Biologia plantarum 62:277-286, 2018 | DOI: 10.1007/s10535-018-0779-2
Identification of the genes involved in heterotrimeric G-protein signaling in mulberry and their regulation by abiotic stresses and signal molecules
- 1 State Key Laboratory of Silkworm Genome Biology, Key Laboratory of Sericultural Biology and Genetic Breeding, Ministry of Agriculture, Southwest University, Chongqing, P.R. China
Heterotrimeric guanine-nucleotide-binding proteins (G-proteins) play important roles in signal transduction and regulate responses to various stresses. Although G-protein signaling pathways have been extensively identified and characterized in model plants, there is little knowledge in non-model and especially in woody plants. Mulberry is an economically and ecologically important perennial tree, which is adaptable to many environmental stresses. In this study, we identified and cloned six G-protein genes including one Gα, one Gβ, two Gγ, one RGS (regulator of G-protein signaling protein) and one RACK1 (receptor for activated C kinase 1) involved in G-protein signaling. Sequence and phylogenetic analysis revealed that Morus G-proteins are evolutionarily conserved compared with those of other plants. A real-time quantitative reverse transcription polymerase chain reaction analysis showed that Morus G-protein signaling genes were ubiquitously but differentially expressed in various tissues. The expression of all of these genes was affected by abiotic stresses and signal molecules, which indicated that Morus G-protein signaling may be involved in environmental stress and defense responses.
Keywords: biotic stress; expression profile; Morus atropurpurea; Morus notabilis
Subjects: G-protein; gene expression; amino acid sequences; phylogenetic analysis; anther culture; cold; drought; salinity
Species: Morus notabilis; Morus atropurpurea
Received: April 15, 2017; Revised: August 26, 2017; Accepted: August 28, 2017; Published: June 1, 2018Show citation
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Supplementary files
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References
- Arya, G.C., Kumar, R., Bisht, N.C.: Evolution, expression differentiation and interaction specificity of heterotrimeric G-protein subunit gene family in the mesohexaploid Brassica rapa. - PloS ONE 9: e105771, 2014.
Go to original source...
- Chen, J.G., Ullah, H., Temple, B., Liang, J., Guo, J., Alonso, J.M.: RACK1 mediates multiple hormone responsiveness and developmental processes in Arabidopsis. - J. exp. Bot. 57: 2697-2708, 2006.
Go to original source...
- Chen, J.G., Willard, F.S., Huang, J., Liang, J., Chasse, S.A., Jones, A.M., Siderovski, D.P.: A seven-transmembrane RGS protein that modulates plant cell proliferation. - Science 301: 1728-1731, 2003.
Go to original source...
- Chen, Y., Zhu, X., Zhu, X.-B., Yu, Y.-F., Ge, H.-M., Gao, Y., Liang, J.-S.: Identification of the regulator of G-protein signaling protein responsive to plant hormones and abiotic stresses in Brassica napus. - J. Integr. Agr. 13: 2634-2644, 2014.
Go to original source...
- Cheng, Z., Li, J.F., Niu, Y., Zhang, X.C., Woody, O.Z., Xiong, Y., Djonović, S., Millet, Y., Bush, J., McConkey, B.J., Sheen, J., Ausubel, F.M.: Pathogen-secreted proteases activate a novel plant immune pathway. - Nature 521: 213-216, 2015.
Go to original source...
- Colaneri, A.C., Tunc-Ozdemir, M., Huang, J.P., Jones, A.M.: Growth attenuation under saline stress is mediated by the heterotrimeric G protein complex. - BMC Plant Biol. 14: 129, 2014.
Go to original source...
- Dell, E.J., Connor, J., Chen, S., Stebbins, E.G., Skiba, N.P., Mochly-Rosen, D., Hamm, H.E.: The betagamma subunit of heterotrimeric G proteins interacts with RACK1 and two other WD repeat proteins. - J. biol. Chem. 277: 49888-49895, 2002.
Go to original source...
- Gao, Y., Li, T., Liu, Y., Ren, C., Zhao, Y., Wang, M.: Isolation and characterization of gene encoding G protein alpha subunit protein responsive to plant hormones and abiotic stresses in Brassica napus. - Mol. Biol. Rep. 37: 3957-3965, 2010a.
Go to original source...
- Gao, Y., Li, T., Zhao, Y., Ren, C., Zhang, Y., Wang, M.: Isolation and characterization of a G protein γ subunit gene responsive to plant hormones and abiotic stresses in Brassica napus L. - Acta Physiol. Plant 33: 391-399, 2010b.
- Hackenberg, D., Sakayama, H., Nishiyama, T., Pandey, S.: Characterization of the heterotrimeric G-protein complex and its regulator from the green alga Chara braunii expands the evolutionary breadth of plant G-protein signaling. - Plant Physiol. 163: 1510-1517, 2013.
Go to original source...
- He, N., Zhang, C., Qi, X., Zhao, S., Tao, Y., Yang, G., Lee, T.H., Wang, X., Cai, Q., Li, D., Lu, M., Liao, S., Luo, G., He, R., Tan, X., Xu, Y., Li, T., Zhao, A., Jia, L., Fu, Q., Zeng, Q., Gao, C., Ma, B., Liang, J., Wang, X., Shang, J., Song, P., Wu, H., Fan, L., Wang, Q., Shuai, Q., Zhu, J., Wei, C., Zhu-Salzman, K., Jin, D., Wang, J., Liu, T., Yu, M., Tang, C., Wang, Z., Dai, F., Chen, J., Liu, Y., Zhao, S., Lin, T., Zhang, S., Wang, J., Wang, J., Yang, H., Yang, G., Wang, J., Paterson, A.H., Xia, Q., Ji, D., Xiang, Z.: Draft genome sequence of the mulberry tree Morus notabilis. - Nat. Commun. 4: 2445, 2013.
Go to original source...
- Huang, X., Qian, Q., Liu, Z., Sun, H., He, S., Luo, D., Xia, G., Chu, C., Li, J., Fu, X.: Natural variation at the DEP1 locus enhances grain yield in rice. - Nat. Genet. 41: 494-497, 2009.
Go to original source...
- Ishida, S., Takahashi, Y., Nagata, T.: Isolation of cDNA of an auxin-regulated gene encoding a G protein beta subunit-like protein from tobacco BY-2 cells. - Proc. nat. Acad. Sci. USA 90: 11152-11156, 1993.
Go to original source...
- Jangam, A.P., Pathak, R.R., Raghuram, N.: Microarray analysis of rice d1 (RGA1) mutant reveals the potential role of Gprotein alpha subunit in regulating multiple abiotic stresses such as drought, salinity, heat, and cold. - Front. Plant Sci. 7: 11, 2016.
Go to original source...
- Jones, J.C., Duffy, J.W., Machius, M., Temple, B.R., Dohlman, H.G., Jones, A.M.: The crystal structure of a self-activating G protein alpha subunit reveals its distinct mechanism of signal initiation. - Sci. Signal. 4: ra8 2011.
Go to original source...
- Klopffleisch, K., Phan, N., Augustin, K., Bayne, R.S., Booker, K.S., Botella, J.R., Carpita, N.C., Carr, T., Chen, J.G., Cooke, T.R., Frick-Cheng, A., Friedman, E.J., Fulk, B., Hahn, M.G., Jiang, K., Jorda, L., Kruppe, L., Liu, C., Lorek, J., McCann, M.C., Molina, A., Moriyama, E.N., Mukhtar, M.S., Mudgil, Y., Pattathil, S., Schwarz, J., Seta, S., Tan, M., Temp, U., Tplorusov, Y., Urano, D., Welter, B., Yang, J., Panstruga, R., Uhrig, J.F., Jones, A.M.: Arabidopsis Gprotein interactome reveals connections to cell wall carbohydrates and morphogenesis. - Mol. syst. Biol. 7: 532, 2011.
- Kumar, R., Arya, G.C., Bisht, N.C.: Differential expression and interaction specificity of the heterotrimeric G-protein family in Brassica nigra reveal their developmental- and conditionspecific roles. - Plant Cell Physiol. 55: 1954-1968, 2014.
- Lee, S., Rojas, C.M., Ishiga, Y., Pandey, S., Mysore, K.S.: Arabidopsis heterotrimeric G-proteins play a critical role in host and nonhost resistance against Pseudomonas syringae pathogens. - PLoS ONE 8: e82445, 2013.
Go to original source...
- Ma, H., Yanofsky, M.F., Meyerowitz, E.M.: Molecular cloning and characterization of GPA1, a G protein alpha subunit gene from Arabidopsis thaliana. - Proc. nat. Acad. Sci. USA 87: 3821-3825, 1990.
Go to original source...
- Mochly-Rosen, D., Khaner, H., Lopez, J.: Identification of intracellular receptor proteins for activated protein kinase C. - Proc. nat. Acad. Sci. USA 88: 3997-4000, 1991.
Go to original source...
- Oki, K., Inaba, N., Kitagawa, K., Fujioka, S., Kitano, H., Fujisawa, Y., Kato, H., Iwasaki, Y.: Function of the alpha subunit of rice heterotrimeric G protein in brassinosteroid signaling. - Plant Cell Physiol. 50:161-172, 2009.
Go to original source...
- Pandey, S., Chen, J.G., Jones, A.M., Assmann, S.M.: G-protein complex mutants are hypersensitive to abscisic acid regulation of germination and postgermination development. - Plant Physiol. 141:243-256, 2006.
Go to original source...
- Perfus-Barbeoch, L., Jones, A.M., Assmann, S.M.: Plant heterotrimeric G protein function: insights from Arabidopsis and rice mutants. - Curr. Opin. Plant Biol. 7: 719-731, 2004.
Go to original source...
- Ramachandra Reddy, A., Chaitanya, K.V., Jutur, P.P., Sumithra, K.: Differential antioxidative responses to water stress among five mulberry (Morus alba L.) cultivars. - Environ. exp. Bot. 52: 33-42, 2004.
Go to original source...
- Ron, D., Chen, C.H., Caldwell, J., Jamieson, L., Orr, E., Mochly-Rosen, D.: Cloning of an intracellular receptor for protein kinase C: a homolog of the beta subunit of G proteins. - Proc. nat. Acad. Sci. USA 93: 839-843, 1994.
Go to original source...
- Roy Choudhury, S., Bisht, N.C., Thompson, R., Todorov, O., Pandey, S.: Conventional and novel Ggamma protein families constitute the heterotrimeric G-protein signaling network in soybean. - PloS ONE 6: e23361, 2011.
Go to original source...
- Roy Choudhury, S., Pandey, S.: Specific subunits of heterotrimeric G proteins play important roles during nodulation in soybean. - Plant Physiol. 162: 522-533, 2013.
Go to original source...
- Roy Choudhury, S., Pandey, S.: Phosphorylation-dependent regulation of G-protein cycle during nodule formation in soybean. - Plant Cell 27: 3260-3276, 2015.
Go to original source...
- Roy Choudhury, S., Riesselman, A.J., Pandey, S.: Constitutive or seedspecific 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: 49-59, 2014a.
Go to original source...
- Roy Choudhury, S., Wang, Y., Pandey, S.: Soyabean Gα proteins with distinct biochemical properties exhibit differential ability to complement Saccharomyces cerevisiae gpa1 mutant. - Biochem. J. 461:75-85, 2014b.
Go to original source...
- Shi, C., Qi, C., Ren, H., Huang, A., Hei, S., She, X.: Ethylene mediates brassinosteroid-induced stomatal closure via G alpha protein-activated hydrogen peroxide and nitric oxide production in Arabidopsis. - Plant J. 82: 280-301, 2015.
- Takano, K.N., Jiang, H., Kubo, T., Sweeney, M., Matsumoto, T., Kanamori, H., Padhukasahasram, B., Bustamante, C., Yoshimura, A., Doi, K., McCouch, S.: Evolutionary history of GS3, a gene conferring grain length in rice. - Genetics 182: 1323-1334, 2009.
Go to original source...
- Trusov, Y., Chakravorty, D., Botella, J.R.: Diversity of heterotrimeric G-protein γ subunits in plants. - BMC Res. Notes 31: 608, 2012.
Go to original source...
- Trusov, Y., Sewelam, N., Rookes, J.E., Kunkel, M., Nowak, E., Schenk, P.M., Botella, J.R.: Heterotrimeric G proteinsmediated resistance to necrotrophic pathogens includes mechanisms independent of salicylic acid-, jasmonic acid/ethylene- and abscisic acid-mediated defense signaling. - Plant J. 58: 69-81, 2009.
Go to original source...
- Tsugama, D., Liu, S., Takano, T.: A bZIP protein, VIP1, interacts with Arabidopsis heterotrimeric G protein β subunit, AGB1. - Plant Physiol. Biochem. 71: 240-246, 2013.
Go to original source...
- Ullah, H., Chen, J.G., Temple, B., Boyes, D.C., Alonso, J.M., Davis, K.R., Ecker, J.R., Jones, A.M.: The beta-subunit of the Arabidopsis G protein negatively regulates auxininduced cell division and affects multiple developmental processes. - Plant Cell 15: 393-409, 2003.
Go to original source...
- Urano, D., Chen, J.G., Botella, J.R., Jones, A.M.: Heterotrimeric G protein signalling in the plant kingdom. - Open Biol. 3: 120186, 2013.
Go to original source...
- Urano, D., Jones, A.M.: Heterotrimeric G protein-coupled signaling in plants. - Annu. Rev. Plant Biol. 65: 365-384, 2014.
Go to original source...
- Urano, D., Phan, N., Jones, J.C., Yang, J., Huang, J., Grigston, J., Taylor, J.P., Jones, A.M.: Endocytosis of the seventransmembrane RGS1 protein activates G-protein-coupled signalling in Arabidopsis. - Nat. cell. Biol. 14: 1079-1088, 2012.
Go to original source...
- Wang, X.Q., Ullah, H., Jones, A.M., Assmann, S.M.: G protein regulation of ion channels and abscisic acid signaling in Arabidopsis guard cells. - Science 292: 2070-2072, 2001.
Go to original source...
- Wei, C., Liu, X., Long, D., Guo, Q., Fang, Y., Bian, C., Zhang, D., Zeng, Q., Xiang, Z., Zhao, A.: Molecular cloning and expression analysis of mulberry MAPK gene family. - Plant Physiol. Biochem. 77: 108-116, 2014.
Go to original source...
- Wettschureck, N., Offermanns, S.: Mammalian G proteins and their cell type specific functions. - Physiol. Rev. 85: 1159-1204, 2005.
Go to original source...
- Xu, D.B., Chen, M., Ma, Y.N., Xu, Z.S., Li, L.C., Chen, Y.F., Ma, Y.Z.: A G-protein beta subunit, AGB1, negatively regulates the ABA response and drought tolerance by downregulating AtMPK6-related pathway in Arabidopsis. - PloS ONE 10: e0116385, 2015.
Go to original source...
- Yadav, D.K., Shukla, D., Tuteja, N.: Rice heterotrimeric G-protein alpha subunit (RGA1): in silico analysis of the gene and promoter and its upregulation under abiotic stress. - Plant Physiol. Biochem. 63: 262-271, 2013.
Go to original source...
- Yadav, D.K., Shukla, D., Tuteja, N.: Isolation, in silico characterization, localization and expression analysis of abiotic stress-responsive rice G-protein β subunit (RGB1). - Plant Signal. Behav. 9: e28890, 2014.
Go to original source...
- Zhang, D.P., Zhou, Y., Yin, J.F., Yan, X.J., Lin, S., Xu, W.F., Baluška, F., Wang, Y.P., Xia, Y.J., Liang, G.H., Liang, J.S.: Rice G-protein subunits qPE9-1 and RGB1 play distinct roles in abscisic acid responses and drought adaptation. - J. exp. Bot. 66: 6371-6384, 2015.
Go to original source...