Abstract
This study characterizes the heterotrimeric G protein gene families in Triticum aestivum, their tissue-specific expression patterns during development and in response to biotic and abiotic stress conditions. There are three Gα genes, three Gβ and 12 Gγ genes, totaling 18 genes encoding heterotrimeric G proteins in the hexaploid wheat genome. Each haploid genome of the hexaploid T. aestivum has a single gene encoding the α subunit of the heterotrimeric G protein complex, GA1, a single Gβ and four Gγ genes. Each gene has three homeologous copies in the A, B and D genomes. The physical interaction between the Gβ (Gpb) and two Gγ subunits, Gpg1 and Gpg2, was shown through bimolecular fluorescence complementation (BiFC). The gene expression in response to biotic and abiotic stresses showed both up-regulation and down-regulation of members of the gene families. Gγ2-B and Gγ2-D are significantly upregulated during heat stress, GA1-D is upregulated by cold stress and Gγ1-A and Gγ1-D were upregulated by Fusarium graminearum inoculation in a F. graminearum resistant cultivar. This suggests that these members may play roles in biotic and abiotic signaling pathways and the roles of these genes within these pathways need further investigation.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Availability of data and material
Nucleotide sequences for the CDS and protein sequences from T. aestivum are included as supplementary material, and GenBank accession numbers are listed in the tables of the manuscript.
Code availability
Not applicable.
References
Arya GC, Kumar R, Bisht NC (2014) Evolution, expression differentiation and interaction specificity of heterotrimeric G-protein subunit gene family in the mesohexaploid Brassica rapa. PLoS ONE 9(9):e105771. https://doi.org/10.1371/journal.pone.0105771
Aubert Y, Vile D, Pervent M, Aldon D, Ranty B, Simonneau T, Vavasseur A, Galaud JP (2010) RD20, a stress-inducible caleosin, participates in stomatal control, transpiration and drought tolerance in Arabidopsis thaliana. Plant Cell Physiol 51(12):1975–1987. https://doi.org/10.1093/pcp/pcq155
Brunetti SC, Arseneault MKM, Gulick PJ (2018) Characterization of the Esi3/RCI2/PMP3 gene family in the Triticeae. BMC Genomics 19(1):898. https://doi.org/10.1186/s12864-018-5311-8
Brunetti SC, Arseneault MKM, Wright JA, Wang Z, Ehdaeivand MR, Lowden MJ, Rivoal J, Khalil HB, Garg G, Gulick PJ (2021) The stress induced caleosin, RD20/CLO3, acts as a negative regulator of GPA1 in Arabidopsis. Plant Mol Biol 107(3):159–175. https://doi.org/10.1007/s11103-021-01189-x
Choudhury SR, Bisht NC, Thompson R, Todorov O, Pandey S (2011) Conventional and novel Gγ protein families constitute the heterotrimeric G-protein signaling network in soybean. PLoS ONE 6(8):e23361. https://doi.org/10.1371/journal.pone.0023361
Dash S, Van Hemert J, Hong L, Wise RP, Dickerson JA (2012) PLEXdb: gene expression resources for plants and plant pathogens. Nucleic Acids Res 40:D1194–D1201. https://doi.org/10.1093/nar/gkr938
Devos KM, Dubcovsky J, Dvořák J, Chinoy CN, Gale MD (1995) Structural evolution of wheat chromosomes 4A, 5A, and 7B and its impact on recombination. Theor Appl Genet 91(2):282–288. https://doi.org/10.1007/bf00220890
Dong H, Yan S, Liu J, Liu P, Sun J (2019) TaCOLD1 defines a new regulator of plant height in bread wheat. Plant Biotechnol J 17(3):687–699. https://doi.org/10.1111/pbi.13008
Dvorak J, Wang L, Zhu T, Jorgensen CM, Luo MC, Deal KR, Gu YQ, Gill BS, Distelfeld A, Devos KM, Qi P, McGuire PE (2018) Reassessment of the evolution of wheat chromosomes 4A, 5A, and 7B. Theor Appl Genet 131(11):2451–2462. https://doi.org/10.1007/s00122-018-3165-8
Eversole K, Feuillet C, Mayer KF, Rogers J (2014) Slicing the wheat genome. Introduction. Science 345(6194):285–287. https://doi.org/10.1126/science.1257983
Fu L, Niu B, Zhu Z, Wu S, Li W (2012) CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 28(23):3150–3152. https://doi.org/10.1093/bioinformatics/bts565
Hossain MS, Koba T, Harada K (2003) Cloning and characterization of two full-length cDNAs, TaGA1 and TaGA2, encoding G-protein alpha subunits expressed differentially in wheat genome. Genes Genet Syst 78(2):127–138. https://doi.org/10.1266/ggs.78.127
Huang S, Sirikhachornkit A, Su X, Faris J, Gill B, Haselkorn R, Gornicki P (2002) Genes encoding plastid acetyl-CoA carboxylase and 3-phosphoglycerate kinase of the Triticum/Aegilops complex and the evolutionary history of polyploid wheat. Proc Natl Acad Sci USA 99(12):8133–8138. https://doi.org/10.1073/pnas.072223799
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(4):494–497. https://doi.org/10.1038/ng.352
Hurowitz EH, Melnyk JM, Chen YJ, Kouros-Mehr H, Simon MI, Shizuya H (2000) Genomic characterization of the human heterotrimeric G protein alpha, beta, and gamma subunit genes. DNA Res 7(2):111–120. https://doi.org/10.1093/dnares/7.2.111
International Wheat Genome Sequencing Consortium (IWGSC) (2022) A chromosome-based draft sequence of the hexaploid bread wheat (Triticum aestivum) genome. Science 345(6194):1251788. https://doi.org/10.1126/science.1251788
Jones AM, Assmann SM (2004) Plants: the latest model system for G-protein research. EMBO Rep 5(6):572–578. https://doi.org/10.1038/sj.embor.7400174
Jones JC, Duffy JW, Machius M, Temple BR, Dohlman HG, Jones AM (2011) The crystal structure of a self-activating G protein alpha subunit reveals its distinct mechanism of signal initiation. Sci Signal 4(159):8. https://doi.org/10.1126/scisignal.2001446
Karimi M, Inzé D, Depicker A (2002) GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci 7(5):193–195. https://doi.org/10.1016/s1360-1385(02)02251-3
Khalil HB, Wang Z, Wright JA, Ralevski A, Donayo AO, Gulick PJ (2011) Heterotrimeric Gα subunit from wheat (Triticum aestivum), GA3, interacts with the calcium-binding protein, Clo3, and the phosphoinositide-specific phospholipase C, PI-PLC1. Plant Mol Biol 77(1–2):145–158. https://doi.org/10.1007/s11103-011-9801-1
Khalil HB, Brunetti SC, Pham UM, Maret D, Laroche A, Gulick PJ (2014) Characterization of the caleosin gene family in the Triticeae. BMC Genom 15(1):239. https://doi.org/10.1186/1471-2164-15-239
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874. https://doi.org/10.1093/molbev/msw054
Li S, Liu Y, Zheng L, Chen L, Li N, Corke F, Lu Y, Fu X, Zhu Z, Bevan MW, Li Y (2012) The plant-specific G protein γ subunit AGG3 influences organ size and shape in Arabidopsis thaliana. New Phytol 194(3):690–703. https://doi.org/10.1111/j.1469-8137.2012.04083.x
Li Q, Zheng Q, Shen W, Cram D, Fowler DB, Wei Y, Zou J (2015) Understanding the biochemical basis of temperature-induced lipid pathway adjustments in plants. Plant Cell 27(1):86–103. https://doi.org/10.1105/tpc.114.134338
Liu Z, Xin M, Qin J, Peng H, Ni Z, Yao Y, Sun Q (2015) Temporal transcriptome profiling reveals expression partitioning of homeologous genes contributing to heat and drought acclimation in wheat (Triticum aestivum L.). BMC Plant Biol 15:152. https://doi.org/10.1186/s12870-015-0511-8
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(6):1209–1221. https://doi.org/10.1016/j.cell.2015.06.046
Pandey P, Irulappan V, Bagavathiannan MV, Senthil-Kumar M (2017) Impact of combined abiotic and biotic stresses on plant growth and avenues for crop improvement by exploiting physio-morphological traits. Front Plant Sci 8:537. https://doi.org/10.3389/fpls.2017.00537
Pingault L, Choulet F, Alberti A, Glover N, Wincker P, Feuillet C, Paux E (2015) Deep transcriptome sequencing provides new insights into the structural and functional organization of the wheat genome. Genome Biol 16(1):29. https://doi.org/10.1186/s13059-015-0601-9
Ramírez-González RH, Borrill P, Lang D, Harrington SA, Brinton J et al (2018) The transcriptional landscape of polyploid wheat. Science 361(6403):6089. https://doi.org/10.1126/science.aar6089
Ridha Farajalla M, Gulick PJ (2007) The alpha-tubulin gene family in wheat (Triticum aestivum L.) and differential gene expression during cold acclimation. Genome 50(5):502. https://doi.org/10.1139/g07-027
Schreiber AW, Sutton T, Caldo RA, Kalashyan E, Lovell B, Mayo G, Muehlbauer GJ, Druka A, Waugh R, Wise RP, Langridge P, Baumann U (2009) Comparative transcriptomics in the Triticeae. BMC Genomics 10:285. https://doi.org/10.1186/1471-2164-10-285
Subramaniam G, Trusov Y, Lopez-Encina C, Hayashi S, Batley J, Botella JR (2016) Type B heterotrimeric G protein γ-subunit regulates auxin and ABA signaling in tomato. Plant Physiol 170(2):1117–1134. https://doi.org/10.1104/pp.15.01675
Takahashi S, Katagiri T, Yamaguchi-Shinozaki K, Shinozaki K (2000) An Arabidopsis gene encoding a Ca2+-binding protein is induced by abscisic acid during dehydration. Plant Cell Physiol 41(7):898–903. https://doi.org/10.1093/pcp/pcd010
Temple BR, Jones AM (2007) The plant heterotrimeric G-protein complex. Annu Rev Plant Biol 58:249–266. https://doi.org/10.1146/annurev.arplant.58.032806.103827
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(1):210–220. https://doi.org/10.1104/pp.105.069625
Trusov Y, Chakravorty D, Botella JR (2012) Diversity of heterotrimeric G-protein γ subunits in plants. BMC Res Notes 5:608. https://doi.org/10.1186/1756-0500-5-608
Tsugama D, Liu S, Takano T (2013) Arabidopsis heterotrimeric G protein β subunit, AGB1, regulates brassinosteroid signalling independently of BZR1. J Bot Exp 64(11):3213–3223. https://doi.org/10.1093/jxb/ert159
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 5(2):393–409. https://doi.org/10.1105/tpc.006148
Urano D, Jones AM (2014) Heterotrimeric G protein-coupled signaling in plants. Annu Rev Plant Biol 65:365–384. https://doi.org/10.1146/annurev-arplant-050213-040133
Urano D, Jones JC, Wang H, Matthews M, Bradford W, Bennetzen J, Jones AM (2012) G protein activation without a GEF in the plant kingdom. PLoS Genet 8(6):e1002756. https://doi.org/10.1371/journal.pgen.1002756
Urano D, Chen JG, 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
Whelan S, Goldman N (2001) A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol 8(5):691–699. https://doi.org/10.1093/oxfordjournals.molbev.a003851
Yadav DK, Islam SM, Tuteja N (2012) Rice heterotrimeric G-protein gamma subunits (RGG1 and RGG2) are differentially regulated under abiotic stress. Plant Signal Behav 7(7):733–740. https://doi.org/10.4161/psb.20356
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(7):2371–2379. https://doi.org/10.1093/jxb/erq424
Zhang T, Xu P, Wang W, Wang S, Caruana JC, Yang HQ, Lian H (2018) Arabidopsis G-protein β subunit AGB1 interacts with BES1 to regulate brassinosteroid signaling and cell elongation. Front Plant Sci 8:2225. https://doi.org/10.3389/fpls.2017.02225
Acknowledgements
We would like to thank Dr. Alan Jones, North Carolina State University for the gift of the PCL YFP BiFC Constructs. The authors acknowledge the Centre for Microscopy and Cellular Imaging (CMCI) funded by Concordia University, Montreal, Canada, and the Canada Foundation for Innovation.
Funding
This work is supported by grants from Indian Council of Agricultural Research, India, the Natural Science and Engineering Research Council of Canada, and the Concordia University Faculty of Arts and Science (Grant RGPIN/667-2016).
Author information
Authors and Affiliations
Contributions
NDG, ZH, and SCB carried out the bioinformatic analysis, NDG carried out the BiFC assays and wrote the initial draft of the manuscript, ZH carried out laboratory analysis of different wheat cultivars. PJG conceived and directed the research. All authors contributed to the preparation of the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare there is no conflict of interest in the publication.
Ethics approval
Not applicable.
Consent to participate
Not applicable.
Consent for publication
All authors have given consent to publish.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Gawande, N.D., Hamiditabar, Z., Brunetti, S.C. et al. Characterization of the heterotrimeric G protein gene families in Triticum aestivum and related species. 3 Biotech 12, 99 (2022). https://doi.org/10.1007/s13205-022-03156-9
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s13205-022-03156-9