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VaCPK21, a calcium-dependent protein kinase gene of wild grapevine Vitis amurensis Rupr., is involved in grape response to salt stress

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Abstract

Ca2+-dependent protein kinases (CDPKs) are known to play important roles in signal transduction in response to various abiotic stresses that limit crop yields. Vitis amurensis is a wild grape species that possesses a high adaptive potential and displays a high resistance to environmental stresses, such as low temperatures or microbial pathogens. The roles of most grape CDPKs in the adaptation to various stresses have not yet been uncovered. A recent CDPK gene expression analysis revealed that expression of VaCPK21 gene was significantly up-regulated under salt stress and, to a less degree, under high mannitol and high temperature stresses in V. amurensis plant cuttings. In this study, the effects of overexpressing the VaCPK21 gene in callus cell lines of V. amurensis and transgenic plants of A. thaliana on their responses to abiotic stresses were investigated. The VaCPK21-overexpressing cell cultures of V. amurensis, soil-grown plants of A. thaliana, and seedlings of A. thaliana exhibited higher tolerance to salt stress in comparison with the controls transformed with the “empty” vector. Heat, cold, and drought stress resistance of the transgenic V. amurensis calli and A. thaliana plants was comparable to that of the controls. Under salt stress conditions, the stress-related genes AtCOR15, AtCOR47, AtCAT1, AtCSD1, AtNHX1, AtKIN1, AtRD26, and AtRD29B demonstrated strong up-regulation in the VaCPK21-transgenic but not in the control Arabidopsis plants. Together, the results indicate that VaCPK21 may act as a positive regulator involved in the grapevine response to salt stress.

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References

  • Aleynova OA, Dubrovina AS, Manyakhin AY, Karetin YA, Kiselev KV (2015) Regulation of resveratrol production in Vitis amurensis cell cultures by calcium-dependent protein kinases. Appl Biochem Biotechnol 175:1460–1476

    Article  CAS  PubMed  Google Scholar 

  • Aleynova-Shumakova OA, Dubrovina AS, Manyakhin AY, Karetin YA, Kiselev KV (2014) VaCPK20 gene overexpression significantly increased resveratrol content and expression of stilbene synthase genes in cell cultures of Vitis amurensis Rupr. Appl Microbiol Biotechnol 98:5541–5549

    Article  CAS  PubMed  Google Scholar 

  • Asano T, Tanaka N, Yang G, Hayashi N, Komatsu S (2005) Genome-wide identification of the rice calcium-dependent protein kinase and its closely related kinase gene families: comprehensive analysis of the CDPKs gene family in rice. Plant Cell Physiol 46:356–366

    Article  CAS  PubMed  Google Scholar 

  • Asano T, Hayashi N, Kobayashi M, Aoki N, Miyao A, Mitsuhara I, Ichikawa H, Komatsu S, Hirochika H, Kikuchi S, Ohsugi R (2012) A rice calcium-dependent protein kinase OsCPK12 oppositely modulates salt stress tolerance and blast disease resistance. Plant J 69:26–36

    Article  CAS  PubMed  Google Scholar 

  • Batistič O, Kudla J (2012) Analysis of calcium signaling pathways in plants. Biochim Biophys Acta 1820(8):1283–1293

    Article  PubMed  Google Scholar 

  • Bekesiova I, Nap JP, Mlynarova L (1999) Isolation of high quality DNA and RNA from leaves of the carnivorous plant Drosera rotundifolia. Plant Mol Biol Rep 17:269–277

    Article  CAS  Google Scholar 

  • Boudsocq M, Sheen J (2013) CDPKs in immune and stress signaling. Trends Plant Sci 18(1):30–40

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chen F, Fasoli M, Tornielli GB, Dal Santo S, Pezzotti M, Zhang L, Cai B, Cheng ZM (2013a) The evolutionary history and diverse physiological roles of the grapevine calcium-dependent protein kinase gene family. PLoS One 8:e80818

    Article  PubMed Central  PubMed  Google Scholar 

  • Chen J, Xue B, Xia X, Yin W (2013b) A novel calcium-dependent protein kinase gene from Populus euphratica, confers both drought and cold stress tolerance. Biochem Biophys Res Commun 441:630–636

    Article  CAS  PubMed  Google Scholar 

  • Cheng SH, Willmann MR, Chen HC, Sheen J (2002) Calcium signaling through protein kinases. The Arabidopsis calcium-dependent protein kinase gene family. Plant Physiol 129:469–485

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Choi HI, Park HJ, Park JH, Kim S, Im MY, Seo HH, Kim YW, Hwang I, Kim SY (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 139:1750–1761

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Das R, Pandey GK (2010) Expressional analysis and role of calcium regulated kinases in abiotic stress signaling. Curr Genomics 11:2–13

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dubrovina AS, Kiselev KV, Khristenko VS (2013) Expression of calcium-dependent protein kinase (CDPK) genes under abiotic stress conditions in wild-growing grapevine Vitis amurensis. J Plant Physiol 170:1491–1500

    Article  CAS  PubMed  Google Scholar 

  • Dubrovina AS, Kiselev KV, Khristenko VS, Aleynova OA (2015) VaCPK20, a calcium-dependent protein kinase gene of wild grapevine Vitis amurensis Rupr., mediates cold and drought stress tolerance. J Plant Physiol 185:1–12

    Article  CAS  PubMed  Google Scholar 

  • Franz S, Ehlert B, Liese A, Kurth J, Cazalé AC, Romeis T (2011) Calcium-dependent protein kinase CPK21 functions in abiotic stress response in Arabidopsis thaliana. Mol Plant 4(1):83–96

    Article  CAS  PubMed  Google Scholar 

  • Fujita M, Fujita Y, Maruyama K, Seki M, Hiratsu K, Ohme-Takagi M, Tran LS, Yamaguchi-Shinozaki K, Shinozaki K (2004) A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signaling pathway. Plant J 39:863–876

  • Geiger D, Scherzer S, Mumm P, Marten I, Ache P, Matschi S, Liese A, Wellmann C, Al-Rasheid KA, Grill E, Romeis T, Hedrich R (2010) Guard cell anion channel SLAC1 is regulated by CDPK protein kinases with distinct Ca2+ affinities. Proc Natl Acad Sci USA 107:8023–8028

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Harshavardhan VT, Van Son L, Seiler C, Junker A, Weigelt-Fischer K, Klukas C, Altmann T, Sreenivasulu N, Bäumlein H, Kuhlmann M (2014) AtRD22 and AtUSPL1, members of the plant-specific BURP domain family involved in Arabidopsis thaliana drought tolerance. PLoS One 9(10):e110065

    Article  PubMed Central  PubMed  Google Scholar 

  • Jaillon O, Aury JM, Noel B, Policriti A, Clepet C, Casagrande A, Choisne N, Aubourg S, Vitulo N, Jubin C et al (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463–467

    Article  CAS  PubMed  Google Scholar 

  • Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat Biotechnol 17:287–291

    Article  CAS  PubMed  Google Scholar 

  • Kiselev KV, Dubrovina AS, Veselova MV, Bulgakov VP, Fedoreyev SA, Zhuravlev YN (2007) The rolB gene-induced overproduction of resveratrol in Vitis amurensis transformed cells. J Biotechnol 128:681–692

    Article  CAS  PubMed  Google Scholar 

  • Kiselev KV, Dubrovina AS, Bulgakov VP (2009) Phenylalanine ammonia-lyase and stilbene synthase gene expression in rolB transgenic cell cultures of Vitis amurensis. Appl Microbiol Biotechnol 82:647–655

    Article  CAS  PubMed  Google Scholar 

  • Kiselev KV, Dubrovina AS, Shumakova OA, Karetin YA, Manyakhin AY (2013) Structure and expression profiling of a novel calcium-dependent protein kinase gene, CDPK3a, in leaves, stems, grapes, and cell cultures of wild-growing grapevine Vitis amurensis Rupr. Plant Cell Rep 32:431–442

    Article  CAS  PubMed  Google Scholar 

  • Kiselev KV, Dubrovina AS, Tyunin AP (2015) The methylation status of plant genomic DNA influences PCR efficiency. J Plant Physiol 175:59–67

    Article  CAS  PubMed  Google Scholar 

  • Kishor P, Hong Z, Miao GH, Hu C, Verma D (1995) Overexpression of [delta]-pyrroline-5-carboxylate synthetase increases proline production and confers osmotolerance in transgenic plants. Plant Physiol 108(4):1387–1394

    PubMed Central  CAS  PubMed  Google Scholar 

  • Klimecka M, Muszyńska G (2007) Structure and functions of plant calcium-dependent protein kinases. Acta Biochim Pol 54:219–233

    CAS  PubMed  Google Scholar 

  • Kobayashi M, Ohura I, Kawakita K, Yokota N, Fujiwara M, Shimamoto K, Doke N, Yoshioka H (2007) Calcium-dependent protein kinases regulate the production of reactive oxygen species by potato NADPH oxidase. Plant Cell 19:1065–1080

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Komatsu S, Yang G, Khan M, Onodera H, Toki S, Yamaguchi M (2007) Overexpression of calcium-dependent protein kinase 13 and calreticulin interacting protein 1 confers cold tolerance on rice plants. Mol Genet Genom 277:713–723

    Article  CAS  Google Scholar 

  • Liese A, Romeis T (2013) Biochemical regulation of in vivo function of plant calcium-dependent protein kinases (CDPK). Biochim Biophys Acta-Mol Cell Res 7:1582–1589

    Article  Google Scholar 

  • Liu L, Li H (2013) Review: research progress in amur grape, Vitis amurensis Rupr. Can J Plant Sci 93:565–575

    Article  Google Scholar 

  • Liu P, Yang GD, Li H, Zheng CC, Wu CA (2010) Overexpression of NHX1 s in transgenic Arabidopsis enhances photoprotection capacity in high salinity and drought conditions. Acta Physiol Plant 32:81–90

    Article  CAS  Google Scholar 

  • Liu D, Li W, Cheng J, Hou L (2014) Expression analysis and functional characterization of a cold-responsive gene COR15A from Arabidopsis thaliana. Acta Physiol Plant 36:2421–2432

    Article  CAS  Google Scholar 

  • Ma SY, Wu WH (2007) AtCPK23 functions in Arabidopsis responses to drought and salt stresses. Plant Mol Biol 65(4):511–518

    Article  CAS  PubMed  Google Scholar 

  • Ma YY, Zhang YL, Shao H, Lu J (2010) Differential physio-biochemical responses to cold stress of cold-tolerant and non-tolerant grapes (Vitis L.) from China. J Agron Crop Sci 196:212–219

    Article  CAS  Google Scholar 

  • Msanne J, Lin J, Stone JM, Awada T (2011) Characterization of abiotic stress-responsive Arabidopsis thaliana RD29A and RD29B genes and evaluation of transgenes. Planta 234:97–107

    Article  CAS  PubMed  Google Scholar 

  • Puhakainen T, Hess MW, Mäkelä P, Svensson J, Heino P, Palva ET (2004) Overexpression of multiple dehydrin genes enhances tolerance to freezing stress in Arabidopsis. Plant Mol Biol 54(5):743–753

    Article  CAS  PubMed  Google Scholar 

  • Ray S, Agarwal P, Arora R, Kapoor S, Tyagi AK (2007) Expression analysis of calcium-dependent protein kinase gene family during reproductive development and abiotic stress conditions in rice (Oryza sativa L. ssp. indica). Mol Genet Genomics 278:493–505

    Article  CAS  PubMed  Google Scholar 

  • Sakuma Y, Maruyama K, Osakabe Y, Qin F, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2006) Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in drought-responsive gene expression. Plant Cell 18:1292–1309

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Schulz P, Herde M, Romeis T (2013) Calcium-dependent protein kinases: hubs in plant stress signaling and development. Plant Physiol 163(2):523–530

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Shah SH, Ali S, Jan SA, Jalal-Ud-Din Ali GM (2015) Piercing and incubation method of in planta transformation producing stable transgenic plants by overexpressing DREB1A gene in tomato (Solanum lycopersicum Mill.). Plant Cell Tissue Organ Cult 120:1139–1157

    Article  CAS  Google Scholar 

  • Shen YY, Duan CQ, Liang XE, Zhang DP (2004) Membrane-associated protein kinase activities in the developing mesocarp of grape berry. J Plant Physiol 161:15–23

    Article  CAS  PubMed  Google Scholar 

  • Surekha C, Kumari KN, Aruna LV, Suneetha G, Arundhati A, Kishor PBK (2014) Expression of the Vigna aconitifolia P5CSF129A gene in transgenic pigeonpea enhances proline accumulation and salt tolerance. Plant Cell Tissue Organ Cult 116:27–36

    Article  CAS  Google Scholar 

  • Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Ann Bot 91(5):503–527

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tzfira T, Tian GW, Lacroix B, Vyas S, Li J, Leitner-Dagan Y, Krichevsky A, Taylor T, Vainstein A, Citovsky V (2005) pSAT vectors: a modular series of plasmids for autofluorescent protein tagging and expression of multiple genes in plants. Plant Mol Biol 57:503–516

    Article  CAS  PubMed  Google Scholar 

  • Valmonte GR, Arthur K, Higgins CM, MacDiarmid RM (2014) Calcium-dependent protein kinases in plants: evolution, expression and function. Plant Cell Physiol 55:551–569

    Article  CAS  PubMed  Google Scholar 

  • Velasco R, Zharkikh A, Troggio M, Cartwright DA, Cestaro A, Pruss D, Pindo M, Fitzgerald LM, Vezzulli S, Reid J et al (2007) A high quality draft consensus sequence of the genome of a heterozygous grapevine variety. PLoS One 2:e1326

    Article  PubMed Central  PubMed  Google Scholar 

  • Verslues PE, Sharma S (2010) Proline metabolism and its implications for plant-environment interaction. Arabidopsis Book 8:e0140

    Article  PubMed Central  PubMed  Google Scholar 

  • Wang H, Datla R, Georges F, Loewen M, Cutler AJ (1995) Promoters from kin1 and cor6.6, two homologous Arabidopsis thaliana genes: transcriptional regulation and gene expression induced by low temperature, ABA, osmoticum and dehydration. Plant Mol Biol 28(4):605–617

    Article  CAS  PubMed  Google Scholar 

  • Wang C, Jing R, Mao X, Chang X, Li A (2011) TaABC1, a member of the activity of bc1 complex protein kinase family from common wheat, confers enhanced tolerance to abiotic stresses in Arabidopsis. J Exp Bot 62:1299–1311

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wang HM, Zhou L, Fu YP, Cheung MY, Wong FL et al (2012) Expression of an apoplast-localized BURP-domain protein from soybean (GmRD22) enhances tolerance towards abiotic stress. Plant Cell Environ 35:1932–1947

    Article  CAS  PubMed  Google Scholar 

  • Weckwerth P, Ehlert B, Romeis T (2015) ZmCPK1, a calcium-independent kinase member of the Zea mays CDPK gene family, functions as a negative regulator in cold stress signalling. Plant Cell Environ 38:544–558

    Article  CAS  PubMed  Google Scholar 

  • Wei S, Hu W, Deng X, Zhang Y, Liu X, Zhao X, Luo Q, Jin Z, Li Y, Zhou S, Sun T, Wang L, Yang G, He G (2014) A rice calcium-dependent protein kinase OsCPK9 positively regulates drought stress tolerance and spikelet fertility. BMC Plant Biol 14:133

    Article  PubMed Central  PubMed  Google Scholar 

  • Wernimont AK, Artz JD, Finerty Lin YH, Amani M, Allali-Hassani A, Senisterra G, Vedadi M, Tempel W, Mackenzie F et al (2010) Structures of apicomplexan calcium-dependent protein kinases reveal mechanism of activation by calcium. Nat Struct Mol Biol 17:596–601

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Xiong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14:S165–S183

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Xiong AS, Jiang HH, Zhuang J, Peng RH, Jin XF, Zhu B, Wang F, Zhang J, Yao QH (2013) Expression and function of a modified AP2/ERF transcription factor from Brassica napus enhances cold tolerance in transgenic Arabidopsis. Mol Biotechnol 53:198–206

    Article  CAS  PubMed  Google Scholar 

  • Yu XC, Li MJ, Gao GF, Feng HZ, Geng XQ, Peng CC, Zhu SY, Wang XJ, Shen YY, Zhang DP (2006) Abscisic acid stimulates a calcium-dependent protein kinase in grape berry. Plant Physiol 140:558–579

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yu XC, Zhu SY, Gao GF, Wang XJ, Zhao R, Zou KQ, Wang XF, Zhang XY, Wu FQ, Peng CC, Zhang DP (2007) Expression of a grape calcium-dependent protein kinase ACPK1 in Arabidopsis thaliana promotes plant growth and confers abscisic acid-hypersensitivity in germination, postgermination growth, and stomatal movement. Plant Mol Biol 64:531–538

    Article  CAS  PubMed  Google Scholar 

  • Yue Y, Zhang M, Zhang J, Duan L, Li Z (2012) SOS1 gene overexpression increased salt tolerance in transgenic tobacco by maintaining a higher K(+)/Na(+) ratio. J Plant Physiol 169(3):255–261

    Article  CAS  PubMed  Google Scholar 

  • Zhang XR, Henriques R, Lin SS, Niu QW, Chua NH (2006) Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method. Nat Protoc 1:641–646

    Article  CAS  PubMed  Google Scholar 

  • Zhang K, Han YT, Zhao FL, Hu Y, Gao YR, Ma YF, Zheng Y, Wang YJ, Wen YQ (2015) Genome-wide identification and expression analysis of the CDPK gene family in grape, Vitis spp. BMC Plant Biol 15:164

    Article  PubMed Central  PubMed  Google Scholar 

  • Zhao J, Gao Y, Zhang Z, Chen T, Guo W, Zhang T (2013) A receptor-like kinase gene (GbRLK) from Gossypium barbadense enhances salinity and drought-stress tolerance in Arabidopsis. BMC Plant Biol 13:110

    Article  PubMed Central  PubMed  Google Scholar 

  • Zou JJ, Wei FJ, Wang C, Wu JJ, Ratnasekera D, Liu WX, Wu WH (2010) Arabidopsis calcium-dependent protein kinase CPK10 functions in abscisic acid- and Ca2+-mediated stomatal regulation in response to drought stress. Plant Physiol 154:1232–1243

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zuo R, Hu R, Chai G, Xu M, Qi G, Kong Y, Zhou G (2013) Genome-wide identification, classification, and expression analysis of CDPK and its closely related gene families in poplar (Populus trichocarpa). Mol Biol Rep 40(3):2645–2662

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by Grants from the following institutions and foundations: the Russian Science Foundation (14-14-00366) and the Dynasty Foundation (DP-B-09/14). The Russian Science Foundation supported binary vector construction, grape cell culture transformations, and selection of the transgenic calli; the Dynasty Foundation supported abiotic stress tolerance assays, transformations of Arabidopsis, and selection of the transgenic plants.

Author contributions

A.S. Dubrovina carried out a considerable part of the experiments, analyzed the data, and wrote the paper. K.V. Kiselev was involved in the experimental process, data analysis, and in the discussion of the obtained results. V.S. Khristenko and O.A. Aleynova participated in the experimental work.

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Authors and Affiliations

  1. Laboratory of Biotechnology, Institute of Biology and Soil Science, Far Eastern Branch of the Russian Academy of Sciences, Vladivostok, Russia, 690022

    Alexandra S. Dubrovina, Konstantin V. Kiselev, Valeriya S. Khristenko & Olga A. Aleynova

  2. Department of Biochemistry, Microbiology and Biotechnology, Far Eastern Federal University, Vladivostok, Russia, 690090

    Konstantin V. Kiselev & Valeriya S. Khristenko

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  1. Alexandra S. Dubrovina
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  2. Konstantin V. Kiselev
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  3. Valeriya S. Khristenko
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  4. Olga A. Aleynova
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Correspondence to Alexandra S. Dubrovina.

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Dubrovina, A.S., Kiselev, K.V., Khristenko, V.S. et al. VaCPK21, a calcium-dependent protein kinase gene of wild grapevine Vitis amurensis Rupr., is involved in grape response to salt stress. Plant Cell Tiss Organ Cult 124, 137–150 (2016). https://doi.org/10.1007/s11240-015-0882-4

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