A rice calcium-dependent protein kinase OsCPK9 positively regulates drought stress tolerance and spikelet fertility
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- 作者：Shuya Wei (12)
Wei Hu (12) (13)
Xiaomin Deng (12) (13)
Yingying Zhang (12)
Xiaodong Liu (12)
Xudong Zhao (12)
Qingchen Luo (12)
Zhengyi Jin (12)
Yin Li (12)
Shiyi Zhou (12)
Tao Sun (12)
Lianzhe Wang (12)
Guangxiao Yang (12)
Guangyuan He (12)
12. The Genetic Engineering International Cooperation Base of Chinese Ministry of Science and Technology ; Key Laboratory of Molecular Biophysics of Chinese Ministry of Education ; College of Life Science and Technology ; Huazhong University of Science & Technology ; Wuhan ; 430074 ; China
13. Institute of Tropical Bioscience and Biotechnology ; Chinese Academy of Tropical Agricultural Sciences ; Haikou ; 571101 ; China - 关键词：Abscisic acid (ABA) signaling ; Abiotic stresses ; Calcium ; dependent protein kinase (CDPK) ; Drought stress tolerance ; Rice ; Spikelet fertility
- 刊名：BMC Plant Biology
- 出版年：2014
- 出版时间：December 2014
- 年：2014
- 卷：14
- 期：1
- 全文大小：1,879 KB
- 参考文献：1. Asano, T, Hayashi, N, Kikuchi, S, Ohsugi, R (2012) CDPK-mediated abiotic stress signaling. Plant Signal Behav 7: pp. 817-821 CrossRef
2. Ludwig, AA, Romeis, T, Jones, JDG (2004) CDPK-mediated signaling pathways: specificity and cross-talk. J Exp Bot 55: pp. 181-188 CrossRef
3. Harper, JF, Harmon, A (2005) Plants, symbiosis and parasites: a calcium signalling connection. Nat Rev Mol Cell Biol 6: pp. 555-566 CrossRef
4. Harper, JF, Breton, G, Harmon, A (2004) Decoding Ca2+ signals through plant protein kinases. Annu Rev Plant Biol 55: pp. 263-288 CrossRef
5. Harmon, AC, Gribskov, M, Harper, JF (2000) CDPKs-a kinase for every Ca2+ signal?. Trends Plant Sci 5: pp. 154-159 CrossRef
6. Bohmer, M, Romeis, T (2007) A chemical-genetic approach to elucidate protein kinase function in planta. Plant Mol Biol 65: pp. 817-827 CrossRef
7. Schulz, P, Herde, M, Romeis, T (2013) Calcium-dependent protein kinases: hubs in plant stress signaling and development. Plant Physiol 163: pp. 523-530 CrossRef
8. 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: pp. 469-485 CrossRef
9. Hrabak, EM, Chan, CW, Gribskov, M, Harper, JF, Choi, JH, Halford, N, Kudla, J, Luan, S, Nimmo, HG, Sussman, MR, Thomas, M, Walker-Simmons, K, Zhu, JK, Harmon, AC (2003) The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiol 132: pp. 666-680 CrossRef
10. Zhu, SY, Yu, XC, Wang, XJ, Zhao, R, Li, Y, Fan, RC, Shang, Y, Du, SY, Wang, XF, Wu, FQ, Xu, YH, Zhang, XY, Zhang, DP (2007) Two calcium-dependent protein kinases, CPK4 and CPK11, regulate abscisic acid signal transduction in Arabidopsis. Plant Cell 19: pp. 3019-3036 CrossRef
11. Xu, J, Tian, YS, Peng, RH, Xiong, AS, Zhu, B, Jin, XF, Gao, F, Fu, XY, Hou, XL, Yao, QH (2010) AtCPK6, a functionally redundant and positive regulator involved in salt/drought stress tolerance in Arabidopsis. Planta 231: pp. 1251-1260 CrossRef
12. Mehlmer, N, Wurzinger, B, Stael, S, Hofmann-Rodrigues, D, Csaszar, E, Pfister, B, Bayer, R, Teige, M (2010) The Ca2+-dependent protein kinase CPK3 is required for MAPK-independent salt-stress acclimation in Arabidopsis. Plant J 63: pp. 484-498 CrossRef
13. Mori, IC, Murata, Y, Yang, YZ, Munemasa, S, Wang, YF, Andreoli, S, Tiriac, H, Alonso, JM, Harper, JF, Ecker, JR, Kwak, JM, Schroeder, JI (2006) CDPKs CPK6 and CPK3 function in ABA regulation of guard cell S-type anion- and Ca2+-permeable channels and stomatal closure. PLoS Biol 4: pp. 1749-1762 CrossRef
14. Brandt, B, Brodsky, DE, Xue, SW, Negi, J, Iba, K, Kangasj盲rvi, J, Ghassemian, M, Stephan, AB, Hu, HH, Schroeder, JI (2012) Reconstitution of abscisic acid activation of SLAC1 anion channel by CPK6 and OST1 kinases and branched ABI1 PP2C phosphatase action. Proc Natl Acad Sci USA 109: pp. 10593-10598 CrossRef
15. Scherzer, S, Maierhofer, T, Al-Rasheid, KA, Geiger, D, Hedrich, R (2012) Multiple calcium-dependent kinases modulate ABA-activated guard cell anion channels. Mol Plant 5: pp. 1409-1412 CrossRef
16. 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, andmodulates its activity. Plant Physiol 139: pp. 1750-1761 CrossRef
17. 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: pp. 1232-1243 CrossRef
18. Ma, SY, Wu, WH (2007) AtCPK23 functions in Arabidopsis responses to drought and salt stresses. Plant Mol Biol 65: pp. 511-518 CrossRef
19. Franz, S, Ehlert, B, Liese, A, Kurth, J, Cazale, AC, Romeis, T (2011) Calcium-dependent protein kinase CPK21 functions in abiotic stress response in Arabidopsis thaliana. Mol Plant 4: pp. 83-96 CrossRef
20. 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: pp. 8023-8028 CrossRef
21. Zhao, R, Sun, HL, Mei, C, Wang, XJ, Yan, L, Liu, R, Zhang, XF, Wang, XF, Zhang, DP (2011) The Arabidopsis Ca2+-dependent protein kinase CPK12 negatively regulates abscisic acid signaling in seed germination and post-germination growth. New Phytol 192: pp. 61-73 CrossRef
22. Asano, T, Tanaka, N, Yang, GX, 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: pp. 356-366 CrossRef
23. 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: pp. 493-505 CrossRef
24. Saijo, Y, Hata, S, Kyozuka, J, Shimamoto, K, Izui, K (2000) Over-expression of a single Ca2+-dependent protein kinase confers both cold and salt/drought tolerance on rice plants. Plant J 23: pp. 319-327 CrossRef
25. Asano, T, Hakata, M, Nakamura, H, Aoki, N, Komatsu, S, Ichikawa, H, Hirochika, H, Ohsugi, R (2011) Functional characterisation of OsCPK21, a calcium-dependent protein kinase that confers salt tolerance in rice. Plant Mol Biol 75: pp. 179-191 CrossRef
26. Asano, T, Hayashi, N, Kobayashi, M (2012) A rice calcium-dependent protein kinase OsCPK12 oppositely modulates salt-stress tolerance and blast disease resistance. Plant Journal 69: pp. 26-36 CrossRef
27. Asano, T, Kunieda, N, Omura, Y, Ibe, H, Kawasaki, T, Takano, M, Sato, M, Furuhashi, H, Mujin, T, Takaiwa, F, Wu, CY, Tada, Y, Satozawa, T, Sakamoto, M, Shimada, H (2002) Rice SPK, a calmodulin-like domain protein kinase, is required for storage product accumulation during seed development: phosphorylation of sucrose synthase is a possible factor. Plant Cell 14: pp. 619-628 CrossRef
28. Ho, SL, Huang, LF, Lu, CA, He, SL, Wang, CC, Yu, SP, Chen, J, Yu, SM (2013) Sugar starvation- and GA-inducible calcium-dependent protein kinase 1 feedback regulates GA biosynthesis and activates a 14-3-3 protein to confer drought tolerance in rice seedlings. Plant Mol Biol 81: pp. 347-361 CrossRef
29. Matsui, T, Omasa, K, Horie, T (2000) High temperature at flowering inhibit swelling of pollen grains, a driving force for thecae dehiscence in rice (Oryza sativa L.). Plant Prod Sci 3: pp. 430-434 CrossRef
30. Matsui, T, Omasa, K, Horie, T (2001) The difference in sterility due to high temperatures during the flowering period among japonica rice varieties. Plant Prod Sci 4: pp. 90-93 CrossRef
31. Prasad, PVV, Boote, KJ, Allen, LH, Sheehy, JE, Thomas, JMG (2006) Species, ecotype and cultivar differences in spikelet fertility and harvest index of rice in response to high temperature stress. Field Crop Res 95: pp. 398-411 CrossRef
32. Mundy, J, Chua, NH (1988) Abscisic acid and water-stress induce the expression of a novel rice gene. EMBO J 7: pp. 2279-2286
33. Moons, A, de Keyser, A, van Montagu, M (1997) A group 3 LEA cDNA of rice, responsive to abscisic acid, but not to jasmonic acid, shows variety-specific differences in salt stress response. Gene 191: pp. 197-204 CrossRef
34. Igarashi, Y, Yoshiba, Y, Sanada, Y, Yamaguchi-Shinozaki, K, Wada, K, Shinozaki, K (1997) Characterization of the gene for 鈻?-pyrroline-5-carboxylate synthetase and correlation between the expression of the gene and salt tolerance in Oryza sativa L. Plant Mol Biol 33: pp. 857-865 CrossRef
35. Ohnishi, T, Sugahara, S, Yamada, T, Kikuchi, K, Yoshiba, Y, Hirano, Y, Tsutsumi, N (2005) OsNAC6, a member of the NAC gene family, is induced by various stresses in rice. Genes Genet Syst 80: pp. 135-139 CrossRef
36. Nakashima, K, Tran, LSP, van Nguyen, D, Fujita, M, Maruyama, K, Todaka, D, Ito, Y, Hayashi, N, Shinozaki, K, Yamaguchi-Shinozaki, K (2007) Functional analysis of a NAC-type transcription factor OsNAC6 involved in abiotic and biotic stress-responsive gene expression in rice. Plant J 51: pp. 617-630 CrossRef
37. Zheng, XN, Chen, B, Lu, GJ, Han, B (2009) Overexpression of a NAC transcription factor enhances rice drought and salt tolerance. Biochem Biophys Res Commun 379: pp. 985-989 CrossRef
38. Redillas, MC, Jeong, JS, Kim, YS, Jung, H, Bang, SW, Choi, YD, Ha, SH, Reuzeau, C, Kim, JK (2012) The overexpression of OsNAC9 alters the root architecture of rice plants enhancing drought resistance and grain yield under field conditions. Plant Biotechnol J 10: pp. 792-805 CrossRef
39. Hobo, T, Kowyama, Y, Hattori, T (1999) A bZIP factor, TRAB1, interacts with VP1 and mediates abscisic acid-induced transcription. Proc Natl Acad Sci USA 96: pp. 15348-15353 CrossRef
40. Xiang, Y, Tang, N, Du, H, Ye, HY, Xiong, LZ (2008) Characterization of OsbZIP23 as a key player of the basic leucine zipper transcription factor family for conferring abscisic acid sensitivity and salinity and drought tolerance in rice. Plant Physiol 148: pp. 1938-1952 CrossRef
41. Lu, GJ, Gao, CX, Zheng, XN, Han, B (2009) Identification of OsbZIP72 as a positive regulator of ABA response and drought tolerance in rice. Planta 229: pp. 605-615 CrossRef
42. Zhang, L, Xiao, SS, Li, WQ, Feng, W, Li, J, Wu, ZD, Gao, XW, Liu, FQ, Shao, M (2011) Overexpression of a Harpin-encoding gene hrf1 in rice enhances drought tolerance. J Exp Bot 62: pp. 4229-4238 CrossRef
43. You, J, Zong, W, Li, XK, Ning, J, Hu, HH, Li, XH, Xiao, JH, Xiong, LZ (2013) The SNAC1-targeted gene OsSRO1c modulates stomatal closure and oxidative stress tolerance by regulating hydrogen peroxide in rice. J Exp Bot 64: pp. 569-583 CrossRef
44. Jiang, SS, Zhang, D, Wang, L, Pan, JW, Liu, Y, Kong, XP, Zhou, Y, Li, DQ (2013) A maize calcium-dependent protein kinase gene, ZmCPK4, positively regulated abscisic acid signaling and enhanced drought stress tolerance in transgenic Arabidopsis. Plant Physiol Biochem 71: pp. 112-120 CrossRef
45. 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: pp. 1387-1394
46. Duan, JL, Cai, WM (2012) OsLEA3-2, an abiotic stress induced gene of rice plays a key role in salt and drought tolerance. PLoS One 7: pp. e45117 CrossRef
47. Estruch, JJ, Kadwell, S, Merlin, E, Crossland, L (1994) Cloning and characterization of a maize pollen-specific calcium-dependent calmodulin-independent protein kinase (pollen germination/protein phosphorylation). Proc Natl Acad Sci USA 91: pp. 8837-8841 CrossRef
48. Yoon, GM, Dowd, PE, Gilroy, S, McCubbin, AG (2006) Calcium-dependent protein kinase isoforms in Petunia have distinct functions in pollen tube growth, including regulating polarity. Plant Cell 18: pp. 867-878 CrossRef
49. Zhou, S, Wang, Y, Li, W, Zhao, Z, Ren, Y, Wang, Y, Gu, S, Lin, Q, Wang, D, Jiang, L, Su, N, Zhang, X, Liu, L, Cheng, Z, Lei, C, Wang, J, Guo, X, Wu, F, Ikehashi, H, Wang, H, Wan, J (2011) Pollen semi-sterility1 encodes a kinesin-1-like protein important for male meiosis, anther dehiscence, and fertility in rice. Plant Cell 23: pp. 111-129 CrossRef
50. Pressman, E, Shaked, R, Shen, S, Altahan, L, Firon, N (2012) Variations in carbohydrate content and sucrose-metabolizing enzymes in tomato (Solanum lycopersicum L.) stamen parts during pollen maturation. Am J Plant Sci 3: pp. 252-260 CrossRef
51. Datta, R, Chamusco, KC, Chourey, PS (2002) Starch biosynthesis during pollen maturation is associated with altered patterns of gene expression in maize. Plant Physiol 130: pp. 1645-1656 CrossRef
52. Kong, J, Li, Z, Tan, YP, Wan, CX, Li, SQ, Zhu, YG (2007) Different gene expression patterns of sucrose-starch metabolism during pollen maturation in cytoplasmic male-sterile and male-fertile lines of rice. Physiol Plant 130: pp. 136-147 CrossRef
53. Finkelstein, RR, Gampala, SS, Rock, CD (2002) Abscisic acid signaling in seeds and seedlings. Plant Cell 14: pp. S15-S45
54. Zhu, JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53: pp. 247-273 CrossRef
55. Kagaya, Y, Hobo, T, Murata, M, Ban, A, Hattori, T (2002) Abscisic acid-induced transcription is mediated by phosphorylation of an abscisic acid response element binding factor, TRAB1. Plant Cell 14: pp. 3177-3189 CrossRef
56. Kobayashi, Y, Murata, M, Minami, H, Yamamoto, S, Kagaya, Y, Hobo, T, Yamamoto, A, Hattori, T (2005) 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: pp. 939-949 CrossRef
57. Choi, H, Hong, J, Ha, J, Kang, J, Kim, SY (2000) ABFs, a family of ABA-responsive element binding factors. J Biol Chem 275: pp. 1723-1730 CrossRef
58. Uno, Y, Furihata, T, Abe, H, Yoshida, R, Shinozaki, K, Yamaguchi-Shinozaki, K (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: pp. 11632-11637 CrossRef
59. Yamaguchi-Shinozaki, K, Shinozaki, K (2005) Organization of cis-acting regulatory elements in osmotic- and cold-stress-responsive promoters. Trends Plant Sci 10: pp. 88-94 CrossRef
60. Raghavendra, AS, Gonugunta, VK, Christmann, A, Grill, E (2010) ABA perception and signalling. Trends Plant Sci 15: pp. 395-401 CrossRef
61. Xu, M, Zhu, L, Shou, HX, Wu, P (2005) A PIN1 family gene, OsPIN1, involved in auxin-dependent adventitious root emergence and tillering in rice. Plant Cell Physiol 46: pp. 1674-1681 CrossRef
62. Livak, KJ, Schmittgen, TD (2001) Analysis of relative gene expression data using real-time Quantitative PCR and the 2鈥撐斘擟t method. Methods 25: pp. 402-408 CrossRef
63. Toki, S, Hara, N, Ono, K, Onodera, H, Tagiri, A, Oka, S, Tanaka, H (2006) Early infection of scutellum tissue with Agrobacterium allows high-speed transformation of rice. Plant J 47: pp. 969-976 CrossRef
64. Hu, W, Huang, C, Deng, XM, Zhou, SY, Chen, LH, Li, Y, Wang, C, Ma, ZB, Yuan, QQ, Wang, Y, Cai, R, Liang, XY, Yang, GX, He, GY (2013) TaASR1, a transcription factor gene in wheat, confers drought stress tolerance in transgenic tobacco. Plant Cell Environ 36: pp. 1449-1464 CrossRef
65. Troll, W, Lindsley, J (1955) A photometric method for the determination of proline. J Biol Chem 215: pp. 655-660
66. Dubois, M, Gilles, KA, Hamilton, JK, Rebers, PA, Smith, F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28: pp. 350-356 CrossRef
67. Yang, Q, Chen, ZZ, Zhou, XF, Yin, HB, Li, X, Xin, XF, Hong, XH, Zhu, JK, Gong, ZZ (2009) Overexpression of SOS (Salt Overly Sensitive) genes increases salt tolerance in transgenic Arabidopsis. Mol Plant 2: pp. 22-31 CrossRef
68. Heath, RL, Packer, L (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125: pp. 189-198 CrossRef
69. Zou, MJ, Guan, YC, Ren, HB, Zhang, F, Chen, F (2008) A bZIP transcription factor, OsABI5, is involved in rice fertility and stress tolerance. Plant Mol Biol 66: pp. 675-683 CrossRef - 刊物主题：Plant Sciences; Agriculture; Tree Biology;
- 出版者：BioMed Central
- ISSN：1471-2229
文摘
Background In plants, calcium-dependent protein kinases (CDPKs) are involved in tolerance to abiotic stresses and in plant seed development. However, the functions of only a few rice CDPKs have been clarified. At present, it is unclear whether CDPKs also play a role in regulating spikelet fertility. Results We cloned and characterized the rice CDPK gene, OsCPK9. OsCPK9 transcription was induced by abscisic acid (ABA), PEG6000, and NaCl treatments. The results of OsCPK9 overexpression (OsCPK9-OX) and OsCPK9 RNA interference (OsCPK9-RNAi) analyses revealed that OsCPK9 plays a positive role in drought stress tolerance and spikelet fertility. Physiological analyses revealed that OsCPK9 improves drought stress tolerance by enhancing stomatal closure and by improving the osmotic adjustment ability of the plant. It also improves pollen viability, thereby increasing spikelet fertility. In OsCPK9-OX plants, shoot and root elongation showed enhanced sensitivity to ABA, compared with that of wild-type. Overexpression and RNA interference of OsCPK9 affected the transcript levels of ABA- and stress-responsive genes. Conclusions Our results demonstrated that OsCPK9 is a positive regulator of abiotic stress tolerance, spikelet fertility, and ABA sensitivity.