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Heterotrimeric G-Protein Signaling in Plants

  • Sona PandeyEmail author
Chapter

Abstract

Heterotrimeric GTP-binding proteins comprised of Gα, Gβ, and Gγ subunits are key regulators of a multitude of signaling pathways in all eukaryotes. In plants, these proteins are currently a focus of intense research due to their involvement in affecting many agronomically important traits such as seed yield, organ size, abscisic acid (ABA)-dependent signaling and stress responses, plant defense responses, symbiosis, and nitrogen use efficiency. The mechanistic details of G-protein signaling in modulating these processes remain largely unknown.

The core G-protein components and their activation/deactivation chemistries are broadly conserved all through the eukaryotic evolution; however, their regulatory mechanisms seem to have been rewired in plants to meet specific needs. A set of plant-specific G-protein components also exist that provide a new dimension to this well-characterized signaling pathway. The availability of extensive biochemical data, genetic resources, and sequence information from a variety of plant species has made it possible to compare the G-protein signaling pathways across phyla and between different plant species. Work done in the past two decades has established some of the norms of G-protein signaling in plants and sprung some surprises. This article provides a detailed account of G-protein signaling pathways in plants, their mechanistic details, how they might differ from the classical paradigm, and their importance in manipulating specific responses to generate plants for future needs.

Keywords

G-protein-coupled receptor (GPCR) GTPase activity-accelerating protein (GAP) GTPase Guanine nucleotide exchange factor (GEF) Heterotrimeric G-protein Phospholipase Receptor-like kinase (RLK) Regulator of G-protein signaling (RGS) 

Notes

Acknowledgments

The author sincerely thanks several colleagues for multiple rounds of discussion during the writing of this book chapter. We also apologize to the colleagues whose work could not be cited due to space constraint. Research in the Pandey lab is supported by NIFA/AFRI (2015-67013-22964) and NSF (IOS-1557942 and MCB-1714693) grants to SP.

References

  1. Alvarez S, Hicks LM, Pandey S (2011) ABA-dependent and -independent G-protein signaling in Arabidopsis roots revealed through an iTRAQ proteomics approach. J Proteome Res 10:3107–3122PubMedCrossRefGoogle Scholar
  2. Anantharaman V, Abhiman S, de Souza RF, Aravind L (2011) Comparative genomics uncovers novel structural and functional features of the heterotrimeric GTPase signaling system. Gene 475:63–78PubMedCrossRefGoogle Scholar
  3. Apone F, Alyeshmerni N, Wiens K, Chalmers D, Chrispeels MJ, Colucci G (2003) The G-protein-coupled receptor GCR1 regulates DNA synthesis through activation of phosphatidylinositol-specific phospholipase C. Plant Physiol 133:571–579PubMedPubMedCentralCrossRefGoogle Scholar
  4. Aranda-Sicilia MN, Trusov Y, Maruta N, Chakravorty D, Zhang Y, Botella JR (2015) Heterotrimeric G proteins interact with defense-related receptor-like kinases in Arabidopsis. J Plant Physiol 188:44–48PubMedCrossRefPubMedCentralGoogle Scholar
  5. Assmann SM (2004) Plant G proteins, phytohormones, and plasticity: three questions and a speculation. Sci STKE 2004:re20PubMedGoogle Scholar
  6. 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 190:35–48PubMedCrossRefGoogle Scholar
  7. Bommert P, Je BI, Goldshmidt A, Jackson D (2013) The maize Galpha gene COMPACT PLANT2 functions in CLAVATA signalling to control shoot meristem size. Nature 502:555–558PubMedCrossRefGoogle Scholar
  8. Booker KS, Schwarz J, Garrett MB, Jones AM (2010) Glucose attenuation of auxin-mediated bimodality in lateral root formation is partly coupled by the heterotrimeric G protein complex. PLoS One 5:e12833PubMedPubMedCentralCrossRefGoogle Scholar
  9. Botella JR (2012) Can heterotrimeric G proteins help to feed the world? Trends Plant Sci 17:563–568PubMedCrossRefGoogle Scholar
  10. Botto JF, Ibarra S, Jones AM (2009) The heterotrimeric G-protein complex modulates light sensitivity in Arabidopsis thaliana seed germination. Photochem Photobiol 85:949–954PubMedPubMedCentralCrossRefGoogle Scholar
  11. Broghammer A, Krusell L, Blaise M, Sauer J, Sullivan JT, Maolanon N, Vinther M, Lorentzen A, Madsen EB, Jensen KJ, Roepstorff P, Thirup S, Ronson CW, Thygesen MB, Stougaard J (2012) Legume receptors perceive the rhizobial lipochitin oligosaccharide signal molecules by direct binding. Proc Natl Acad Sci U S A 109:13859–13864PubMedPubMedCentralCrossRefGoogle Scholar
  12. Chakraborty N, Sharma P, Kanyuka K, Pathak RR, Choudhury D, Hooley R, Raghuram N (2015a) G-protein alpha-subunit (GPA1) regulates stress, nitrate and phosphate response, flavonoid biosynthesis, fruit/seed development and substantially shares GCR1 regulation in A. thaliana. Plant Mol Biol 89:559–576PubMedCrossRefPubMedCentralGoogle Scholar
  13. Chakraborty N, Sharma P, Kanyuka K, Pathak RR, Choudhury D, Hooley RA, Raghuram N (2015b) Transcriptome analysis of Arabidopsis GCR1 mutant reveals its roles in stress, hormones, secondary metabolism and phosphate starvation. PLoS One 10:e0117819PubMedPubMedCentralCrossRefGoogle Scholar
  14. Chakravorty D, Trusov Y, Zhang W, Acharya BR, Sheahan MB, McCurdy DW, Assmann SM, Botella JR (2011) An atypical heterotrimeric G-protein gamma-subunit is involved in guard cell K(+)-channel regulation and morphological development in Arabidopsis thaliana. Plant J 67:840–851PubMedCrossRefPubMedCentralGoogle Scholar
  15. 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 169:512–529PubMedPubMedCentralCrossRefGoogle Scholar
  16. Chen JG, Willard FS, Huang J, Liang J, Chasse SA, Jones AM, Siderovski DP (2003) A seven-transmembrane RGS protein that modulates plant cell proliferation. Science 301:1728–1731PubMedCrossRefPubMedCentralGoogle Scholar
  17. Chen JG, Pandey S, Huang J, Alonso JM, Ecker JR, Assmann SM, Jones AM (2004) GCR1 can act independently of heterotrimeric G-protein in response to brassinosteroids and gibberellins in Arabidopsis seed germination. Plant Physiol 135:907–915PubMedPubMedCentralCrossRefGoogle Scholar
  18. Chen JG, Gao Y, Jones AM (2006) Differential roles of Arabidopsis heterotrimeric G-protein subunits in modulating cell division in roots. Plant Physiol 141:887–897PubMedPubMedCentralCrossRefGoogle Scholar
  19. Colaneri AC, Tunc-Ozdemir M, Huang JP, Jones AM (2014) Growth attenuation under saline stress is mediated by the heterotrimeric G protein complex. BMC Plant Biol 14:129PubMedPubMedCentralCrossRefGoogle Scholar
  20. Coursol S, Fan LM, Le Stunff H, Spiegel S, Gilroy S, Assmann SM (2003) Sphingolipid signalling in Arabidopsis guard cells involves heterotrimeric G proteins. Nature 423:651–654PubMedCrossRefGoogle Scholar
  21. Delgado-Cerezo M, Sanchez-Rodriguez C, Escudero V, Miedes E, Fernandez PV, Jorda L, Hernandez-Blanco C, Sanchez-Vallet A, Bednarek P, Schulze-Lefert P, Somerville S, Estevez JM, Persson S, Molina A (2012) Arabidopsis heterotrimeric G-protein regulates cell wall defense and resistance to necrotrophic fungi. Mol Plant 5:98–114PubMedCrossRefPubMedCentralGoogle Scholar
  22. Ding L, Pandey S, Assmann SM (2008) Arabidopsis extra-large G proteins (XLGs) regulate root morphogenesis. Plant J 53:248–263PubMedCrossRefPubMedCentralGoogle Scholar
  23. 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 112:1164–1171PubMedCrossRefPubMedCentralGoogle Scholar
  24. Fan LM, Zhang W, Chen JG, Taylor JP, Jones AM, Assmann SM (2008) Abscisic acid regulation of guard-cell K+ and anion channels in Gbeta- and RGS-deficient Arabidopsis lines. Proc Natl Acad Sci U S A 105:8476–8481PubMedPubMedCentralCrossRefGoogle Scholar
  25. Ferrero-Serrano A, Su Z, Assmann SM (2018) Illuminating the role of the Galpha heterotrimeric G protein subunit, RGA1, in regulating photoprotection and photoavoidance in rice. Plant Cell Environ 41:451–468PubMedCrossRefPubMedCentralGoogle Scholar
  26. Fox AR, Soto GC, Jones AM, Casal JJ, Muschietti JP, Mazzella MA (2012) cry1 and GPA1 signaling genetically interact in hook opening and anthocyanin synthesis in Arabidopsis. Plant Mol Biol 80:315–324PubMedPubMedCentralCrossRefGoogle Scholar
  27. Friedman EJ, Wang HX, Jiang K, Perovic I, Deshpande A, Pochapsky TC, Temple BR, Hicks SN, Harden TK, Jones AM (2011) Acireductone dioxygenase 1 (ARD1) is an effector of the heterotrimeric G protein beta subunit in Arabidopsis. J Biol Chem 286:30107–30118PubMedPubMedCentralCrossRefGoogle Scholar
  28. Fujisawa Y, Kato T, Ohki S, Ishikawa A, Kitano H, Sasaki T, Asahi T, Iwasaki Y (1999) Suppression of the heterotrimeric G protein causes abnormal morphology, including dwarfism, in rice. Proc Natl Acad Sci U S A 96:7575–7580PubMedPubMedCentralCrossRefGoogle Scholar
  29. Gao Y, Wang S, Asami T, Chen JG (2008) Loss-of-function mutations in the Arabidopsis heterotrimeric G-protein alpha subunit enhance the developmental defects of brassinosteroid signaling and biosynthesis mutants. Plant Cell Physiol 49:1013–1024PubMedCrossRefPubMedCentralGoogle Scholar
  30. Ge XM, Cai HL, Lei X, Zhou X, Yue M, He JM (2015) Heterotrimeric G protein mediates ethylene-induced stomatal closure via hydrogen peroxide synthesis in Arabidopsis. Plant J 82:138–150PubMedCrossRefGoogle Scholar
  31. Gilman AG (1987) G proteins: transducers of receptor-generated signals. Annual Review of Biochemistry 56:615–649PubMedCrossRefGoogle Scholar
  32. Gilman AG (1995) Nobel Lecture. G proteins and regulation of adenylyl cyclase. Biosci Rep 15:65–97PubMedCrossRefGoogle Scholar
  33. Gish LA, Clark SE (2011) The RLK/Pelle family of kinases. Plant J 66:117–127PubMedPubMedCentralCrossRefGoogle Scholar
  34. Gookin TE, Bendtsen JD (2013) Topology assessment, G protein-coupled receptor (GPCR) prediction, and in vivo interaction assays to identify plant candidate GPCRs. Methods Mol Biol 1043:1–12PubMedCrossRefGoogle Scholar
  35. Gookin TE, Kim J, Assmann SM (2008) Whole proteome identification of plant candidate G-protein coupled receptors in Arabidopsis, rice, and poplar: computational prediction and in-vivo protein coupling. Genome Biol 9:R120PubMedPubMedCentralCrossRefGoogle Scholar
  36. Hackenberg D, Perroud PF, Quatrano R, Pandey S (2016) Sporophyte formation and life cycle completion in moss requires heterotrimeric G-proteins. Plant Physiol 172:1154–1166PubMedPubMedCentralGoogle Scholar
  37. Hackenberg D, McKain MR, Lee SG, Roy Choudhury S, McCann T, Schreier S, Harkess A, Pires JC, Wong GK, Jez JM, Kellogg EA, Pandey S (2017) Galpha 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 216:562–575PubMedCrossRefGoogle Scholar
  38. Hao LH, Wang WX, Chen C, Wang YF, Liu T, Li X, Shang ZL (2012) Extracellular ATP promotes stomatal opening of Arabidopsis thaliana through heterotrimeric G protein alpha subunit and reactive oxygen species. Mol Plant 5:852–864PubMedCrossRefGoogle Scholar
  39. He JM, Ma XG, Zhang Y, Sun TF, Xu FF, Chen YP, Liu X, Yue M (2013) Role and interrelationship of Galpha protein, hydrogen peroxide, and nitric oxide in ultraviolet B-induced stomatal closure in Arabidopsis leaves. Plant Physiol 161:1570–1583PubMedPubMedCentralCrossRefGoogle Scholar
  40. Heo JB, Sung S, Assmann SM (2012) Ca2+-dependent GTPase, extra-large G protein 2 (XLG2), promotes activation of DNA-binding protein related to vernalization 1 (RTV1), leading to activation of floral integrator genes and early flowering in Arabidopsis. J Biol Chem 287:8242–8253PubMedPubMedCentralCrossRefGoogle Scholar
  41. Hu X, Qian Q, Xu T, Zhang Y, Dong G, Gao T, Xie Q, Xue Y (2013) The U-box E3 ubiquitin ligase TUD1 functions with a heterotrimeric G alpha subunit to regulate Brassinosteroid-mediated growth in rice. PLoS Genet 9:e1003391PubMedPubMedCentralCrossRefGoogle Scholar
  42. Huang J, Taylor JP, Chen JG, Uhrig JF, Schnell DJ, Nakagawa T, Korth KL, Jones AM (2006) The plastid protein THYLAKOID FORMATION1 and the plasma membrane G-protein GPA1 interact in a novel sugar-signaling mechanism in Arabidopsis. Plant Cell 18:1226–1238PubMedPubMedCentralCrossRefGoogle Scholar
  43. 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 41:494–497PubMedCrossRefGoogle Scholar
  44. 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 15:1202–1209PubMedPubMedCentralCrossRefGoogle Scholar
  45. Jones AM, Xuan Y, Xu M, Wang RS, Ho CH, Lalonde S, You CH, Sardi MI, Parsa SA, Smith-Valle E, Su T, Frazer KA, Pilot G, Pratelli R, Grossmann G, Acharya BR, Hu HC, Engineer C, Villiers F, Ju C, Takeda K, Su Z, Dong Q, Assmann SM, Chen J, Kwak JM, Schroeder JI, Albert R, Rhee SY, Frommer WB (2014) Border control – a membrane-linked interactome of Arabidopsis. Science 344:711–716PubMedCrossRefGoogle Scholar
  46. Kansup J, Tsugama D, Liu S, Takano T (2013) The Arabidopsis adaptor protein AP-3mu interacts with the G-protein beta subunit AGB1 and is involved in abscisic acid regulation of germination and post-germination development. J Exp Bot 64:5611–5621PubMedPubMedCentralCrossRefGoogle Scholar
  47. Kansup J, Tsugama D, Liu S, Takano T (2014) Arabidopsis G-protein beta subunit AGB1 interacts with NPH3 and is involved in phototropism. Biochem Biophys Res Commun 445:54–57PubMedCrossRefGoogle Scholar
  48. Kaur J, Roy Choudhury S, Vijayakumar A, Hovis L, Rhodes Z, Polzin R, Blumenthal D, Pandey S (2018) Arabidopsis Type III Ggamma protein AGG3 is a positive regulator of yield and stress responses in the model monocot Setaria viridis. Front Plant Sci 9:109PubMedPubMedCentralCrossRefGoogle Scholar
  49. Klopffleisch K, Phan N, Augustin K, Bayne RS, Booker KS, Botella JR, Carpita NC, Carr T, Chen JG, Cooke TR, Frick-Cheng A, Friedman EJ, Fulk B, Hahn MG, Jiang K, Jorda L, Kruppe L, Liu C, Lorek J, McCann MC, Molina A, Moriyama EN, Mukhtar MS, Mudgil Y, Pattathil S, Schwarz J, Seta S, Tan M, Temp U, Trusov Y, Urano D, Welter B, Yang J, Panstruga R, Uhrig JF, Jones AM (2011) Arabidopsis G-protein interactome reveals connections to cell wall carbohydrates and morphogenesis. Mol Syst Biol 7:532PubMedPubMedCentralCrossRefGoogle Scholar
  50. Lapik YR, Kaufman LS (2003) The Arabidopsis cupin domain protein AtPirin1 interacts with the G protein alpha-subunit GPA1 and regulates seed germination and early seedling development. Plant Cell 15:1578–1590PubMedPubMedCentralCrossRefGoogle Scholar
  51. Lee S, Rojas CM, Ishiga Y, Pandey S, Mysore KS (2013) Arabidopsis heterotrimeric G-proteins play a critical role in host and nonhost resistance against Pseudomonas syringae pathogens. PLoS One 8:e82445PubMedPubMedCentralCrossRefGoogle Scholar
  52. Lee CS, Ahn W, Choi YE (2017) The G-protein alpha-subunit gene CGA1 is involved in regulation of resistance to heat and osmotic stress in Chlamydomonas reinhardtii. Cell Mol Biol (Noisy-le-grand) 63:29–39CrossRefGoogle Scholar
  53. Li S, Liu Y, Zheng L, Chen L, Li N, Corke F, Lu Y, Fu X, Zhu Z, Bevan MW, Li Y (2012a) The plant-specific G protein gamma subunit AGG3 influences organ size and shape in Arabidopsis thaliana. New Phytol 194:690–703PubMedCrossRefGoogle Scholar
  54. Li S, Pandey S, Gookin TE, Zhao Z, Wilson L, Assmann SM (2012b) Gene-sharing networks reveal organizing principles of transcriptomes in Arabidopsis and other multicellular organisms. Plant Cell 24:1362–1378PubMedPubMedCentralCrossRefGoogle Scholar
  55. Liang X, Ding P, Lian K, Wang J, Ma M, Li L, Li L, Li M, Zhang X, Chen S, Zhang Y, Zhou JM (2016) Arabidopsis heterotrimeric G proteins regulate immunity by directly coupling to the FLS2 receptor. Elife 5:e13568PubMedPubMedCentralCrossRefGoogle Scholar
  56. Liang Y, Gao Y, Jones AM (2017) Extra large G-protein interactome reveals multiple stress response function and partner-dependent XLG subcellular localization. Front Plant Sci 8:1015PubMedPubMedCentralCrossRefGoogle Scholar
  57. Liang X, Ma M, Zhou Z, Wang J, Yang X, Rao S, Bi G, Li L, Zhang X, Chai J, Chen S, Zhou JM (2018) Ligand-triggered de-repression of Arabidopsis heterotrimeric G proteins coupled to immune receptor kinases. Cell Res. 28: 529–543PubMedPubMedCentralCrossRefGoogle Scholar
  58. 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 161:2146–2158PubMedPubMedCentralCrossRefGoogle Scholar
  59. Liu C, Xu Y, Long D, Cao B, Hou J, Xiang Z, Zhao A (2017) Plant G-protein beta subunits positively regulate drought tolerance by elevating detoxification of ROS. Biochem Biophys Res Commun 491:897–902PubMedCrossRefGoogle Scholar
  60. Llorente F, Alonso-Blanco C, Sanchez-Rodriguez C, Jorda L, Molina A (2005) ERECTA receptor-like kinase and heterotrimeric G protein from Arabidopsis are required for resistance to the necrotrophic fungus Plectosphaerella cucumerina. Plant J 43:165–180PubMedCrossRefGoogle Scholar
  61. Lorek J, Griebel T, Jones AM, Kuhn H, Panstruga R (2013) The role of Arabidopsis heterotrimeric G-protein subunits in MLO2 function and MAMP-triggered immunity. Mol Plant Microbe Interact 26:991–1003PubMedPubMedCentralCrossRefGoogle Scholar
  62. Ma H, Yanofsky MF, Meyerowitz EM (1990) Molecular cloning and characterization of GPA1, a G protein alpha subunit gene from Arabidopsis thaliana. Proc Natl Acad Sci U S A 87:3821–3825PubMedPubMedCentralCrossRefGoogle Scholar
  63. 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 160:1209–1221CrossRefGoogle Scholar
  64. Maeda K, Houjyou Y, Komatsu T, Hori H, Kodaira T, Ishikawa A (2009) AGB1 and PMR5 contribute to PEN2-mediated preinvasion resistance to Magnaporthe oryzae in Arabidopsis thaliana. Mol Plant Microbe Interact 22:1331–1340PubMedCrossRefGoogle Scholar
  65. Maruta N, Trusov Y, Brenya E, Parekh U, Botella JR (2015) Membrane-localized extra-large G proteins and Gbg of the heterotrimeric G proteins form functional complexes engaged in plant immunity in Arabidopsis. Plant Physiol 167:1004–1016PubMedPubMedCentralCrossRefGoogle Scholar
  66. McCudden CR, Hains MD, Kimple RJ, Siderovski DP, Willard FS (2005) G-protein signaling: back to the future. Cell Mol Life Sci 62:551–577PubMedPubMedCentralCrossRefGoogle Scholar
  67. Mishra G, Zhang W, Deng F, Zhao J, Wang X (2006) A bifurcating pathway directs abscisic acid effects on stomatal closure and opening in Arabidopsis. Science 312:264–266PubMedCrossRefGoogle Scholar
  68. Misra S, Wu Y, Venkataraman G, Sopory SK, Tuteja N (2007) Heterotrimeric G-protein complex and G-protein-coupled receptor from a legume (Pisum sativum): role in salinity and heat stress and cross-talk with phospholipase C. Plant J 51:656–669PubMedCrossRefGoogle Scholar
  69. Mudgil Y, Uhrig JF, Zhou J, Temple B, Jiang K, Jones AM (2009) Arabidopsis N-MYC DOWNREGULATED-LIKE1, a positive regulator of auxin transport in a G protein-mediated pathway. Plant Cell 21:3591–3609PubMedPubMedCentralCrossRefGoogle Scholar
  70. Mudgil Y, Karve A, Teixeira PJ, Jiang K, Tunc-Ozdemir M, Jones AM (2016) Photosynthate regulation of the root system architecture mediated by the heterotrimeric G protein complex in Arabidopsis. Front Plant Sci 7:1255PubMedPubMedCentralCrossRefGoogle Scholar
  71. Nilson SE, Assmann SM (2010a) The alpha-subunit of the Arabidopsis heterotrimeric G protein, GPA1, is a regulator of transpiration efficiency. Plant Physiol 152:2067–2077PubMedPubMedCentralCrossRefGoogle Scholar
  72. Nilson SE, Assmann SM (2010b) Heterotrimeric G proteins regulate reproductive trait plasticity in response to water availability. New Phytol 185:734–746PubMedCrossRefGoogle Scholar
  73. Okamoto H, Gobel C, Capper RG, Saunders N, Feussner I, Knight MR (2009) The alpha-subunit of the heterotrimeric G-protein affects jasmonate responses in Arabidopsis thaliana. J Exp Bot 60:1991–2003PubMedPubMedCentralCrossRefGoogle Scholar
  74. Oki K, Inaba N, Kitagawa K, Fujioka S, Kitano H, Fujisawa Y, Kato H, Iwasaki Y (2009) Function of the alpha subunit of rice heterotrimeric G protein in brassinosteroid signaling. Plant Cell Physiol 50:161–172PubMedCrossRefGoogle Scholar
  75. Oldham WM, Hamm HE (2008) Heterotrimeric G protein activation by G-protein-coupled receptors. Nat Rev Mol Cell Biol 9:60–71PubMedCrossRefGoogle Scholar
  76. Pandey S (2016) Phospholipases as GTPase activity accelerating proteins (GAPs) in plants. Plant Signal Behav 11:e1176821PubMedPubMedCentralCrossRefGoogle Scholar
  77. Pandey S (2017) Heterotrimeric G-protein regulatory circuits in plants: conserved and novel mechanisms. Plant Signal Behav 12:e1325983PubMedPubMedCentralCrossRefGoogle Scholar
  78. Pandey S, Assmann SM (2004) The Arabidopsis putative G protein-coupled receptor GCR1 interacts with the G protein alpha subunit GPA1 and regulates abscisic acid signaling. Plant Cell 16:1616–1632PubMedPubMedCentralCrossRefGoogle Scholar
  79. Pandey S, Vijayakumar A (2018) Emerging themes in heterotrimeric G-protein signaling in plants. Plant Sci 270:292–300PubMedCrossRefGoogle Scholar
  80. Pandey S, Chen JG, Jones AM, Assmann SM (2006) G-protein complex mutants are hypersensitive to abscisic acid regulation of germination and postgermination development. Plant Physiol 141:243–256PubMedPubMedCentralCrossRefGoogle Scholar
  81. Pandey S, Monshausen GB, Ding L, Assmann SM (2008) Regulation of root-wave response by extra large and conventional G proteins in Arabidopsis thaliana. Plant J 55:311–322PubMedCrossRefPubMedCentralGoogle Scholar
  82. Pandey S, Nelson DC, Assmann SM (2009) Two novel GPCR-type G proteins are abscisic acid receptors in Arabidopsis. Cell 136:136–148PubMedCrossRefGoogle Scholar
  83. Pandey S, Wang RS, Wilson L, Li S, Zhao Z, Gookin TE, Assmann SM, Albert R (2010) Boolean modeling of transcriptome data reveals novel modes of heterotrimeric G-protein action. Mol Syst Biol 6:372PubMedPubMedCentralCrossRefGoogle Scholar
  84. Pingret JL, Journet EP, Barker DG (1998) Rhizobium nod factor signaling. Evidence for a G- protein-mediated transduction mechanism. Plant Cell 10:659–672PubMedPubMedCentralGoogle Scholar
  85. Raghuram N, Chandok MR, Sopory SK (1999) Light regulation of nitrate reductase gene expression in maize involves a G-protein. Mol Cell Biol Res Commun 2:86–90PubMedCrossRefGoogle Scholar
  86. Reed RR (1990) G protein diversity and the regulation of signaling pathways. New Biol 2:957–960PubMedGoogle Scholar
  87. Rodbell M (1992) The role of GTP-binding proteins in signal transduction: from the sublimely simple to the conceptually complex. Curr Top Cell Regul 32:1–47PubMedCrossRefGoogle Scholar
  88. Rodbell M (1995) Nobel Lecture. Signal transduction: evolution of an idea. Biosci Rep 15:117–133PubMedCrossRefGoogle Scholar
  89. Ross EM (2011) Galpha(q) and phospholipase C-beta: turn on, turn off, and do it fast. Sci Signal 4:pe5PubMedCrossRefGoogle Scholar
  90. Roy Choudhury S, Pandey S (2013) Specific subunits of heterotrimeric G proteins play important roles during nodulation in soybean. Plant Physiol 162:522–533CrossRefGoogle Scholar
  91. Roy Choudhury S, Pandey S (2015) Phosphorylation-dependent regulation of G-protein cycle during nodule formation in soybean. Plant Cell 27:3260–3276CrossRefGoogle Scholar
  92. Roy Choudhury S, Pandey S (2016a) Interaction of heterotrimeric G-protein components with receptor-like kinases in plants: an alternative to the established signaling paradigm? Mol Plant 9:1093–1095PubMedCrossRefPubMedCentralGoogle Scholar
  93. Roy Choudhury S, Pandey S (2016b) The role of PLDalpha1 in providing specificity to signal-response coupling by heterotrimeric G-protein components in Arabidopsis. Plant J 86:50–61PubMedCrossRefPubMedCentralGoogle Scholar
  94. Roy Choudhury S, Pandey S (2017a) Phosphatidic acid binding inhibits RGS1 activity to affect specific signaling pathways in Arabidopsis. Plant J 90:466–477PubMedCrossRefPubMedCentralGoogle Scholar
  95. Roy Choudhury S, Pandey S (2017b) Recently duplicated plant heterotrimeric Galpha proteins with subtle biochemical differences influence specific outcomes of signal-response coupling. J Biol Chem 292:16188–16198PubMedPubMedCentralCrossRefGoogle Scholar
  96. Roy Choudhury S, Bisht NC, Thompson R, Todorov O, Pandey S (2011) Conventional and novel Ggamma protein families constitute the heterotrimeric G-protein signaling network in soybean. PLoS One 6:e23361CrossRefGoogle Scholar
  97. Roy Choudhury S, Riesselman AJ, Pandey S (2014a) Constitutive or seed-specific overexpression of Arabidopsis G-protein gamma subunit 3 (AGG3) results in increased seed and oil production and improved stress tolerance in Camelina sativa. Plant Biotechnol J 12:49–59PubMedCrossRefPubMedCentralGoogle Scholar
  98. Roy Choudhury S, Wang Y, Pandey S (2014b) Soya bean Galpha proteins with distinct biochemical properties exhibit differential ability to complement Saccharomyces cerevisiae gpa1 mutant. Biochem J 461:75–85PubMedCrossRefPubMedCentralGoogle Scholar
  99. Selinger Z, Cassel D (1981) Role of guanine nucleotides in hormonal activation of adenylate cyclase. Adv Cyclic Nucleotide Res 14:15–22PubMedPubMedCentralGoogle Scholar
  100. Siderovski DP, Willard FS (2005) The GAPs, GEFs, and GDIs of heterotrimeric G-protein alpha subunits. Int J Biol Sci 1:51–66PubMedPubMedCentralCrossRefGoogle Scholar
  101. Spiegel AM, Backlund PS Jr, Butrynski JE, Jones TL, Simonds WF (1991) The G protein connection: molecular basis of membrane association. Trends Biochem Sci 16:338–341PubMedCrossRefGoogle Scholar
  102. Steffens B, Sauter M (2009) Heterotrimeric G protein signaling is required for epidermal cell death in rice. Plant Physiol 151:732–740PubMedPubMedCentralCrossRefGoogle Scholar
  103. Subramaniam G, Trusov Y, Lopez-Encina C, Hayashi S, Batley J, Botella JR (2016) Type B heterotrimeric G Protein gamma-subunit regulates auxin and ABA signaling in tomato. Plant Physiol 170:1117–1134PubMedCrossRefGoogle Scholar
  104. Suharsono U, Fujisawa Y, Kawasaki T, Iwasaki Y, Satoh H, Shimamoto K (2002) The heterotrimeric G protein alpha subunit acts upstream of the small GTPase Rac in disease resistance of rice. Proc Natl Acad Sci U S A 99:13307–13312PubMedPubMedCentralCrossRefGoogle Scholar
  105. 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 46:652–656PubMedCrossRefGoogle Scholar
  106. 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 9:851PubMedPubMedCentralCrossRefGoogle Scholar
  107. Sutherland EW (1971) Nobel prize in physiology or medicine 1971: the action of hormones outlined. Lakartidningen 68(44):4991–4995PubMedGoogle Scholar
  108. Sutherland EW, Rall TW, Menon T (1962) Adenyl cylase. I. Distribution, preparation, and properties. J Biol Chem 237:1220–1227PubMedGoogle Scholar
  109. Swain DM, Sahoo RK, Srivastava VK, Tripathy BC, Tuteja R, Tuteja N (2017) Function of heterotrimeric G-protein gamma subunit RGG1 in providing salinity stress tolerance in rice by elevating detoxification of ROS. Planta 245:367–383PubMedCrossRefGoogle Scholar
  110. Torres MA, Morales J, Sanchez-Rodriguez C, Molina A, Dangl JL (2013) Functional interplay between Arabidopsis NADPH oxidases and heterotrimeric G protein. Mol Plant Microbe Interact 26:686–694PubMedCrossRefGoogle Scholar
  111. Trusov Y, Rookes JE, Chakravorty D, Armour D, Schenk PM, Botella JR (2006) Heterotrimeric G proteins facilitate Arabidopsis resistance to necrotrophic pathogens and are involved in jasmonate signaling. Plant Physiol 140:210–220PubMedPubMedCentralCrossRefGoogle Scholar
  112. Trusov Y, Rookes JE, Tilbrook K, Chakravorty D, Mason MG, Anderson D, Chen JG, Jones AM, Botella JR (2007) Heterotrimeric G protein gamma subunits provide functional selectivity in Gbetagamma dimer signaling in Arabidopsis. Plant Cell 19:1235–1250PubMedPubMedCentralCrossRefGoogle Scholar
  113. Trusov Y, Sewelam N, Rookes JE, Kunkel M, Nowak E, Schenk PM, Botella JR (2009) Heterotrimeric G proteins-mediated resistance to necrotrophic pathogens includes mechanisms independent of salicylic acid-, jasmonic acid/ethylene- and abscisic acid-mediated defense signaling. Plant J 58:69–81PubMedCrossRefGoogle Scholar
  114. Tsugama D, Liu S, Takano T (2013a) Arabidopsis heterotrimeric G protein beta subunit, AGB1, regulates brassinosteroid signalling independently of BZR1. J Exp Bot 64:3213–3223PubMedPubMedCentralCrossRefGoogle Scholar
  115. Tsugama D, Liu S, Takano T (2013b) A bZIP protein, VIP1, interacts with Arabidopsis heterotrimeric G protein beta subunit, AGB1. Plant Physiol Biochem 71:240–246PubMedCrossRefGoogle Scholar
  116. Tunc-Ozdemir M, Urano D, Jaiswal DK, Clouse SD, Jones AM (2016) Direct modulation of heterotrimeric G protein-coupled signaling by a receptor kinase complex. J Biol Chem 291:13918–13925PubMedPubMedCentralCrossRefGoogle Scholar
  117. 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 U S A 97:11638–11643PubMedPubMedCentralCrossRefGoogle Scholar
  118. Ullah H, Chen JG, Young JC, Im KH, Sussman MR, Jones AM (2001) Modulation of cell proliferation by heterotrimeric G protein in Arabidopsis. Science 292:2066–2069PubMedCrossRefGoogle Scholar
  119. Ullah H, Chen JG, Wang S, Jones AM (2002) Role of a heterotrimeric G protein in regulation of Arabidopsis seed germination. Plant Physiol 129:897–907PubMedPubMedCentralCrossRefGoogle Scholar
  120. Ullah H, Chen JG, Temple B, Boyes DC, Alonso JM, Davis KR, Ecker JR, Jones AM (2003) The beta-subunit of the Arabidopsis G protein negatively regulates auxin-induced cell division and affects multiple developmental processes. Plant Cell 15:393–409PubMedPubMedCentralCrossRefGoogle Scholar
  121. Urano D, Jones AM (2014) Heterotrimeric G protein-coupled signaling in plants. Annu Rev Plant Biol 65:365–384PubMedCrossRefPubMedCentralGoogle Scholar
  122. Urano D, Jones JC, Wang H, Matthews M, Bradford W, Bennetzen JL, Jones AM (2012a) G protein activation without a GEF in the plant kingdom. PLoS Genet 8:e1002756PubMedPubMedCentralCrossRefGoogle Scholar
  123. Urano D, Phan N, Jones JC, Yang J, Huang J, Grigston J, Taylor JP, Jones AM (2012b) Endocytosis of the seven-transmembrane RGS1 protein activates G-protein-coupled signalling in Arabidopsis. Nat Cell Biol 14:1079–1088PubMedPubMedCentralCrossRefGoogle Scholar
  124. Urano D, Colaneri A, Jones AM (2014) G alpha modulates salt-induced cellular senescence and cell division in rice and maize. J Exp Bot 65:6553–6561PubMedPubMedCentralCrossRefGoogle Scholar
  125. Urano D, Dong T, Bennetzen JL, Jones AM (2015a) Adaptive evolution of signaling partners. Mol Biol Evol 32:998–1007PubMedPubMedCentralCrossRefGoogle Scholar
  126. Urano D, Jackson D, Jones AM (2015b) A G protein alpha null mutation confers prolificacy potential in maize. J Exp Bot 66:4511–4515PubMedPubMedCentralCrossRefGoogle Scholar
  127. Urano D, Maruta N, Trusov Y, Stoian R, Wu Q, Liang Y, Jaiswal DK, Thung L, Jackson D, Botella JR, Jones AM (2016a) Saltational evolution of the heterotrimeric G protein signaling mechanisms in the plant kingdom. Sci Signal 9:ra93PubMedCrossRefGoogle Scholar
  128. Urano D, Miura K, Wu Q, Iwasaki Y, Jackson D, Jones AM (2016b) Plant morphology of heterotrimeric G protein mutants. Plant Cell Physiol 57:437–445PubMedPubMedCentralCrossRefGoogle Scholar
  129. 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 beta-subunit gene, RGB1, causes dwarfism and browning of internodes and lamina joint regions. Plant J 67:907–916PubMedCrossRefPubMedCentralGoogle Scholar
  130. Wang XQ, Ullah H, Jones AM, Assmann SM (2001) G protein regulation of ion channels and abscisic acid signaling in Arabidopsis guard cells. Science 292:2070–2072PubMedCrossRefGoogle Scholar
  131. Wang L, Xu YY, Ma QB, Li D, Xu ZH, Chong K (2006) Heterotrimeric G protein alpha subunit is involved in rice brassinosteroid response. Cell Res 16:916–922PubMedCrossRefGoogle Scholar
  132. Wang RS, Pandey S, Li S, Gookin TE, Zhao Z, Albert R, Assmann SM (2011) Common and unique elements of the ABA-regulated transcriptome of Arabidopsis guard cells. BMC Genomics 12:216PubMedPubMedCentralCrossRefGoogle Scholar
  133. 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 173:1235–1246PubMedCrossRefGoogle Scholar
  134. Warpeha KM, Hamm HE, Rasenick MM, Kaufman LS (1991) A blue-light-activated GTP-binding protein in the plasma membranes of etiolated peas. Proc Natl Acad Sci U S A 88:8925–8929PubMedPubMedCentralCrossRefGoogle Scholar
  135. Warpeha KM, Lateef SS, Lapik Y, Anderson M, Lee BS, Kaufman LS (2006) G-protein-coupled receptor 1, G-protein Galpha-subunit 1, and prephenate dehydratase 1 are required for blue light-induced production of phenylalanine in etiolated Arabidopsis. Plant Physiol 140:844–855PubMedPubMedCentralCrossRefGoogle Scholar
  136. Wei Q, Zhou W, Hu G, Wei J, Yang H, Huang J (2008) Heterotrimeric G-protein is involved in phytochrome A-mediated cell death of Arabidopsis hypocotyl. Cell Res 18:949–960. PMID: 19160542PubMedCrossRefGoogle Scholar
  137. Wendt T, Holme I, Dockter C, Preuss A, Thomas W, Druka A, Waugh R, Hansson M, Braumann I (2016) HvDep1 is a positive regulator of culm elongation and grain size in barley and impacts yield in an environment-dependent manner. PLoS One 11:e0168924PubMedPubMedCentralCrossRefGoogle Scholar
  138. Wheeler GL, Bitensky MW (1977) A light-activated GTPase in vertebrate photoreceptors: regulation of light-activated cyclic GMP phosphodiesterase. Proc Natl Acad Sci U S A 74:4238–4242PubMedPubMedCentralCrossRefGoogle Scholar
  139. Wolfenstetter S, Chakravorty D, Kula R, Urano D, Trusov Y, Sheahan MB, McCurdy DW, Assmann SM, Jones AM, Botella JR (2015) Evidence for an unusual transmembrane configuration of AGG3, a class C Ggamma subunit of Arabidopsis. Plant J 81:388–398PubMedCrossRefGoogle Scholar
  140. Wu Y, Xu X, Li S, Liu T, Ma L, Shang Z (2007) Heterotrimeric G-protein participation in Arabidopsis pollen germination through modulation of a plasmamembrane hyperpolarization-activated Ca2+-permeable channel. New Phytol 176:550–559PubMedCrossRefGoogle Scholar
  141. Xu DB, Chen M, Ma YN, Xu ZS, Li LC, Chen YF, Ma YZ (2015) A G-protein beta subunit, AGB1, negatively regulates the ABA response and drought tolerance by down-regulating AtMPK6-related pathway in Arabidopsis. PLoS One 10:e0116385PubMedPubMedCentralCrossRefGoogle Scholar
  142. Xu DB, Gao SQ, Ma YN, Wang XT, Feng L, Li LC, Xu ZS, Chen YF, Chen M, Ma YZ (2017a) The G-Protein beta subunit AGB1 promotes hypocotyl elongation through inhibiting transcription activation function of BBX21 in Arabidopsis. Mol Plant 10:1206–1223PubMedCrossRefGoogle Scholar
  143. Xu L, Yao X, Zhang N, Gong BQ, Li JF (2017b) Dynamic G protein alpha signaling in Arabidopsis innate immunity. Biochem Biophys Res Commun. pii: S0006-291X(17)31382-7Google Scholar
  144. Yu Y, Assmann SM (2015) The heterotrimeric G-protein beta subunit, AGB1, plays multiple roles in the Arabidopsis salinity response. Plant Cell Environ 38:2143–2156PubMedCrossRefGoogle Scholar
  145. Yu TY, Shi DQ, Jia PF, Tang J, Li HJ, Liu J, Yang WC (2016) The Arabidopsis receptor kinase ZAR1 is required for zygote asymmetric division and its daughter cell fate. PLoS Genet 12:e1005933PubMedPubMedCentralCrossRefGoogle Scholar
  146. Yu Y, Chakravorty D, Assmann SM (2018) The G protein beta subunit, AGB1, interacts with FERONIA in RALF1-regulated stomatal movement. Plant Physiol 176(3):2426–2440Google Scholar
  147. Zhang L, Hu G, Cheng Y, Huang J (2008a) Heterotrimeric G protein alpha and beta subunits antagonistically modulate stomatal density in Arabidopsis thaliana. Dev Biol 324:68–75PubMedCrossRefGoogle Scholar
  148. Zhang W, He SY, Assmann SM (2008b) The plant innate immunity response in stomatal guard cells invokes G-protein-dependent ion channel regulation. Plant J 56:984–996PubMedPubMedCentralCrossRefGoogle Scholar
  149. Zhang L, Wei Q, Wu W, Cheng Y, Hu G, Hu F, Sun Y, Zhu Y, Sakamoto W, Huang J (2009) Activation of the heterotrimeric G protein alpha-subunit GPA1 suppresses the ftsh-mediated inhibition of chloroplast development in Arabidopsis. Plant J 58:1041–1053PubMedCrossRefGoogle Scholar
  150. Zhang W, Jeon BW, Assmann SM (2011) Heterotrimeric G-protein regulation of ROS signalling and calcium currents in Arabidopsis guard cells. J Exp Bot 62:2371–2379PubMedCrossRefGoogle Scholar
  151. Zhang H, Wang M, Wang W, Li D, Huang Q, Wang Y, Zheng X, Zhang Z (2012) Silencing of G proteins uncovers diversified plant responses when challenged by three elicitors in Nicotiana benthamiana. Plant Cell Environ 35:72–85CrossRefGoogle Scholar
  152. Zhang T, Xu P, Wang W, Wang S, Caruana JC, Yang HQ, Lian H (2017) Arabidopsis G-protein beta subunit AGB1 interacts with BES1 to regulate Brassinosteroid signaling and cell elongation. Front Plant Sci 8:2225PubMedCrossRefGoogle Scholar
  153. Zhao J, Wang X (2004) Arabidopsis phospholipase Dalpha1 interacts with the heterotrimeric G-protein alpha-subunit through a motif analogous to the DRY motif in G-protein-coupled receptors. J Biol Chem 279:1794–1800PubMedCrossRefGoogle Scholar
  154. 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 Gbeta subunit of heterotrimeric G protein and functions in disease resistance. Mol Plant 2:513–525PubMedPubMedCentralCrossRefGoogle Scholar

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© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  1. 1.Donald Danforth Plant Science CenterSt. LouisUSA

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