Abstract
The activation of G-protein coupled receptors (GPCRs) by extracellular ligands constitutes the first step of heterotrimeric G-protein signalling in animals. In plants, canonical GPCRs have been known for over 25 years, often in association with agronomically important functions. But their role in plant G-protein signalling and even their annotation as GPCR was contested in the last decade, only to be revisited in the light of more recent evidences. In this first ever review on plant GPCRs, we catalogue all the plant GPCRs described to date and discuss the evidences for and against their role in plants in general and G-protein signalling in particular. We argue against writing off GPCRs and point to the missing links to be investigated to establish firm conclusions either way.
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References
Amora DX, Bresso E, Togawa RC, Grynberg P, Maigret B, Martins NF (2016) Prediction of G protein coupled receptors from plant genomes. Int J Curr Res Biosci Plant Biol 3(11):92–107. https://doi.org/10.20546/ijcrbp.2016.311.014
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(2):571–579. https://doi.org/10.1104/pp.103.026005
Baek S-A, Ahn SK, Kim KW, Choi J, Kim J, Ahn J et al (2019) Metabolic profiling reveals glucose and fructose accumulation in gcr1 knock-out mutant of Arabidopsis. Appl Biol Chem. https://doi.org/10.1186/s13765-019-0427-3
Böhme I, Beck-Sickinger AG (2009) Illuminating the life of GPCRs. Cell Commun Signal 7(1):1–22
Chakraborty N, Singh N, Kaur K, Raghuram N (2015) G-protein signaling components GCR1 and GPA1 mediate responses to multiple abiotic stresses in Arabidopsis. Front Plant Sci 6:1000. https://doi.org/10.3389/fpls.2015.01000
Chakraborty N, Kanyuka K, Jaiswal DK, Kumar A, Arora V, Malik A et al (2019) GCR1 and GPA1 coupling regulates nitrate, cell wall, immunity and light responses in Arabidopsis. Sci Rep 9(1):1–17
Chakraborty N, Sharma P, Kanyuka K, Pathak RR, Choudhury D, Hooley R et al (2015a) G-protein α-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(6):559–576
Chakraborty N, Sharma P, Kanyuka K, Pathak RR, Choudhury D, Hooley RA et al (2015) Transcriptome analysis of Arabidopsis GCR1 mutant reveals its roles in stress, hormones, secondary metabolism and phosphate starvation. PLoS ONE 10(2):e0117819. https://doi.org/10.1371/journal.pone.0117819
Chen J-G, Pandey S, Huang J, Alonso JM, Ecker JR, Assmann SM et al (2004) GCR1 can act independently of heterotrimeric G-protein in response to brassinosteroids and gibberellins in Arabidopsis seed germination. Plant Physiol 135(2):907–915. https://doi.org/10.1104/pp.104.038992
Colucci G, Apone F, Alyeshmerni N, Chalmers D, Chrispeels MJ (2002) GCR1, the putative Arabidopsis G protein-coupled receptor gene is cell cycle-regulated, and its overexpression abolishes seed dormancy and shortens time to flowering. Proc Natl Acad Sci 99(7):4736–4741. https://doi.org/10.1073/pnas.072087699
Gao Y, Zeng Q, Guo J, Cheng J, Ellis BE, Chen J-G (2007) Genetic characterization reveals no role for the reported ABA receptor, GCR2, in ABA control of seed germination and early seedling development in Arabidopsis. Plant J 52(6):1001–1013. https://doi.org/10.1111/j.1365-313X.2007.03291.x
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(7):R120. https://doi.org/10.1186/gb-2008-9-7-r120
Humphrey TV, Botella JR (2001) Re-evaluation of the cytokinin receptor role of the Arabidopsis gene GCR1. J Plant Physiol 158(5):645–653. https://doi.org/10.1078/0176-1617-00316
Illingworth CJR, Parkes KE, Snell CR, Mullineaux PM, Reynolds CA (2008) Criteria for confirming sequence periodicity identified by Fourier transform analysis: application to GCR2, a candidate plant GPCR? Biophys Chem 133(1–3):28–35. https://doi.org/10.1016/j.bpc.2007.11.004
Insel PA, Sriram K, Gorr MW, Wiley SZ, Michkov A, Salmerón C et al (2019) GPCRomics: an approach to discover GPCR drug targets. Trends Pharmacol Sci 40(6):378–387
Jaffé FW, Freschet G-EC, Valdes BM, Runions J, Terry MJ, Williams LE (2012) G protein–coupled receptor-type G proteins are required for light-dependent seedling growth and fertility in Arabidopsis. Plant Cell 24(9):3649–3668
Jin Y-N, Cui Z-h, Ma K, Yao J-L, Ruan Y-Y, Guo Z-F (2021) Characterization of ZmCOLD1, novel GPCR-Type G protein genes involved in cold stress from Zea mays L. and the evolution analysis with those from other species. Physiol Mol Biol Plants 27(3):619–632. https://doi.org/10.1007/s12298-021-00966-8
Johnston CA, Temple BR, Chen J-G, Gao Y, Moriyama EN, Jones AM et al (2007) Comment on “A G protein–coupled receptor is a plasmamembrane receptor for the plant hormone abscisic acid.” Science 318:914c–916c
Josefsson L-G, Rask L (1997) Cloning of a putative G-protein-coupled receptor from Arabidopsis thaliana. Eur J Biochem 249:415–420
Kanyuka K, Couch D, Hooley R (2001) A higher plant seven-transmembrane receptor that influences sensitivity to cytokinins. Curr Biol 11(7):535
Kim J, Moriyama EN, Warr CG, Clyne PJ, Carlson JR (2000) Identification of novel multi-transmembrane proteins from genomic databases using quasi-periodic structural properties. Bioinformatics 17(9):767–775
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35(6):1547
Letunic I, Bork P (2019) Interactive tree of life (iTOL) v4: recent updates and new developments. Nucleic Acids Res 47(W1):W256–W259
Liu F, Bian Z, Jia Z, Zhao Q, Song S (2012) The GCR1 and GPA1 participate in promotion of Arabidopsis primary root elongation induced by N-Acyl-homoserine lactones, the bacterial quorum-sensing signals. Mol Plant-Microbe Interactions® 25(5):677–683. https://doi.org/10.1094/mpmi-10-11-0274
Liu X, Yue Y, Li B, Nie Y, Li W, Wu W-H et al (2007) A G protein–coupled receptor is a plasma membrane receptor for the plant hormone abscisic acid. Science 315:1712–1716
Lu P, Magwanga RO, Kirungu JN, Dong Q, Cai X, Zhou Z et al (2019) Genome-wide analysis of the cotton G-coupled receptor proteins (GPCR) and functional analysis of GTOM1, a novel cotton GPCR gene under drought and cold stress. BMC Genomics. https://doi.org/10.1186/s12864-019-5972-y
Luo W, Huan Q, Xu Y, Qian W, Chong K, Zhang J (2021) Integrated global analysis reveals a vitamin E-vitamin K1 sub-network, downstream of COLD1, underlying rice chilling tolerance divergence. Cell Rep 36(3):109397. doi:https://doi.org/10.1016/j.celrep.2021.109397
Ma Y, Dai X, Xu Y, Luo W, Zheng X, Zeng D et al (2015) COLD1 confers chilling tolerance in rice. Cell 160(6):1209–1221. https://doi.org/10.1016/j.cell.2015.01.046
Maeda Y, Ide T, Koike M, Uchiyama Y, Kinoshita T (2008) GPHR is a novel anion channel critical for acidification and functions of the Golgi apparatus. Nat Cell Biol 10(10):1135–1145
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(4):656–669. doi:https://doi.org/10.1111/j.1365-313X.2007.03169.x
Moriyama EN, Strope PK, Opiyo SO, Chen Z, Jones AM (2006) Mining the Arabidopsis thaliana genome for highly-divergent seven transmembrane receptors. Genome Biol 7(10):R96. https://doi.org/10.1186/gb-2006-7-10-r96
Nordström KJ, Sällman Almén M, Edstam MM, Fredriksson R, Schiöth HB (2011) Independent hhsearch, needleman–wunsch-based, and motif analyses reveal the overall hierarchy for most of the G protein-coupled receptor families. Mol Biol Evol 28(9):2471–2480
Oliveira L, Paiva ACM, Vriend G (1999) A low resolution model for the interaction of G proteins with G protein-coupled receptors. Protein Eng 12(12):1087–1095
Pandey S, Assmann SM (2004) The Arabidopsis putative G protein–coupled receptor GCR1 interacts with the G protein α subunit GPA1 and regulates abscisic acid signaling. Plant Cell 16(6):1616–1632. https://doi.org/10.1105/tpc.020321
Pandey S, Nelson DC, Assmann SM (2009) Two novel GPCR-Type G proteins are abscisic acid receptors in Arabidopsis. Cell 136(1):136–148. https://doi.org/10.1016/j.cell.2008.12.026
Plakidou-Dymock S, Dymock D, Hooley R (1998) A higher plant seven-transmembrane receptor that influences sensitivity to cytokinins. Curr Biol 8:315–324
Taddese B, Upton GJG, Bailey GR, Jordan SRD, Abdulla NY, Reeves PJ et al (2014) Do plants contain G protein-coupled receptors? Plant Physiol 164(1):287–307. https://doi.org/10.1104/pp.113.228874
Tall GG, Krumins AM, Gilman AG (2003) Mammalian Ric-8A (synembryn) is a heterotrimeric Gα protein guanine nucleotide exchange factor. J Biol Chem 278(10):8356–8362
Tang YT, Hu T, Arterburn M, Boyle B, Bright JM, Emtage PC et al (2005) PAQR proteins: a novel membrane receptor family defined by an ancient7-transmembrane pass motif. J Mol Evol 61(3):372–380
The Rice Annotation Project Database (RAP-DB) (2008) : update (2008). Nucleic Acids Research, 36(Database), D1028-D1033. doi:https://doi.org/10.1093/nar/gkm978
Rogato A, Valkov VT, Alves LM, Apone F, Colucci G, Chiurazzi M (2016) Down-regulated Lotus japonicus GCR1 plants exhibit nodulation signalling pathways alteration. Plant Sci 247:71–82. https://doi.org/10.1016/j.plantsci.2016.03.007
Spiegel S, Milstien S (2003) Sphingosine-1-phosphate: an enigmatic signalling lipid. Nat Rev Mol Cell Biol 4(5):397–407
Urano D, Jones AM (2013) “Round up the usual suspects”: a comment on nonexistent plant G protein-coupled receptors. Plant Physiol 161(3):1097–1102. https://doi.org/10.1104/pp.112.212324
Urano D, Chen J-G, Botella JR, Jones AM (2013) Heterotrimeric G protein signalling in the plant kingdom. Open Biol 3(3):120186. https://doi.org/10.1098/rsob.120186
Urano D, Miura K, Wu Q, Iwasaki Y, Jackson D, Jones AM (2016) Plant morphology of heterotrimeric G protein mutants. Plant Cell Physiol 57(3):437–445. https://doi.org/10.1093/pcp/pcw002
Warpeha KM, Lateef SS, Lapik Y, Anderson M, Lee B-S, Kaufman LS (2006) G-protein-coupled receptor 1, G-protein Gα-subunit 1, and prephenate dehydratase 1 are required for blue light-induced production of phenylalanine in etiolated Arabidopsis. Plant Physiol 140(3):844–855. https://doi.org/10.1104/pp.105.071282
Warpeha KM, Upadhyay S, Yeh J, Adamiak J, Hawkins SI, Lapik YR et al (2007) The GCR1, GPA1, PRN1, NF-Y signal chain mediates both blue light and abscisic acid responses in Arabidopsis. Plant Physiol 143(4):1590–1600. https://doi.org/10.1104/pp.106.089904
Wei J, Li D-X, Zhang J-R, Shan C, Rengel Z, Song Z-B et al (2018) Phytomelatonin receptor PMTR1-mediated signaling regulates stomatal closure inArabidopsis thaliana. J Pineal Res 65(2):e12500. https://doi.org/10.1111/jpi.12500
Yadav DK, Tuteja N (2011) Rice G-protein coupled receptor (GPCR): In silico analysis and transcription regulation under abiotic stress. Plant Signal Behav 6(8):1079–1086. doi:https://doi.org/10.4161/psb.6.8.15771
Acknowledgements
The authors are thankful to Ms. Bhumika Madan and Ms. Ashu Tyagi for their assistance in organization and careful proof-reading of the manuscript.
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The authors are thankful to UKRI GCRF South Asian Nitrogen Hub (SANH) [NE/S009019/1] GGSIPU [GGSIPU/DRC/Ph.D/Adm/2016/1549], [GGSIPU/DRC/FRGS/2018/22] and [GGSIPU/DRC/FRGS/2019/1553/24] for providing research grants to NR. The authors are also thankful to UKRI GCRF-SANH for providing financial assistance to NC [NES/009019/1].
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Chakraborty, N., Raghuram, N. Life, death and resurrection of plant GPCRs. Plant Mol Biol 111, 221–232 (2023). https://doi.org/10.1007/s11103-022-01323-3
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DOI: https://doi.org/10.1007/s11103-022-01323-3