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

C. Y. Liu1, Y. Z. Xu1, W. Fan1, D. P. Long1, B. N. Cao1, Z. H. Xiang1, A. C. Zhao1,*
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 , one , two , 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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Liu, C.Y., Xu, Y.Z., Fan, W., Long, D.P., Cao, B.N., Xiang, Z.H., & Zhao, A.C. (2018). Identification of the genes involved in heterotrimeric G-protein signaling in mulberry and their regulation by abiotic stresses and signal molecules. Biologia plantarum62(2), 277-286. doi: 10.1007/s10535-018-0779-2.
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References

  1. 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...
  2. 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...
  3. 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...
  4. 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...
  5. 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...
  6. 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...
  7. 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...
  8. 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...
  9. 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.
  10. 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...
  11. 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...
  12. 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...
  13. 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...
  14. 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...
  15. 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...
  16. 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.
  17. 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.
  18. 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...
  19. 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...
  20. 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...
  21. 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...
  22. 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...
  23. 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...
  24. 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...
  25. 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...
  26. 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...
  27. 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...
  28. 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...
  29. 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...
  30. 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...
  31. 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.
  32. 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...
  33. 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...
  34. 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...
  35. 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...
  36. 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...
  37. 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...
  38. Urano, D., Jones, A.M.: Heterotrimeric G protein-coupled signaling in plants. - Annu. Rev. Plant Biol. 65: 365-384, 2014. Go to original source...
  39. 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...
  40. 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...
  41. 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...
  42. Wettschureck, N., Offermanns, S.: Mammalian G proteins and their cell type specific functions. - Physiol. Rev. 85: 1159-1204, 2005. Go to original source...
  43. 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...
  44. 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...
  45. 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...
  46. 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...