Emerging insights into heterotrimeric G protein signaling in plants

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Rice Research Institute of Shenyang Agricultural University, Key Laboratory of Northern Japonica Rice Genetics and Breeding, Ministry of Education and Liaoning Province, Key Laboratory of Northeast Rice Biology and Genetics and Breeding, Ministry of Agriculture, Shenyang 110866, China
b.
The State Key Laboratory of Plant Cell and Chromosome Engineering, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China

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Corresponding author: E-mail address: qianliu@genetics.ac.cn (Qian Liu)

摘要

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Abstract: Heterotrimeric guanine nucleotide-binding protein (G protein) signaling is an evolutionarily conserved mechanism in diverse eukaryotic organisms. In plants, the repertoire of the heterotrimeric G protein complex, which is composed of the Gα, Gβ, and Gγ subunits, is much simpler than that in metazoans, and the identity of typical G protein-coupled receptors (GPCRs) together with their ligands still remains unclear. Comparative phenotypic analysis in Arabidopsis and rice plants using gain- and loss-of-function mutants of G protein components revealed that heterotrimeric G protein signaling plays important roles in a wide variety of plant growth and developmental processes. Grain yield is a complex trait determined by quantitative trait loci (QTL) and is influenced by soil nitrogen availability and environmental changes. Recent studies have shown that the manipulation of two non-canonical Gγ subunits, GS3 (GRAIN SIZE 3) and DEP1 (DENSE AND ERECT PANICLE 1), represents new strategies to simultaneously increase grain yield and nitrogen use efficiency in rice. This review discusses the latest advances in our understanding of the heterotrimeric G protein signal transduction pathway and its application in improving yield and stress tolerance in crops.
- G protein signaling /
- Non-canonical Gγ subunits /
- DEP1 /
- GS3 /
- Yield potential

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参考文献(89)

[1]	Ashikari, M., Wu, J., Yano, M. et al. Proc. Natl. Acad. Sci. U. S. A., 96 (1999),pp. 10284-10289
[2]	Berman, D.M., Wilkie, T.M., Gilman, A.G. GAIP and RGS4 are GTPase activating proteins for the Gi subfamily of G protein alpha subunits Cell, 86 (1996),pp. 445-452
[3]	Bisht, N.C., Jez, J.M., Pandey, S. An elaborate heterotrimeric G-protein family from soybean expands the diversity of plant G-protein networks New Phytol., 190 (2011),pp. 35-48
[4]	Bommert, P., Je, B.I., Goldshmidt, A. et al. Nature, 502 (2013),pp. 555-558
[5]	Botella, J.R. Can heterotrimeric G proteins help to feed the world? Trends Plant Sci., 17 (2012),pp. 563-568
[6]	Cabrera-Vera, T.M., Vanhauwe, J., Thomas, T.O. et al. Insights into G protein structure, function, and regulation Endocr. Rev., 24 (2003),pp. 765-781
[7]	Chakraborty, N., Sharma, P., Kanyuka, K. et al. Plant Mol. Biol., 89 (2015),pp. 559-576
[8]	Chakravorty, D., Trusov, Y., Zhang, W. et al. Plant J., 67 (2011),pp. 840-851
[9]	Chakravorty, D., Gookin, T.E., Milner, M. et al. Plant Physiol., 169 (2015),pp. 512-529
[10]	Chen, J.G., Willard, F.S., Huang, J. et al. A seven-transmembrane RGS protein that modulates plant cell proliferation Science, 301 (2003),pp. 1728-1731
[11]	Chen, J.G., Pandey, S., Huang, J. et al. Plant Physiol., 135 (2004),pp. 907-915
[12]	Chen, Z., Noir, S., Kwaaitaal, M. et al. Plant Cell, 21 (2009),pp. 1972-1991
[13]	Choi, K.Y., Satterberg, B., Lyons, D.M. et al. Cell, 78 (1994),pp. 499-512
[14]	Cheng, Z., Li, J.F., Niu, Y. et al. Pathogen-secreted proteases activate a novel plant immune pathway Nature, 521 (2015),pp. 213-216
[15]	Choudhury, S.R., Bisht, N.C., Thompson, R. et al. Conventional and novel Gγ protein families constitute the heterotrimeric G-protein signaling network in soybean PLoS One, 6 (2011),p. e23361
[16]	Choudhury, S.R., Pandey, S. Specific subunits of heterotrimeric G proteins play important roles during nodulation in soybean Plant Physiol., 162 (2013),pp. 522-533
[17]	Choudhury, S.R., Pandey, S. Phosphorylation-dependent regulation of G-protein cycle during nodule formation in soybean Plant Cell, 27 (2015),pp. 3260-3276
[18]	Choudhury, S.R., Pandey, S. Plant J. (2016),pp. 50-61
[19]	Colaneri, A.C., Jones, A.M. The wiring diagram for plant G signaling Curr. Opin. Plant Biol., 22 (2014),pp. 56-64
[20]	Ding, L., Pandey, S., Assmann, S.M. Plant J., 53 (2008),pp. 248-263
[21]	Fan, C., Xing, Y., Mao, H. et al. Theor. Appl. Genet., 112 (2006),pp. 1164-1171
[22]	Fan, C., Yu, S., Wang, C. et al. Theor. Appl. Genet., 118 (2009),pp. 465-472
[23]	Fu, Y., Lim, S., Urano, D. et al. Reciprocal encoding of signal intensity and duration in a glucose-sensing circuit Cell, 156 (2014),pp. 1084-1095
[24]	Fujisawa, Y., Kato, T., Ohki, S. et al. Suppression of the heterotrimeric G protein causes abnormal morphology, including dwarfism, in rice Proc. Natl. Acad. Sci. U. S. A., 96 (1999),pp. 7575-7580
[25]	Gilman, A.G. G proteins: transducers of receptor-generated signals Annu. Rev. Biochem., 56 (1987),pp. 615-649
[26]	Heo, J.B., Sung, S., Assmann, S.M. J. Biol. Chem., 287 (2012),pp. 8242-8253
[27]	Hu, X., Qian, Q., Xu, T. et al. The U-Box E3 ubiquitin ligase TUD1 functions with a heterotrimeric G a subunit to regulate brassinosteroid-mediated growth in rice PLoS Genet., 9 (2013),p. e1003391
[28]	Huang, J., Philip Taylor, J., Chen, J.G. et al. Plant Cell, 18 (2006),pp. 1226-1238
[29]	Huang, X., Qian, Q., Liu, Z. et al. Nat. Genet., 41 (2009),pp. 494-497
[30]	Ishida, T., Tabata, R., Yamada, M. et al. EMBO Rep., 15 (2014),pp. 1202-1209
[31]	Ishikawa, A., Iwasaki, Y., Asahi, T. Molecular cloning and characterization of a cDNA for the β subunit of a G protein from rice Plant Cell Physiol., 37 (1996),pp. 223-228
[32]	Ishikawa, A., Tsubouchi, H., Iwasaki, Y. et al. Molecular cloning and characterization of a cDNA for the α subunit of a G protein from rice Plant Cell Physiol., 36 (1995),pp. 353-359
[33]	Jaffé, F.W., Freschet, G.E.C., Valdes, B.M. et al. Plant Cell, 24 (2012),pp. 3649-3668
[34]	Johnston, C.A., Taylor, J.P., Gao, Y. et al. Proc. Natl. Acad. Sci. U. S. A., 104 (2007),pp. 17317-17322
[35]	Jones, A.M., Assmann, S.M. Plants: the latest model system for G-protein research EMBO Rep., 5 (2004),pp. 572-578
[36]	Joo, J.H., Wang, S., Chen, J. et al. Plant Cell, 17 (2005),pp. 957-970
[37]	Kato, C., Mizutani, T., Tamaki, H. et al. Characterization of heterotrimeric G protein complexes in rice plasma membrane Plant J., 38 (2004),pp. 320-331
[38]	Lee, Y.-R.J., Assmann, S.M. Plant Mol. Biol., 40 (1999),pp. 55-64
[39]	Li, S., Liu, Y., Zheng, L. et al. New Phytol., 194 (2012),pp. 690-703
[40]	Liang, X., Ding, P., Lian, K. et al. Elife, 5 (2016),p. e13568
[41]	Liu, J., Ding, P., Sun, T. et al. Heterotrimeric G proteins serve as a converging point in plant defense signaling activated by multiple receptor-like kinases Plant Physiol., 161 (2013),pp. 2146-2158
[42]	Ma, H., Yanofsky, M.F., Meyerowitz, E.M. Proc. Natl. Acad. Sci. U. S. A., 87 (1990),pp. 3821-3825
[43]	Ma, Y., Dai, X., Xu, Y. et al. Cell, 160 (2015),pp. 1209-1221
[44]	Mao, H., Sun, S., Yao, J. et al. Linking differential domain functions of the GS3 protein to natural variation of grain size in rice Proc. Natl. Acad. Sci. U. S. A., 107 (2010),pp. 19579-19584
[45]	Maruta, N., Trusov, Y., Brenya, E. et al. Plant Physiol., 167 (2015),pp. 1004-1016
[46]	Mason, M.G., Botella, J.R. Proc. Natl. Acad. Sci. U. S. A., 97 (2000),pp. 14784-14788
[47]	Mason, M.G., Botella, J.R. Biochim. Biophys. Acta, 1520 (2001),pp. 147-153
[48]	Meng, X., Shan, L., He, P. Stack heterotrimeric G proteins and MAPK cascades on a RACK Mol. Plant, 8 (2015),pp. 1691-1693
[49]	Okamoto, H., Matsui, M., Deng, X.W. Plant Cell, 13 (2001),pp. 1639-1652
[50]	Pandey, S., Assmann, S.M. Plant Cell, 16 (2004),pp. 1616-1632
[51]	Pandey, S., Nelson, D.C., Assmann, S.M. Cell, 136 (2009),pp. 136-148
[52]	Perfus-Barbeoch, L., Jones, A.M., Assmann, S.M. Curr. Opin. Plant Biol., 7 (2004),pp. 719-731
[53]	Phan, N., Urano, D., Srba, M. et al. Sugar-induced endocytosis of plant 7TM-RGS proteins Plant Sign. Behav., 8 (2013),p. e22814
[54]	Rasmussen, S.G.F., DeVree, B.T., Zou, Y. et al. Crystal structure of the β2 adrenergic receptor-Gs protein complex Nature, 477 (2011),pp. 549-555
[55]	Ross, E.M., Wilkie, T.M. GTPase-activating proteins for heterotrimeric G proteins: regulators of G protein signaling (RGS) and RGS-like proteins Annu. Rev. Biochem., 69 (2000),pp. 795-827
[56]	Shi, Y., Yang, S. COLD1: a cold sensor in rice Sci. China Life Sci., 58 (2015),pp. 409-410
[57]	Sondek, J., Siderovski, D.P. Ggamma-like (GGL) domains: new frontiers in G-protein signaling and beta-propeller scaffolding Biochem. Harmacol., 61 (2001),pp. 1329-1337
[58]	Su, J., Xu, J., Zhang, S. RACK1, scaffolding a heterotrimeric G protein and a MAPK cascade Trends Plant Sci., 20 (2015),pp. 405-407
[59]	Subramaniam, G., Trusov, Y., Lopez-Encina, C. et al. Type B heterotrimeric G protein γ-subunit regulates auxin and ABA signaling in tomato Plant Physiol., 170 (2016),pp. 1117-1134
[60]	Sun, H., Qian, Q., Wu, K. et al. Heterotrimeric G proteins regulate nitrogen-use efficiency in rice Nat. Genet., 46 (2014),pp. 652-656
[61]	Taddese, B., Upton, G.J., Bailey, G.R. et al. Do plants contain g protein-coupled receptors? Plant Physiol., 164 (2014),pp. 287-307
[62]	Taguchi-Shiobara, F., Kawagoe, Y., Kato, H. et al. Breed. Sci., 61 (2011),pp. 17-25
[63]	Takano-Kai, N., Jiang, H., Kubo, T. et al. Genetics, 182 (2009),pp. 1323-1334
[64]	Trusov, Y., Chakravorty, D., Botella, J.R. Diversity of heterotrimeric G-protein γ subunits in plants BMC Res. Notes, 5 (2012),p. 608
[65]	Ullah, H., Chen, J.G., Young, J.C. et al. Science, 292 (2001),pp. 2066-2069
[66]	Urano, D., Jones, J.C., Wang, H. et al. G protein activation without a GEF in the plant kingdom PLoS Genet., 8 (2012),p. e1002756
[67]	Urano, D., Phan, N., Jones, J.C. et al. Nat. Cell Biol., 14 (2012),pp. 1079-1088
[68]	Urano, D., Chen, J.-G., Botella, J.R. et al. Heterotrimeric G protein signalling in the plant kingdom Open Biol., 3 (2013),p. 120186
[69]	Urano, D., Jones, A.M. “Round up the usual suspects”: a comment on nonexistent plant G protein-coupled receptors Plant Physiol., 161 (2013),pp. 1097-1102
[70]	Urano, D., Colaneri, A., Jones, A.M. Gα modulates salt-induced cellular senescence and cell division in rice and maize J. Exp. Bot., 65 (2014),pp. 6553-6561
[71]	Urano, D., Jones, A.M. Heterotrimeric G protein-coupled signaling in plants Annu. Rev. Plant Biol., 65 (2014),pp. 365-384
[72]	Urano, D., Jackson, D., Jones, A.M. A G protein alpha null mutation confers prolificacy potential in maize J. Exp. Bot., 66 (2015),pp. 4511-4515
[73]	Urano, D., Miura, K., Wu, Q. et al. Plant morphology of heterotrimeric G protein mutants Plant Cell Physiol., 57 (2016),pp. 437-445
[74]	Wang, C., Chen, S., Yu, S. Theor. Appl. Genet., 122 (2011),pp. 905-913
[75]	Wang, J., Nakazaki, T., Chen, S. et al. Theor. Appl. Genet., 119 (2009),pp. 85-91
[76]	Wang, X. Phospholipase D in hormonal and stress signaling Curr. Opin. Plant Biol., 5 (2002),pp. 408-414
[77]	Warpeha, K.M., Lateef, S.S., Lapik, Y. et al. Plant Physiol., 140 (2006),pp. 844-855
[78]	Warpeha, K.M., Upadhyay, S., Yeh, J. et al. Plant Physiol., 143 (2007),pp. 1590-1600
[79]	Weiss, C.A., Garnaat, C.W., Mukai, K. et al. Proc. Natl. Acad. Sci. U. S. A., 91 (1994),pp. 9554-9558
[80]	Wettschureck, N., Offermanns, S. Mammalian G proteins and their cell type specific functions Physiol. Rev., 85 (2005),pp. 1159-1204
[81]	Wolfenstetter, S., Chakravorty, D., Kula, R. et al. Plant J., 81 (2015),pp. 388-398
[82]	Yamada, M., Sawa, S. The roles of peptide hormones during plant root development Curr. Opin. Plant. Biol., 16 (2013),pp. 56-61
[83]	Yu, T.Y., Shi, D.Q., Jia, P.F. et al. PLoS Genet., 12 (2016),p. e1005933
[84]	Yu, Y., Assmann, S.M. Plant Signal. Behav., 11 (2016),p. e1085275
[85]	Zhang, H., Gao, Z., Zheng, X. et al. The role of G-proteins in plant immunity Plant Signal. Behav., 7 (2012),pp. 1284-1288
[86]	Zhao, J., Wang, X. J. Biol. Chem., 279 (2004),pp. 1794-1800
[87]	Zheng, H., Kunst, L., Hawes, C. et al. A GFP-based assay reveals a role for RHD3 in transport between the endoplasmic reticulum and Golgi apparatus Plant J., 37 (2004),pp. 398-414
[88]	Zhou, Y., Zhu, J., Li, Z. et al. Genetics, 183 (2009),pp. 315-324
[89]	Zhu, H., Li, G.-J., Ding, L. et al. Mol. Plant, 2 (2009),pp. 513-525