A Novel G-Protein-Coupled Receptors Gene from Upland Cotton Enhances Salt Stress Tolerance in Transgenic Arabidopsis

Genes - Tập 9 Số 4 - Trang 209
Pu Lu1, Zhongli Zhou2,1, Hejun Lu3, Joy Nyangasi Kirungu1, Yangyang Wei4, Qi Dong1, Xingxing Wang1, Xiaoyan Cai1, Kunbo Wang1, Fang Liu1
1Research Base in Anyang Institute of Technology, State Key Laboratory of Cotton Biology, Institute of Cotton Research, Chinese Academy of Agricultural Science (ICR, CAAS), Anyang 455000, Henan, China
2Jaramogi Oginga Odinga University of Science and Technology, P.O. Box 210-40601, 210 Bondo, Kenya
3Gembloux Agro-Bio Tech, University of Liège, 5030 Gembloux, Belgium
4Anyang Institute of Technology, Anyang 455000, Henan, China

Tóm tắt

Plants have developed a number of survival strategies which are significant for enhancing their adaptation to various biotic and abiotic stress factors. At the transcriptome level, G-protein-coupled receptors (GPCRs) are of great significance, enabling the plants to detect a wide range of endogenous and exogenous signals which are employed by the plants in regulating various responses in development and adaptation. In this research work, we carried out genome-wide analysis of target of Myb1 (TOM1), a member of the GPCR gene family. The functional role of TOM1 in salt stress tolerance was studied using a transgenic Arabidopsis plants over-expressing the gene. By the use of the functional domain PF06454, we obtained 16 TOM genes members in Gossypium hirsutum, 9 in Gossypium arboreum, and 11 in Gossypium raimondii. The genes had varying physiochemical properties, and it is significant to note that all the grand average of hydropathy (GRAVY) values were less than one, indicating that all are hydrophobic in nature. In all the genes analysed here, both the exonic and intronic regions were found. The expression level of Gh_A07G0747 (GhTOM) was significantly high in the transgenic lines as compared to the wild type; a similar trend in expression was observed in all the salt-related genes tested in this study. The study in epidermal cells confirmed the localization of the protein coded by the gene TOM1 in the plasma membrane. Analysis of anti-oxidant enzymes showed higher concentrations of antioxidants in transgenic lines and relatively lower levels of oxidant substances such as H2O2. The low malondialdehyde (MDA) level in transgenic lines indicated that the transgenic lines had relatively low level of oxidative damage compared to the wild types. The results obtained indicate that Gh_A07G0747 (GhTOM) can be a putative target gene for enhancing salt stress tolerance in plants and could be exploited in the future for the development of salt stress-tolerant cotton cultivars.

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Tài liệu tham khảo

Žádníková, P., Smet, D., Zhu, Q., Straeten, D., and Van Der Benková, E. (2015). Strategies of seedlings to overcome their sessile nature: Auxin in mobility control. Front. Plant Sci., 6.

Fujita, 2006, Crosstalk between abiotic and biotic stress responses: A current view from the points of convergence in the stress signaling networks, Curr. Opin. Plant Biol., 9, 436, 10.1016/j.pbi.2006.05.014

Atkinson, 2012, The interaction of plant biotic and abiotic stresses: From genes to the field, J. Exp. Bot., 63, 3523, 10.1093/jxb/ers100

Gilroy, 2001, Signal processing and transduction in plant cells: The end of the beginning?, Nat. Rev. Mol. Cell Biol., 2, 307, 10.1038/35067109

Mahajan, 2005, Cold, salinity and drought stresses: An overview, Arch. Biochem. Biophys., 444, 139, 10.1016/j.abb.2005.10.018

Dangl, 1995, Talking through walls: Signaling in plant development, Cell, 83, 1071, 10.1016/0092-8674(95)90134-5

Xue, 2008, Magnificent seven: Roles of G protein-coupled receptors in extracellular sensing in fungi, FEMS Microbiol. Rev., 32, 1010, 10.1111/j.1574-6976.2008.00131.x

Jacoby, 2006, The 7 TM G-protein-coupled receptor target family, ChemMedChem, 1, 760, 10.1002/cmdc.200600134

Wang, 2001, G protein regulation of ion channels and abscisic acid signaling in Arabidopsis guard cells, Science, 292, 2070, 10.1126/science.1059046

Wojcikiewicz, 2004, Regulated ubiquitination of proteins in GPCR-initiated signaling pathways, Trends Pharmacol. Sci., 25, 35, 10.1016/j.tips.2003.11.008

Latijnhouwers, 2004, A Gα subunit controls zoospore motility and virulence in the potato late blight pathogen Phytophthora infestans, Mol. Microbiol., 51, 925, 10.1046/j.1365-2958.2003.03893.x

Trusov, 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, 10.1111/j.1365-313X.2008.03755.x

Trusov, 2016, Plant G-Proteins come of age: Breaking the bond with animal models, Front. Chem., 4, 24, 10.3389/fchem.2016.00024

Urano, 2014, Heterotrimeric G Protein–coupled signaling in plants, Annu. Rev. Plant Biol., 65, 365, 10.1146/annurev-arplant-050213-040133

Taddese, 2014, Do plants contain G Protein-coupled receptors?, Plant Physiol., 164, 287, 10.1104/pp.113.228874

Josefsson, 1997, Cloning of a putative G-protein-coupled receptor from Arabidopsis thaliana, Eur. J. Biochem., 249, 415, 10.1111/j.1432-1033.1997.t01-1-00415.x

Dymock, 1998, A higher plant seven-transmembrane receptor that influences sensitivity to cytokinins, Curr. Biol., 8, 315, 10.1016/S0960-9822(98)70131-9

Gookin, 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, R120, 10.1186/gb-2008-9-7-r120

Baldwin, 1993, The probable arrangement of the helices in G protein-coupled receptors, EMBO J., 12, 1693, 10.1002/j.1460-2075.1993.tb05814.x

Dong, 2014, Structural and functional insights into the juxtamembranous amino-terminal tail and extracellular loop regions of class B GPCRs, Br. J. Pharmacol., 171, 1085, 10.1111/bph.12293

Wheatley, 2012, Lifting the lid on GPCRs: The role of extracellular loops, Br. J. Pharmacol., 165, 1688, 10.1111/j.1476-5381.2011.01629.x

Chakraborty, 2015, 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, 559, 10.1007/s11103-015-0374-2

Chakraborty, 2015, G-protein signaling components GCR1 and GPA1 mediate responses to multiple abiotic stresses in Arabidopsis, Front. Plant Sci., 6, 1000, 10.3389/fpls.2015.01000

Munns, 2002, Comparative physiology of salt and water stress, Plant Cell Environ., 25, 239, 10.1046/j.0016-8025.2001.00808.x

Wang, 2003, Plant responses to drought, salinity and extreme temperatures: Towards genetic engineering for stress tolerance, Planta, 218, 1, 10.1007/s00425-003-1105-5

Gill, 2010, Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants, Plant Physiol. Biochem., 48, 909, 10.1016/j.plaphy.2010.08.016

Apel, 2004, Reactive oxygen species: Metabolism, oxidative stress, and signal transduction, Annu. Rev. Plant Biol., 55, 373, 10.1146/annurev.arplant.55.031903.141701

Birben, 2012, Oxidative stress and antioxidant defense, WAO J., 5, 9

Gossett, 1994, Antioxidant response to NaCl stress in salt-tolerant and salt-sensitive cultivars of cotton, Crop Sci., 34, 706, 10.2135/cropsci1994.0011183X003400030020x

Vaidyanathan, 2003, Scavenging of reactive oxygen species in NaCl-stressed rice (Oryza sativa L.)—Differential response in salt-tolerant and sensitive varieties, Plant Sci., 165, 1411, 10.1016/j.plantsci.2003.08.005

Radi, 2013, Physiological and biochemical responses of salt-tolerant and salt-sensitive wheat and bean cultivars to salinity, J. Biol., 3, B72

Palacio, 2013, Effect of oxidative stress on plasma membrane fluidity of THP-1 induced macrophages, Biochim. Biophys. Acta Biomembr., 1828, 357, 10.1016/j.bbamem.2012.08.013

Janero, 1990, Malondialdehyde and thiobarbituric acid-reactivity as diagnostic indices of lipid peroxidation and peroxidative tissue injury, Free Radic. Biol. Med., 9, 515, 10.1016/0891-5849(90)90131-2

Finn, R.D., Clements, J., and Eddy, S.R. (2011). HMMER web server: Interactive sequence similarity searching. Nucleic Acids Res., 39.

Horton, 2007, WoLF PSORT: Protein localization predictor, Nucleic Acids Res., 35, W585, 10.1093/nar/gkm259

Emanuelsson, 2007, Locating proteins in the cell using TargetP, SignalP and related tools, Nat. Protoc., 2, 953, 10.1038/nprot.2007.131

Hawkins, 2005, Prediction of subcellular localization using sequence-biased recurrent networks, Bioinformatics, 21, 2279, 10.1093/bioinformatics/bti372

Zhu, T., Liang, C.Z., Meng, Z.G., Sun, G.Q., Meng, Z.H., Guo, S.D., and Zhang, R. (2017). CottonFGD: An integrated functional genomics database for cotton. BMC Plant Biol., 17.

Magwanga, R.O., Lu, P., Kirungu, J.N., Lu, H., Wang, X., Cai, X., Zhou, Z., Zhang, Z., Salih, H., and Wang, K. (2018). Characterization of the late embryogenesis abundant (LEA) proteins family and their role in drought stress tolerance in upland cotton. BMC Genet., 19.

Kumar, 2016, MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets, Mol. Biol. Evol., 33, 1870, 10.1093/molbev/msw054

Hu, 2015, GSDS 2.0: An upgraded gene feature visualization server, Bioinformatics, 31, 1296, 10.1093/bioinformatics/btu817

Bailey, 2009, MEME SUITE: Tools for motif discovery and searching, Nucleic Acids Res., 37, W202, 10.1093/nar/gkp335

Clough, 1998, Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana, Plant J., 16, 735, 10.1046/j.1365-313x.1998.00343.x

Moradpour, 2017, Evaluation of pEASY-Uni Seamless Cloning and Assembly Kit to clone multiple fragments of Elaeis guineensis DNA, Meta Gene, 14, 134, 10.1016/j.mgene.2017.09.001

Benoit, R.M., Ostermeier, C., Geiser, M., Li, J.S.Z., Widmer, H., and Auer, M. (2016). Seamless insert-plasmid assembly at high efficiency and low cost. PLoS ONE, 11.

Sun, 2007, A simple and effective method for protein subcellular localization using Agrobacterium-mediated transformation of onion epidermal cells, Biologia (Bratisl.), 62, 529, 10.2478/s11756-007-0104-6

Cakmak, 1992, Magnesium deficiency and high light intensity enhance activities of superoxide dismutase, ascorbate peroxidase, and glutathione reductase in bean leaves, Plant Physiol., 98, 1222, 10.1104/pp.98.4.1222

Yu, 1999, Drought and salinity differentially influence activities of superoxide dismutases in narrow-leafed lupins, Plant Sci., 142, 1, 10.1016/S0168-9452(98)00246-5

Giannopolitis, 1977, Superoxide Dismutases: II. purification and quantitative relationship with water-soluble protein in seedlings, Plant Physiol., 59, 315, 10.1104/pp.59.2.315

Sahoo, 2001, Induction of a new isozyme of superoxide dismutase at low temperature in Potentilla astrisanguinea Lodd. variety argyrophylla (Wall. ex. Lehm) Griers, J. Plant Physiol., 158, 1093, 10.1078/0176-1617-00224

Kakkar, 1984, A modified spectrophotometric assay of superoxide dismutase, Indian J. Biochem. Biophys., 21, 130

Tetley, 1974, The metabolism of oat leaves during senescence: I. respiration, carbohydrate metabolism, and the action of cytokinins, Plant Physiol., 54, 294, 10.1104/pp.54.3.294

Heath, 1968, Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation, Arch. Biochem. Biophys., 125, 189, 10.1016/0003-9861(68)90654-1

Singh, 1998, Primer premier: Program for design of degenerate primers from a protein sequence, Biotechniques, 24, 318, 10.2144/98242pf02

Tuteja, 2009, Signaling through G protein coupled receptors, Plant. Signal. Behav., 4, 942, 10.4161/psb.4.10.9530

Mmadi, M., Dossa, K., Wang, L., Zhou, R., Wang, Y., Cisse, N., Sy, M., and Zhang, X. (2017). Functional characterization of the versatile MYB gene family uncovered their important roles in plant development and responses to drought and waterlogging in sesame. Genes (Basel), 8.

Revell, 2008, Phylogenetic signal, evolutionary process, and rate, Syst. Biol., 57, 591, 10.1080/10635150802302427

Zhu, 2004, Influence of silicon supply on chlorophyll content, chlorophyll fluorescence, and antioxidative enzyme activities in tomato plants under salt stress, J. Plant Nutr., 27, 2101, 10.1081/PLN-200034641

Maggio, 2001, Unravelling the functional relationship between root anatomy and stress tolerance, Aust. J. Plant Physiol., 28, 999

Chaves, 2009, Photosynthesis under drought and salt stress: Regulation mechanisms from whole plant to cell, Ann. Bot., 103, 551, 10.1093/aob/mcn125

Farooq, 2006, The use of cell membrane stability (CMS) technique to screen for salt tolerant wheat varieties, J. Plant Physiol., 163, 629, 10.1016/j.jplph.2005.06.006

Huang, 2012, Signal transduction during cold, salt, and drought stresses in plants, Mol. Biol. Rep., 39, 969, 10.1007/s11033-011-0823-1

Munns, 2005, Genes and salt tolerance: Bringing them together, New Phytol., 167, 645, 10.1111/j.1469-8137.2005.01487.x

Vassilatis, 2003, The G protein-coupled receptor repertoires of human and mouse, Proc. Natl. Acad. Sci. USA, 100, 4903, 10.1073/pnas.0230374100

Pech, 2012, RsFA (YbeB) proteins are conserved ribosomal silencing factors, PLoS Genet., 8, 1

Shu, 2012, Effects of salt stress on the structure and function of the photosynthetic apparatus in Cucumis sativus and its protection by exogenous putrescine, Physiol. Plant, 146, 285, 10.1111/j.1399-3054.2012.01623.x

Bagag, 2013, Characterization of hydrophobic peptides in the presence of detergent by photoionization mass spectrometry, PLoS ONE, 8, 1, 10.1371/journal.pone.0079033

Kim, 2016, CsRCI2A and CsRCI2E genes show opposite salt sensitivity reaction due to membrane potential control, Acta Physiol. Plant., 38, 1, 10.1007/s11738-016-2072-3

Yamanaka, 2000, TOM1, an Arabidopsis gene required for efficient multiplication of a tobamovirus, encodes a putative transmembrane protein, Proc. Natl. Acad. Sci. USA, 97, 10107, 10.1073/pnas.170295097

Madhusudhan, 2009, Changes in antioxidant enzymes, hydrogen peroxide, salicylic acid and oxidative stress in compatible and incompatible host-tobamovirus interaction, J. Plant Interact., 4, 157, 10.1080/17429140802419516

Miller, 2010, Reactive oxygen species homeostasis and signalling during drought and salinity stresses, Plant Cell Environ., 33, 453, 10.1111/j.1365-3040.2009.02041.x

Jain, 2001, Ameliorative effects of proline on salt stress-induced lipid peroxidation in cell lines of groundnut (Arachis hypogaea L.), Plant Cell Rep., 20, 463, 10.1007/s002990100353

Chen, X., Lu, X., Shu, N., Wang, D., Wang, S., Wang, J., Guo, L., Guo, X., Fan, W., and Lin, Z. (2017). GhSOS1, a plasma membrane Na+/H+ antiporter gene from upland cotton, enhances salt tolerance in transgenic Arabidopsis thaliana. PLoS ONE, 12.

Shinozaki, 2007, Gene networks involved in drought stress response and tolerance, J. Exp. Bot., 58, 221, 10.1093/jxb/erl164

Chakraborty, 2015, Transcriptome analysis of Arabidopsis GCR1 mutant reveals its roles in stress, hormones, secondary metabolism and phosphate starvation, PLoS ONE, 10, 1, 10.1371/journal.pone.0117819

Pandey, 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, 1616, 10.1105/tpc.020321

Sasaki, 2005, Expression of GCR1, the transcriptional activator of glycolytic enzyme genes in the yeast Saccharomyces cerevisiae, is positively autoregulated by Gcr1p, Yeast, 22, 305, 10.1002/yea.1212

Huie, 1992, Characterization of the DNA-binding activity of GCR1: In vivo evidence for two GCR1-binding sites in the upstream activating sequence of TPI of Saccharomyces cerevisiae, Mol. Cell. Biol., 12, 2690

Boekema, 1996, How does photosystem 2 split water? The structural basis of efficient energy conversion, Trends Biochem. Sci., 21, 44, 10.1016/S0968-0004(96)80177-0

Mozafariyan, 2013, The effects of different sodium Chloride concentrations on the growth and photosynthesis parameters of tomato (Lycopersicum esculentum cv. Foria), Agric. Crop. Sci., 6, 203

Abdullah, 1990, Effect of pre- and post-kinetin treatments on salt tolerance of different potato cultivars growing on saline soils, J. Agron. Crop. Sci., 165, 94, 10.1111/j.1439-037X.1990.tb00839.x

Reddy, 1985, Effect of salinity on protein metabolism in bajara (Pennisetum typhoides S and H) leaves, Indian J. Plant. Physiol., 28, 190

Hashimoto, 2012, Phosphorylation of calcineurin B-like (CBL) calcium sensor proteins by their CBL-interacting protein kinases (CIPKs) is required for full activity of CBL–CIPK complexes toward their target proteins, J. Biol. Chem., 287, 7956, 10.1074/jbc.M111.279331

Kudla, 2009, Plant calcineurin B-like proteins and their interacting protein kinases, Biochim. Biophys. Acta Mol. Cell Res., 1793, 985, 10.1016/j.bbamcr.2008.10.006

Wang, 2007, Overexpression of a putative maize calcineurin B-like protein in Arabidopsis confers salt tolerance, Plant Mol. Biol., 65, 733, 10.1007/s11103-007-9238-8

Pandey, 2004, The calcium sensor calcineurin B-like 9 modulates abscisic acid sensitivity and biosynthesis in Arabidopsis, Plant Cell, 16, 1912, 10.1105/tpc.021311

Pandey, 2015, Calcineurin B-like protein-interacting protein kinase CIPK21 regulates osmotic and salt stress responses in Arabidopsis, Plant Physiol., 169, 780, 10.1104/pp.15.00623

Choi, 2005, Arabidopsis calcium-dependent protein kinase AtCPK32 interacts with ABF4, a transcriptional regulator of abscisic acid-responsive gene expression, and modulates its activity, Plant Physiol., 139, 1750, 10.1104/pp.105.069757

Uno, 2000, Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions, Proc. Natl. Acad. Sci. USA, 97, 11632, 10.1073/pnas.190309197

Msanne, 2011, Characterization of abiotic stress-responsive Arabidopsis thaliana RD29A and RD29B genes and evaluation of transgenes, Planta, 234, 97, 10.1007/s00425-011-1387-y

Virlouvet, 2014, ABA signaling is necessary but not sufficient for RD29B transcriptional memory during successive dehydration stresses in Arabidopsis thaliana, Plant J., 79, 150, 10.1111/tpj.12548

Winicov, 2000, Alfin1 transcription factor overexpression enhances plant root growth under normal and saline conditions and improves salt tolerance in alfalfa, Planta, 210, 416, 10.1007/PL00008150

Pasapula, 2011, Expression of an Arabidopsis vacuolar H+-pyrophosphatase gene (AVP1) in cotton improves drought- and salt tolerance and increases fibre yield in the field conditions, Plant Biotechnol. J., 9, 88, 10.1111/j.1467-7652.2010.00535.x

Zelazny, 1995, Plasma membrane sterols are essential for sensing osmotic changes in the halotolerant alga Dunaliella, Plant Physiol., 109, 1395, 10.1104/pp.109.4.1395

Lee, 2013, Divergences in morphological changes and antioxidant responses in salt-tolerant and salt-sensitive rice seedlings after salt stress, Plant Physiol. Biochem., 70, 325, 10.1016/j.plaphy.2013.05.047

Mitsuya, 2000, Effects of sodium chloride on foliar ultrastructure of sweet potato (Ipomoea batatas Lam.) plantlets grown under light and dark conditions in vitro, J. Plant Physiol., 157, 661, 10.1016/S0176-1617(00)80009-7

Salman, 2012, Multiple self-splicing introns in the 16S rRNA genes of giant sulfur bacteria, Proc. Natl. Acad. Sci. USA, 109, 4203, 10.1073/pnas.1120192109

Urano, 2013, “Round up the usual suspects”: A comment on nonexistent plant G protein-coupled receptors, Plant Physiol., 161, 1097, 10.1104/pp.112.212324