Abstract
Main conclusion
Heterotrimeric G protein and interacting effectors are relevant for agronomic significance. We can manipulate G protein and effectors, individually or in combination, to develop plant ideotypes by intelligent design breeding.
Heterotrimeric guanine nucleotide-binding protein (G protein) is involved in a wide range of biological events, many of which with agronomic significance. In this review, we summarize recent advances of plant G protein research. We first retrieve maize G protein core subunits Gα, Gβ, and Gγ based on information of Arabidopsis and rice G proteins using integrated BLAST and domain confirmation. Then, we briefly introduce the distribution and function of G protein. We also describe the interaction between G protein and CLAVATA receptor, brassinosteroid signaling kinase complex, and MADS-domain transcription factor. Finally, we discuss the application of G protein knowledge in intelligent plant breeding with focus on the improvement of agronomically important traits.
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References
Bisht NC, Jez JM, Pandey S (2011) An elaborate heterotrimeric G-protein family from soybean expands the diversity of plant G-protein networks. New Phytol 190:35–48
Bommert P, Je BI, Goldshmidt A, Jackson D (2013) The maize Gα gene COMPACT PLANT2 functions in CLAVATA signalling to control shoot meristem size. Nature 502:555–558
Botella JR (2012) Can heterotrimeric G proteins help to feed the world? Trends Plant Sci 17:563–568
Brear AG, Yoon J, Wojtyniak M, Sengupta P (2014) Diverse cell type-specific mechanisms localize G protein-coupled receptors to Caenorhabditis elegans sensory cilia. Genetics 197:667–684
Chakravorty D, Trusov Y, Zhang W, Acharya BR, Sheahan MB, McCurdy DW, Assmann SM, Botella JR (2011) An atypical heterotrimeric G-protein γ-subunit is involved in guard cell K+-channel regulation and morphological development in Arabidopsis thaliana. Plant J 67:840–851
Chakravorty D, Gookin TE, Milner MJ, Yu Y, Assmann SM (2015) Extra-large G proteins expand the repertoire of subunits in Arabidopsis heterotrimeric G protein signaling. Plant Physiol 169:512–529
Chen Y, Ji F, Xie H, Liang J, Zhang J (2006) The regulator of G-protein signaling proteins involved in sugar and abscisic acid signaling in Arabidopsis seed germination. Plant Physiol 140:302–310
Cheng Z, Li JF, Niu Y, Zhang XC, Woody OZ, Xiong Y, Djonović S, Millet Y, Bush J, McConkey BJ, Sheen J, Ausubel FM (2015) Pathogen-secreted proteases activate a novel plant immune pathway. Nature 521:213–216
Fan C, Xing Y, Mao H, Lu T, Han B, Xu C, Li X, Zhang Q (2006) GS3, a major QTL for grain length and weight and minor QTL for grain width and thickness in rice, encodes a putative transmembrane protein. Theor Appl Genet 112:1164–1171
Ferrero-Serrano Á, Assmann SM (2016) The α-subunit of the rice heterotrimeric G protein, RGA1, regulates drought tolerance during the vegetative phase in the dwarf rice mutant d1. J Exp Bot 67:3433–3443
Huang X, Qian Q, Liu Z, Sun H, He S, Luo D, Xia G, Chu C, Li J, Fu X (2009) Natural variation at the DEP1 locus enhances grain yield in rice. Nat Genet 41:494–497
Ishida T, Tabata R, Yamada M, Aida M, Mitsumasu K, Fujiwara M, Yamaguchi K, Shigenobu S, Higuchi M, Tsuji H, Shimamoto K, Hasebe M, Fukuda H, Sawa S (2014) Heterotrimeric G proteins control stem cell proliferation through CLAVATA signaling in Arabidopsis. EMBO Rep 15:1202–1209
Je BI, Xu F, Wu Q, Liu L, Meeley R, Gallagher JP, Corcilius L, Payne RJ, Bartlett ME, Jackson D (2018) The CLAVATA receptor FASCIATED EAR2 responds to distinct CLE peptides by signaling through two downstream effectors. Elife 7:e35673
Johnston CA, Taylor JP, Gao Y, Kimple AJ, Grigston JC, Chen JG, Siderovski DP, Jones AM, Willard FS (2007) GTPase acceleration as the rate-limiting step in Arabidopsis G protein-coupled sugar signaling. Proc Natl Acad Sci USA 104:17317–17322
Kim TW, Wang ZY (2010) Brassinosteroid signal transduction from receptor kinases to transcription factors. Annu Rev Plant Biol 61:681–704
Kunihiro S, Saito T, Matsuda T, Inoue M, Kuramata M, Taguchi-Shiobara F, Youssefian S, Berberich T, Kusano T (2013) Rice DEP1, encoding a highly cysteine-rich G protein γ subunit, confers cadmium tolerance on yeast cells and plants. J Exp Bot 64:4517–4527
Lease KA, Wen J, Li J, Doke JT, Liscum E, Walker JC (2001) A mutant Arabidopsis heterotrimeric G-protein β subunit affects leaf, flower, and fruit development. Plant Cell 13:2631–2641
Li Q, Yang X, Bai G, Warburton ML, Mahuku G, Gore M, Dai J, Li J, Yan J (2010) Cloning and characterization of a putative GS3 ortholog involved in maize kernel development. Theor Appl Genet 120:753–763
Li S, Liu W, Zhang X, Liu Y, Li N, Li Y (2012) Roles of the Arabidopsis G protein γ subunit AGG3 and its rice homologs GS3 and DEP1 in seed and organ size control. Plant Signal Behav 7:1357–1359
Liu J, Ding P, Sun T, Nitta Y, Dong O, Huang X, Yang W, Li X, Botella JR, Zhang Y (2013) Heterotrimeric G proteins serve as a converging point in plant defense signaling activated by multiple receptor-like kinases. Plant Physiol 161:2146–2158
Liu Q, Han R, Wu K, Zhang J, Ye Y, Wang S, Chen J, Pan Y, Li Q, Xu X, Zhou J, Tao D, Wu Y, Fu X (2018) G-protein βγ subunits determine grain size through interaction with MADS-domain transcription factors in rice. Nat Commun 9:852
Ma Y, Dai X, Xu Y, Luo W, Zheng X, Zeng D, Pan Y, Lin X, Liu H, Zhang D, Xiao J, Guo X, Xu S, Niu Y, Jin J, Zhang H, Xu X, Li L, Wang W, Qian Q, Ge S, Chong K (2015) COLD1 confers chilling tolerance in rice. Cell 160:1209–1221
Mao H, Sun S, Yao J, Wang C, Yu S, Xu C, Li X, Zhang Q (2010) Linking differential domain functions of the GS3 protein to natural variation of grain size in rice. Proc Natl Acad Sci USA 107:19579–19584
Maruta N, Trusov Y, Brenya E, Parekh U, Botella JR (2015) Membrane-localized extra-large G proteins and Gβγ of the heterotrimeric G proteins form functional complexes engaged in plant immunity in Arabidopsis. Plant Physiol 167:1004–1016
Papayannopoulou T, Priestley GV, Bonig H (2003) Nakamoto B (2003) The role of G-protein signaling in hematopoietic stem/progenitor cell mobilization. Blood 101:4739–4747
Peng Y, Chen L, Li S, Zhang Y, Xu R, Liu Z, Liu W, Kong J, Huang X, Wang Y, Cheng B, Zheng L, Li Y (2018) BRI1 and BAK1 interact with G proteins and regulate sugar-responsive growth and development in Arabidopsis. Nat Commun 9:1522
Ross EM (2008) Coordinating speed and amplitude in G-protein signaling. Curr Biol 18:R777–R783
Roy Choudhury S, Riesselman AJ, Pandey S (2014) Constitutive or seed-specific overexpression of Arabidopsis G-protein γ subunit 3 (AGG3) results in increased seed and oil production and improved stress tolerance in Camelina sativa. Plant Biotechnol J 12:49–59
Schoof H, Lenhard M, Haecker A, Mayer KF, Jürgens G, Laux T (2000) The stem cell population of Arabidopsis shoot meristems in maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100:635–644
Stewart A, Fisher RA (2015) Introduction: G protein-coupled receptors and RGS proteins. Prog Mol Biol Transl Sci 133:1–11
Sun H, Qian Q, Wu K, Luo J, Wang S, Zhang C, Ma Y, Liu Q, Huang X, Yuan Q, Han R, Zhao M, Dong G, Guo L, Zhu X, Gou Z, Wang W, Wu Y, Lin H, Fu X (2014) Heterotrimeric G proteins regulate nitrogen-use efficiency in rice. Nat Genet 46:652–656
Sun S, Wang L, Mao H, Shao L, Li X, Xiao J, Ouyang Y, Zhang Q (2018) A G-protein pathway determines grain size in rice. Nat Commun 9:851
Swain DM, Sahoo RK, Srivastava VK, Tripathy BC, Tuteja R, Tuteja N (2017) Function of heterotrimeric G-protein γ subunit RGG1 in providing salinity stress tolerance in rice by elevating detoxification of ROS. Planta 245:367–383
Theißen G, Melzer R, Rümpler F (2016) MADS-domain transcription factors and the floral quartet model of flower development: linking plant development and evolution. Development 143:3259–3271
Thung L, Trusov Y, Chakravorty D, Botella JR (2012) Gγ1+Gγ2+Gγ3=Gβ: the search for heterotrimeric G-protein γ subunits in Arabidopsis is over. J Plant Physiol 169:542–545
Trusov Y, Rookes JE, Tilbrook K, Chakravorty D, Mason MG, Anderson D, Chen JG, Jones AM, Botella JR (2007) Heterotrimeric G protein γ subunits provide functional selectivity in Gβγ dimer signaling in Arabidopsis. Plant Cell 19:1235–1250
Ueguchi-Tanaka M, Fujisawa Y, Kobayashi M, Ashikari M, Iwasaki Y, Kitano H, Matsuoka M (2000) Rice dwarf mutant d1, which is defective in the alpha subunit of the heterotrimeric G protein, affects gibberellin signal transduction. Proc Natl Acad Sci USA 97:11638–11643
Ullah H, Chen JG, Young JC, Im KH, Sussman MR, Jones AM (2001) Modulation of cell proliferation by heterotrimeric G protein in Arabidopsis. Science 292:2066–2069
Urano D, Jones JC, Wang H, Matthews M, Bradford W, Bennetzen JL, Jones AM (2012) G protein activation without a GEF in the plant kingdom. PLoS Genet 8:e1002756
Urano D, Colaneri A, Jones AM (2014) Gα modulates salt-induced cellular senescence and cell division in rice and maize. J Exp Bot 65:6553–6561
Utsunomiya Y, Samejima C, Takayanagi Y, Izawa Y, Yoshida T, Sawada Y, Fujisawa Y, Kato H, Iwasaki Y (2011) Suppression of the rice heterotrimeric G protein β-subunit gene, RGB1, causes dwarfism and browning of internodes and lamina joint regions. Plant J 67:907–916
Wang Y, Huang Z, Deng D, Ding H, Zhang R, Wang S, Bian Y, Yin Z, Xu X (2013) Meta-analysis combined with syntenic metaQTL mining dissects candidate loci for maize yield. Mol Breeding 31:601–614
Wang D, Zhao WL, Cai MJ, Wang JX, Zhao XF (2015) G-protein-coupled receptor controls steroid hormone signaling in cell membrane. Sci Rep 5:8675
Wang Y, Xu J, Deng D, Ding H, Bian Y, Yin Z, Wu Y, Zhou B, Zhao Y (2016) A comprehensive meta-analysis of plant morphology, yield, stay-green, and virus disease resistance QTL in maize (Zea mays L.). Planta 243:459–471
Wang Y, Wu Y, Yu B, Yin Z, Xia Y (2017) Extra-large G proteins interact with E3 Ligases PUB4 and PUB2 and function in cytokinin and developmental processes. Plant Physiol 173:1235–1246
Waters EM, Thompson LI, Patel P, Gonzales AD, Ye HZ, Filardo EJ, Clegg DJ, Gorecka J, Akama KT, McEwen BS, Milner TA (2015) G-protein-coupled estrogen receptor 1 is anatomically positioned to modulate synaptic plasticity in the mouse hippocampus. J Neurosci 35:2384–2397
Wu Q, Regan M, Furukawa H, Jackson D (2018) Role of heterotrimeric Gα proteins in maize development and enhancement of agronomic traits. PLoS Genet 14:e1007374
Xu J, Zhang S (2015) Mitogen-activated protein kinase cascades in signalling plant growth and development. Trends Plant Sci 20:56–64
Zhang DP, Zhou Y, Yin JF, Yan XJ, Lin S, Xu WF, Baluška F, Wang YP, Xia YJ, Liang GH, Liang JS (2015) Rice G-protein subunits qPE9-1 and RGB1 play distinct roles in abscisic acid responses and drought adaptation. J Exp Bot 66:6371–6384
Zhu H, Li GJ, Ding L, Cui X, Berg H, Assmann SM, Xia Y (2009) Arabidopsis extra large G-protein 2 (XLG2) interacts with the Gβγ subunit of heterotrimeric G protein and functions in disease resistance. Mol Plant 2:513–525
Acknowledgements
This work was supported by the National Natural Science Foundation of China (31571671), the National Key Research and Development Program of China (2016YFD0101002), the Natural Science Foundation of the Jiangsu Higher Education Institutions of China (18KJA210002), the Qing Lan Project of Yangzhou University (QLYZU201809), and the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD).
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Wang, Y., Wang, Y. & Deng, D. Multifaceted plant G protein: interaction network, agronomic potential, and beyond. Planta 249, 1259–1266 (2019). https://doi.org/10.1007/s00425-019-03112-7
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DOI: https://doi.org/10.1007/s00425-019-03112-7