Abstract
Protein phosphorylation/dephosphorylation is a major signalling event induced by abiotic stresses in plants. Sucrose nonfermenting 1-related protein kinase 2 (SnRK2) plays important roles in response to osmotic stress. In the present study, four SnRK2s, TpSnRK2.1/3/7/8, were cloned and characterized from Triticum polonicum L. (dwarf Polish wheat, DPW, AABB). All of these were individually located on 2AL, 1AL, 2AL, and 5BL. Two spliced isoforms of TpSnRK2.8 (TpSnRK2.8a and TpSnRK2.8b) were observed. TpSnRK2.1 and TpSnRK2.3 were classified into the group II; TpSnRK2.7 was classified into the group I; and TpSnRK2.8a/b were classified into the group III. Expression patterns revealed that TpSnRK2.1 responded to cold, NaCl, polyethylene glycol (PEG), and abscisic acid (ABA) in both roots and leaves; TpSnRK2.3 was strongly regulated by cold, NaCl, and ABA in both roots and leaves, and by PEG in roots; TpSnRK2.7 was induced by NaCl and PEG in roots, but was not activated by ABA; and TpSnRK2.8s were significantly activated by cold, NaCl, PEG, and ABA in both roots and leaves. From the above results, we inferred that TpSnRK2.1/3/8 may participate in the responses to environmental stresses in ABA-dependent signal transduction pathway but TpSnRK2.7 is possibly involved in responses to environmental stresses in a non-ABA-dependent manner. They play important roles in specific tissues under different stresses.
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Abbreviations
- AA:
-
amino acid
- ABA:
-
abscisic acid
- AMPKs:
-
AMP-activated protein kinases
- DPW:
-
dwarf Polish wheat
- ORF:
-
open reading frame
- PEG:
-
polyethylene glycol
- qPCR:
-
quantitative PCR
- SnRK:
-
sucrose nonfermenting 1-related protein kinase
- UTR:
-
untranslated region
References
Anderberg, R.J., Walker-Simmons, M.K.: Isolation of a wheat cDNA clone for an abscisic acid-inducible transcript with homology to protein kinase. — Proc. nat. Acad. Sci. USA 89: 10183–10187, 1992.
Boudsocq, M., Barbier-Brygoo, H., Lauriere, C.: Identification of nine SNF1-related protein kinase 2 activated by hyperosmotic and saline stresses in Arabidopsis thaliana. — J. Biol. inorg. Chem. 279: 41758–41766, 2004.
Boudsocq, M., Droillard, M.J., Barbier-Brygoo, H., Lauriere, C.: Different phosphorylation mechanisms are involved in the activation of sucrose non-fermenting 1 related protein kinases 2 by osmotic stresses and abscisic acid. — Plant mol. Biol. 63: 491–503, 2007.
Boudsocq, M., Lauriere, C.: Osmotic signaling in plants. Multiple pathways mediated by emerging kinase families. — Plant Physiol. 138: 1185–1194, 2005.
Burza, A.M., Pekala, I., Sikora, J., Siedlecki, P., Malagocki, P., Bucholc, M., Koper, L., Zielenkiewicz, P., Dadlez, M., Dobrowolska, G.: Nicotiana tabacum osmotic stressactivated stressactivated kinase is regulated by phosphorylation on Ser-154 and Ser - 158 in the kinase activation loop. — J. Biol. inorg. Chem. 281: 34299–34311, 2006.
Cailliatte R., Lapeyre, B., Briat, J.F., Mari, S., Curie, C.: The NRAMP6 metal transporter contributes to cadmium toxicity. — Biochem. J. 422: 217–228, 2009.
Coello, P., Hey, S.J., Halford, N.G.: The sucrose nonfermenting-1-related (SnRK) family of protein kinases: potential for manipulation to improve stress tolerance and increase yield. — J. exp. Bot. 62: 883–893, 2011.
Du, W.M., Lin, H.X., Chen,.S, Wu, Y.S., Zhang, J., Fuglsang, A.T., Palmgren, M.G., Wu, W.H., Guo, Y.: Phosphorylation of SOS3-like calcium-binding proteins by their interacting SOS2-like protein kinases is a common regulatory mechanism in Arabidopsis. — Plant Physiol. 156: 2235–2243, 2011.
Duncan, D.B.: Multiple Range and Multiple F Tests. — Int. Biometric Soc. 11: 1–42, 1955.
Fujii, H., Verslues, P.E., Zhu, J.K.: Identification of two protein kinases required for abscisic acid regulation of seed germination, root growth, and gene expression in Arabidopsis. — Plant Cell 19: 485–494, 2007.
Fujita, M., Fujita, Y., Noutoshi, Y., Takahashi, F., Narusaka, Y., Yamaguchi-Shinozaki, K., Shinozaki, K.: 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: 436–442, 2006.
Fujita, Y., Nakashima, K., Yoshida, T., Katagiri, T., Kidokoro, S., Kanamori, N.: Three SnRK2 protein kinases are the main positive regulators of abscisic acid signaling in response to water stress in Arabidopsis. — Plant Cell Physiol. 50: 2123–2132, 2009.
Fujita, Y., Yoshida, T., Yamaguchi-Shinozaki, K.: Pivotal role of the AREB/ABF-SnRK2 pathway in ABRE-mediated transcription in response to osmotic stress in plants. — Physiol. Plant. 147: 15–27, 2013.
Halford, N.G., Hardie, D.G.: SNF1 - related protein kinases: global regulators of carbon metabolism in plants. — Plant mol. Biol. 37: 735–748, 1998.
Halford, N.G., Hey, S.J.: Snf1-related protein kinases (SnRKs) act within an intricate network that links metabolic and stress signalling in plants. — Biochem. J. 419: 247–259, 2009.
Harmon, A.C.: Calcium-regulated protein kinases of plants. Gravitational and Space. — Biol. Bull. 16: 83–90, 2003.
Holappa, L.D., Walker-Simmons, M.K., Riechers, D.E., Beckles, D.M., Jones, R.L.: A Triticum tauschii protein kinase related to wheat PKABA1 is associated with ABA signaling and is distributed between the nucleus and cytosol. — J. Cereal. Sci. 41: 333–346, 2005.
Hrabak, E.M., Chan, C.W., Gribskov, M., Harper, J.F., Choi, J.H., Halford, N., Kudla, J., Luan, S., Nimmo, H.G., Sussman, M.R., Thomas, M., Walker-Simmoms, K., Zhu, J.K., Harmon, A.C. The Arabidopsis CDPK-SnRK superfamily of protein kinases. — Plant Physiol. 132: 666–680, 2003.
Huai, J., Wang, M., He, J., Zheng, J., Dong, Z., Lu, H., Zhao, J.F., Wang, G.Y.: Cloning and characterization of the SnRK2 gene family from Zea mays. — Plant Cell Rep. 12: 1861–1868, 2008.
Kimura, T., Shibagaki, N., Ohkama-Ohtsu, N., Hayashi, H., Yoneyama, T., Davies, J.P., Fujiware, T.: Arabidopsis SnRK2.3 protein kinase is involved in the regulation of sulfur-responsive gene expression and O-acetyl-L-serine accumulation under limited sulfur supply. — Soil Sci. Plant Nutr. 52: 211–220, 2006.
Kobayashi, Y., Yamamoto, S., Minami, H., Kagaya, Y., Hattori, T.: Differential activation of the rice sucrose nonfermenting1-related protein kinase 2 family by hyperosmotic stress and abscisic acid. — Plant Cell 16: 1163–1177, 2004.
Kobayashi, Y., Murata, M., Minami, H., Yamamoto, S., Kagaya, Y., Hobo, T., Yamamoto, A.A., Hattori, T.: Abscisic acid-activated SnRK2 protein kinases function in the gene-regulation pathway of ABA signal transduction by phosphorylating ABA response element-binding factors. — Plant J. 44: 939–949, 2005.
Kulik, A., Anielska-Mazur, A., Bucholc, M., Koen, E., Szymanska, E., Zmienko, A., Krzywinska, E., Wawer, I., Ruszkowski, F., Figlerowicz, M., Sklodowska, A., Wendehenne, D., Dobrowolska, G.: SnRK2s are involved in cadmium stress response. — Plant Physiol. 60: 868–883, 2012.
Kulik, A., Wawer, I., Krzywinska, E., Bucholc, M., Dobrowolska, G.: SnRK2 protein kinases-Key regulators of plant response to abiotic stresses. — Omics 15: 859–72, 2011.
Li, J., Wang, X.Q., Watson, M.B., Assmann, S.M.: Regulation of abscisic acid-induced stomatal closure and anion channels by guard cell AAPK kinase. — Science 287: 300–303, 2000.
Li, L.B., Zhang, Y.R., Liu, K.C., Ni, Z.F., Fang, Z.J., Sun, Q.X.: Identification and bioinformatics analysis of SnRK2 and CIPK family genes in sorghum. — Agr. Sci China 9: 19–30, 2010.
Lin, H.X., Yang, Y.Q., Quan, R.D., Mendoza, L., Wu, Y.S., Du, W.M., Zhao, S., Schumaker, K.S., Pardo, J.M., Guo, Y. Phosphorylation of SOS3-like calcium binding protein 8 by SOS2-protein kinase stabilizes their protein complex and regulates salt tolerance in Arabidopsis. — Plant Cell 21: 1607–1619, 2009.
Livak, K.J., Schmittgen, T.D.: Analysis of relative gene expression data usingreal-time quantitative PCR and the 2-delta deltaC(T) method. — Methods. 25: 402–408, 2001.
Luan, S., Kudla, J., Rodriguez-Concepcion, M., Yalovsky, S., Gruissem, W.: Calmodulins and calcineurin B-like proteins: calcium sensors for specific signal response coupling in plants. — Plant Physiol. 56: 2235–2243, 2011.
Mao, X., Zhang, H., Tian, S., Chang, X., Jing, R.: TaSnRK2.4, an SNF1-type serine/threonine protein kinase of wheat (Tricitum aestivum L.), confers enhanced multistress tolerance in Arabidopsis. — J. exp. Bot. 61: 683–696, 2010.
McLoughlin, F., Galvan-Ampudia, C.S., Julkowskal, M.M., Caarls, L., Does, D., Laurie`re, L., Munnik, T., Haring, M.A., Testerink, C.: The Snf1-related protein kinases SnRK2.4 and SnRK2.10 are involved in maintenance of root system architecture during salt stress. — Plant J. 72: 436–449, 2012.
Michalcová, V., Dušinský, D., Sabo, M., Beyroutiová, M.A., Hauptvogel, P., Ivanicová, Z., Švec, M.: Taxonomical classification and origin of Kamut wheat. — Plant Syst. Evol. 300: 1749–1757, 2014.
Monks, D.E., Aghoram, K., Courtney, P.D., Dewald, D.B., Dewey, R.E.: Hyperosmotic stress induces the rapid phosphorylation of a soybean phosphatidylinositol transfer protein homolog through activation of the protein kinasesSPK1 and SPK2. — Plant Cell 3: 1205–1219, 2001.
Nakashima, K., Fujita, Y., Kanamori, N., Katagiri, T., Umezawa, T., Kidokoro, S.: Three Arabidopsis SnRK2 protein kinases, SRK2D/SnRK2.2, SRK2E/SnRK2.6/OST1 and SRK2I/SnRK2.3, involved in ABA signaling are essential for the control of seed development and dormancy. — Plant Cell Physiol. 50: 1345–1363, 2009.
Piattoni, C.V., Bustos, D.M., Guerrero, S.A., Iglesias, A.A.: Non-phosphorylating glycerol dehydro-3-phosphate dehydrogenase is phosphorylated in wheat endosperm at serine-404 by an SNF1-related protein kinase allosterically inhibited by ribose-5-phosphate. — Plant Physiol. 156: 1337–1350, 2011.
Polge, C., Thomas, M.: SNF1/AMPK/SnRK1 kinases, global regulators at the heart of energy control. — Trends Plant Sci. 12: 20–28, 2006.
Resh, M.D.: Fatty acylation of proteins: new insights into membrane targeting of myristoylated and palmitoylated proteins. — Biochim. biophys. Acta 1451: 1–16, 1999.
Saha, J., Chatterjee, C., Sengupta, A., Gupta, K., Gupta, B.: Genome-wide analysis and evolutionary study of sucrose non-fermenting 1-related protein kinase 2 (SnRK2) gene family members in Arabidopsis and Oryza. — Comp. Biol. Chem. 49: 59–70, 2014.
Silva, P., Gerós, H.: Regulation by salt of vacuolar H+-ATPase and H+-pyrophosphatase activities and Na+/H+ exchange. — Plant Signal. Behav. 8: 718–726, 2009.
Shukla, V., Mattoo, A.K.: Sucrose non-fermenting 1-related protein kinase 2 (SnRK2): a family of protein kinases involved in hyperosmotic stress signaling. — Physiol. mol. Biol. 14: 91–100, 2008.
Stepien, ´Ł., Mohler, V., Bocianowski, J., Koczyk, G. Assessing genetic diversity of Polish wheat (Triticum aestivum L.) varieties using microsatellite markers. — Genet. Resour. Crop Evol. 54: 1499–1506, 2007.
Tian, S.J., Mao, X.G., Zhang, H.Y., Chen, S.S., Zhai, C.C., Yang, S.M., Jing, R.L.: Cloning and characterization of TaSnRK2.3, a novel SnRK2 gene in common wheat. — J. exp. Bot. 64: 2063–2080, 2013.
Wang, Y., Wang, X.L., Gu, M.X., Kang, H.Y., Zeng, J., Fan, X., Sha, L.N., Zhang, H.Q., Yu, K., Zhou, Y.H.: Cloning and characterization of four novel SnRK2 genes from dwarf Polish wheat (Triticum polonicum L.). — Biol. Plant. 59: 211–219, 2015.
Wang, Y., Wang, C., Zhang, H., Yue, Z., Liu, X., Ji, W.: Genetic analysis of wheat (Triticum aestivum L.) and related species with markers. Genet. Resour. — Crop Evol. 60: 1105–1117, 2013.
Xu, M.R., Huang, L.Y., Zhang, F., Zhu, L.H., Zhou, Y.L., Li, Z.K.: Genome-wide phylogenetic analysis of stressactivated protein kinase genes in rice (OsSAPKs) and expression profiling in response to Xanthomonas oryzae var. oryzicola infection. — Plant mol. Biol. Rep. 31: 877–885, 2013.
Xu, Z.S., Liu, L., Ni, Z.H., Liu, P., Chen, M., Li, L.C., Chen, Y.F., Ma, Y.Z.: W55a encodes a novel protein kinase that is involved in multiple stress responses. — J. integr. Plant Biol. 51: 58–66, 2009.
Yoshida, R., Hobo, T., Ichimura, K., Mizoguchi, T., Takahashi, F., Aronso, J., Ecker, J.A., Shinozaki, K.: ABA-activated SnRK2 protein kinase is required for dehydration stress signaling in Arabidopsis. — Plant Cell Physiol. 143: 1473–1483, 2002.
Zhang, H., Mao, X., Wang, C., Jing, R.: Overexpression of a common wheat gene TaSnRK2.8 enhances tolerance to drought, salt and low temperature in Arabidopsis. — Plos ONE 5: 16–41, 2010.
Zhang, H., Mao, X., Jing, R., Chang, X., Xie, H.: Characterization of a common wheat (Triticum aestivum L.) TaSnRK2.7 gene involvement in abiotic stress responses. — J. exp. Bot. 62: 975–988, 2011.
Zheng, Z.F., Xu, X.P., Crosley, R.A., Greenwalt, S.A., Sun, Y., Blakeslee, B., Wang, L.Z., Ni, W.T., Sopko, M.S., Yao, C.L., Yau, K., Burton, S., Zhuang, M.B., McCaskill, D.G., Gachotte, D., Thompson, M., Greene, T.W.: The protein kinase SnRK2.6 mediates the regulation of sucrose metabolism and plant growth in Arabidopsis. — Plant Physiol. 153: 99–113, 2010.
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Acknowledgments: The authors thank the National Natural Science Foundation of China (Nos. 31671688 and 31470305), the Bureau of Science and Technology, and the Bureau of Education of Sichuan Province, China.
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Jiang, Y., Wang, Y., Huang, Z. et al. Cloning and characterization of four TpSnRK2s from dwarf Polish wheat. Biol Plant 61, 601–610 (2017). https://doi.org/10.1007/s10535-017-0719-6
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DOI: https://doi.org/10.1007/s10535-017-0719-6