disease resistance of rice. Proc Natl Acad Sci. 2002;99(20):13307-13312. https://doi.org/10.1073/pnas.192244099.

[57] Petry A, Görlach A. Regulation of NADPH oxidases by G protein-coupled receptors. Antioxid Redox Signal. 2019;30(1):74-94. https://doi.org/10.1089/ars.2018.7525.

[58] Wrzaczek M, Brosché M, Kangasjärvi J. ROS signaling loops – production, perception, regulation. Curr Opin Plant Biol. 2013;16(5):575-582. https://doi.org/10.1016/j.pbi.2013.07.002.

[59] Wong HL, Pinontoan R, Hayashi K, et al. Regulation of rice NADPH oxidase by binding of rac GTPase to its N-terminal extension. Plant Cell. 2007;19(12):4022-34. https://doi.org/10.1105/tpc.107.055624.

[60] Sirichandra C, Gu D, Hu HC, et al. Phosphorylation of the Arabidopsis AtrbohF NADPH oxidase by OST1 protein kinase. FEBS Lett. 2009;583(18):2982-2986. https://doi.org/10.1016/j.febslet.2009.08.033.

[61] Suzuki N, Miller G, Morales J, et al. Respiratory burst oxidases: the engines of ROS signaling. Curr Opin Plant Biol. 2011;14(6):691-699. https://doi.org/10.1016/j.pbi.2011.07.014.

[62] Zeevaart JA, Creelman RA. Metabolism and physiology of abscisic acid. Annu Rev Plant Physiol Plant Mol Biol. 1988;39(1):439-473. https://doi.org/10.1146/annurev.pp.39.060188.002255.

[63] Wang XQ, Ullah H, Jones AM, Assmann SM. G protein regulation of ion channels and abscisic acid signaling in Arabidopsis guard cells. Science. 2001;292(5524):2070-2072. https://doi.org/10.1126/science.1059046.

[64] Fan L-M, Zhang W, Chen J-G, et al. Abscisic acid regulation of guard-cell K+ and anion channels in Gβ- and RGS-deficient Arabidopsis lines. Proc Natl Acad Sci. 2008;105(24):8476-8481. https://doi.org/10.1073/pnas.0800980105.

[65] Mori IC, Murata Y, Yang Y, et al. CDPKs CPK6 and CPK3 function in ABA regulation of guard cell S-type anion- and Ca2+-permeable channels and stomatal closure. PLoS Biol. 2006;4(10):e327. https://doi.org/10.1371/journal.pbio.0040327.

[66] Lee SC, Lan W, Buchanan BB, Luan S. A protein kinase-phosphatase pair interacts with an ion channel to regulate ABA signaling in plant guard cells. Proc Natl Acad Sci. 2009;106(50):21419-21424. https://doi.org/10.1073/pnas.0910601106.

[67] Geiger D, Scherzer S, Mumm P, et al. Activity of guard cell anion channel SLAC1 is controlled by drought-stress signaling kinase-phosphatase pair. Proc Natl Acad Sci. 2009;106(50):21425-21430. https://doi.org/10.1073/pnas.0912021106.

[68] Geiger D, Scherzer S, Mumm P, et al. Guard cell anion channel SLAC1 is regulated by CDPK protein kinases with distinct Ca2+ affinities. Proc Natl Acad Sci. 2010;107(17):8023-8028. https://doi.org/10.1073/pnas.0912030107.

[69] Vlad F, Rubio S, Rodrigues A, et al. Protein phosphatases 2C regulate the activation of the Snf1-related kinase OST1 by abscisic acid in Arabidopsis. Plant Cell. 2009;21(10):3170-3184. https://doi.org/10.1105/tpc.109.069179.

[70] Tsugama D, Liu H, Liu S, Takano T. Arabidopsis heterotrimeric G protein β subunit interacts with a plasma membrane 2C-type protein phosphatase, PP2C52. Biochim Biophys Acta. 2012;1823(12):2254-60. https://doi.org/10.1016/j.bbamcr.2012.10.001.

[71] Hauser F, Li Z, Waadt R, Schroeder JI. SnapShot: abscisic acid signaling. Cell. 2017;171(7):1708-1708.e0. https://doi.org/10.1016/j.cell.2017.11.045.

[72] Tunc-Ozdemir M, Jones AM. Ligand-induced dynamics of heterotrimeric G protein-coupled receptor-like kinase complexes. PLoS One. 2017;12(2):e0171854. https://doi.org/10.1371/journal.pone.0171854.

[73] Choudhury SR, Pandey S. Heterotrimeric G-protein complex and its role in regulation of nodule development. Exocytosis Cell Res. 2016;27(2):29-35.

[74] Botella JR. Can heterotrimeric G proteins help to feed the world? Trends Plant Sci. 2012;17(10):563-568. https://doi.org/10.1016/j.tplants.2012.06.002.

[75] Yadav DK, Islam SM, Tuteja N. Rice heterotrimeric G-protein gamma subunits (RGG1 and RGG2) are differentially regulated under abiotic stress. Plant Signal Behav. 2012;7(7):733-40. https://doi.org/10.4161/psb.20356.

[76] Swain DM, Sahoo RK, Srivastava VK, et al. Function of heterotrimeric G-protein γ subunit RGG1 in providing salinity stress tolerance in rice by elevating detoxification of ROS. Planta. 2017;245(2):367-383. https://doi.org/10.1007/s00425-016-2614-3.

[77] Ullah H, Chen J-G, Temple B, et al. The beta-subunit of the Arabidopsis G protein negatively regulates auxin-induced cell division and affects multiple developmental processes. Plant Cell. 2003;15(2):393-409. https://doi.org/10.1105/tpc.006148.

[78] Jones AM. A reevaluation of the role of the heterotrimeric G protein in coupling light responses in Arabidopsis. Plant Physiol. 2003;131(4):1623-1627. https://doi.org/10.1104/pp.102.017624.

[79] Lian H, Xu P, He S, et al. Photoexcited CRYPTOCHROME 1 interacts directly with G protein β subunit AGB1 to regulate the DNA-binding activity of HY5 and photomorphogenesis in Arabidopsis. Mol Plant. 2018;11(10):1248-1263. https://doi.org/10.1016/j.molp.2018.08.004.

[80] Ullah H, Chen JG, Young JC, et al. Modulation of cell proliferation by heterotrimeric G protein in Arabidopsis. Science. 2001;292(5524):2066-2069. https://doi.org/10.1126/science.1059040.

[81] Chen JG, Gao Y, Jones AM. Differential roles of Arabidopsis heterotrimeric G-protein subunits in modulating cell division in roots. Plant Physiol. 2006;141(3):887-897. https://doi.org/10.1104/pp.106.079202.

[82] Betsuyaku S, Takahashi F, Kinoshita A, et al. Mitogen-activated protein kinase regulated by the CLAVATA receptors contributes to shoot apical meristem homeostasis. Plant Cell Physiol. 2011;52(1):14-29. https://doi.org/10.1093/pcp/pcq157.

[83] Laux T, Mayer KF, Berger J, et al. The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development. 1996;122(1):87-96.

[84] Fletcher JC, Brand U, Running MP, et al. Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science. 1999;283(5409):1911-1914. https://doi.org/10.1126/science.283.5409.1911.

[85] Somssich M, Je BI, Simon R, Jackson D. CLAVATA- WUSCHEL signaling in the shoot meristem. Development. 2016;143(18):3238-48. https://doi.org/10.1242/dev.133645.

[86] Kinoshita A, Betsuyaku S, Osakabe Y, et al. RPK2 is an essential receptor-like kinase that transmits the CLV3 signal in Arabidopsis. Development. 2010;137(22):3911-20. https://doi.org/10.1242/dev.048199.

[87] Ishida T, Tabata R, Yamada M, et al. Heterotrimeric G proteins control stem cell proliferation through CLAVATA signaling in Arabidopsis. EMBO Rep. 2016;17(8):1236. https://doi.org/10.15252/embr.201678010.

Funding

Russian Science FoundationРоссийский научный фонд()

RIGHTS & PERMISSIONS

Bovin A.D., Dolgikh E.A.