OsDMI3 is a novel component of abscisic acid signaling in the induction of antioxidant defense in leaves of rice

Molecular Plant

Volumn 5, Issue 6, 2012, Pages 1359-1374

  Shi, Ben ^a   Ni, Lan ^a   Zhang, Aying ^a   Cao, Jianmei ^a   Zhang, Hong ^a   Qin, Tingting ^a   Tan, Mingpu ^a   Zhang, Jianhua ^b   Jiang, Mingyi ^a  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

^b HONG KONG BAPTIST UNIVERSITY   (Hong Kong)

Author keywords

abscisic acid; antioxidant defense; OsDMI3; oxidative stress; signal transduction

Indexed keywords

EID: 84870502886     PISSN: 16742052     EISSN: 17529867     Source Type: Journal    
DOI: 10.1093/mp/sss068     Document Type: Article

References (69)

1. An, C.I., Sawada, A., Kawaguchi, Y., Fukusaki, E., and Kobayashi, A. (2005). Transient RNAi induction against endogenous genes in Arabidopsis protoplasts using in vitro-prepared double-stranded RNA. Biosci. Biotechnol. Biochem. 69, 415-418. (Pubitemid 40413267)
2. Bart, R., Chern, M., Park, C.J., Bartley, L., and Ronald, P.C. (2006). A novel system for gene silencing using siRNAs in rice leaf and stem-derived protoplasts. Plant Methods. 2, 13.
3. Bouallegue, A., Pandey, N.R., and Srivastava, A.K. (2009). CaMKII knockdown attenuates H2O2-induced phosphorylation of ERK1/2, PKB/Akt and IGF-1R in vascular smooth muscle cells. Free Radic. Biol. Med. 47, 858-866.
4. Bouché, N., Yellin, A., Snedden, W.A., and Fromm, H. (2005). Plant-specific calmodulin-binding proteins. Annu. Rev. Plant Biol. 56, 435-466. (Pubitemid 40802417)
5. Bradford, M.M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
6. Bright, J., Desikan, R., Hancock, J.T., Weir, I.S., and Neill, S.J. (2006). ABA-induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis. Plant J. 45, 113-122. (Pubitemid 43373736)
7. Capoen, W., Herder, J.D., Sun, J., Verplancke, C., Keyser, A.D., Rycke, R.D., Goormachtig, S., Oldroyd, G., and Holsters, M. (2009). Calcium spiking patters and the role of the calcium/ calmodulin-dependent kinase CCaMK in lateral root base nodulation of Sesbania rostrata. Plant Cell. 21, 1526-1540.
8. Chen, C., Ane, J.M., and Zhu, H. (2008). OsIPD3, an ortholog of the Medicago truncatula DMI3 interacting protein IPD3, is required for mycorrhizal symbiosis in rice. New Phytol. 180, 311-315.
9. Chen, C., Gao, M., Liu, J., and Zhu, H. (2007). Fungal symbiosis in rice requires an ortholog of a legume common symbiosis gene encoding a Ca2+/calmodulin-dependent protein kinase. Plant Physiol. 145, 1619-1628. (Pubitemid 350276780)
10. Chen, S., Tao, L., Zeng, L., Vega-Sanchez, M.E., Umemura, K., and Wang, G.L. (2006). A highly efficient transient protoplast system for analyzing defence gene expression and protein-protein interactions in rice. Mol. Plant Pathol. 7, 417-427. (Pubitemid 44337800)
11. Cho, D., Shin, D., Jeon, B.W., and Kwak, J.M. (2009). ROS-mediated ABA signaling. J. Plant Biol. 52, 102-113.
12. Cutler, S.R., Rodriguez, P.L., Finkelstein, R.R., and Abrams, S.R. (2010). Abscisic acid: emergence of a core signaling network. Annu. Rev. Plant Biol. 61, 651-679.
13. Dammann, C., Ichida, A., Hong, B., Romanowsky, S.M., Hrabak, E.M., Harmon, A.C., Pickard, B.G., and Harper, J.F. (2003). Subcellular targeting of nine calcium-dependent protein kinase isoforms from Arabidopsis. Plant Physiol. 132, 1840-1848. (Pubitemid 37024146)
14. DeFalco, T.A., Bender K.W., and Snedden, W.A. (2010). Breaking the code: Ca2+ sensors in plant signaling. Biochem. J. 425, 27-40.
15. Godfroy, O., Debelle, F., Timmers, T., and Rosenberg, C. (2006). A rice calcium- and calmodulin-dependent protein kinase restores nodulation to a legume mutant. Mol. Plant-Microbe Interact. 19, 495-501. (Pubitemid 43668273)
16. Guan, L., Zhao, J., and Scandalios, J.G. (2000). Cis-elements and trans-factors that regulate expression of the maize Cat1 antioxidant gene in response to ABA and osmotic stress: H2O2 is the likely intermediary signaling molecule for the response. Plant J. 22, 87-95. (Pubitemid 30308401)
17. Harper, J.F., Breton, G., and Harmon, A. (2004). Decoding Ca2+ signals through plant protein kinases. Annu. Rev. Plant Biol. 55, 263-288. (Pubitemid 38940933)
18. Hayashi, T., Banba, M., Shimoda, Y., Kouchi, H., Hayashi M., and Imaizumi-Anraku, H. (2010). A dominant function of CCaMK in intracellular accommodation of bacterial and fungal endosymbionts. Plant J. 63, 141-154.
19. Hodges, D.M., DeLong, J.M., Forney, C.F., and Prange, P.K. (1999). Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta. 207, 604-611.
20. Hu, X.L., Jiang, M.Y., Zhang, J.H., Zhang, A.Y., Lin, F., and Tan, M.P. (2007). Calcium/calmodulin is required for abscisic acid-induced antioxidant defense and functions both upstream and downstream of H2O2 production in leaves of maize plants. New Phytol. 173, 27-38. (Pubitemid 44924238)
21. Huang, X.Y., Chao, D.Y., Gao, J.P., Zhu, M.Z., Shi, M., and Lin, H.X. (2009). A previously unknown zinc finger protein, DST, regulates drought and salt tolerance in rice via stomatal aperture control. Genes Dev. 23, 1805-1817.
22. Hubbard, K.E., Nishimura, N., Hitomi K., Getzoff, E.D., and Schroeder, J.I. (2010). Early abscisic acid signal transduction mechanisms: newly discovered components and newly emerging questions. Genes Dev. 24, 1695-1708.
23. Ishida, A., Shigeri Y., Taniguchi, T., and Kameshita, I. (2003). Protein phosphatases that regulate multifunctional Ca2+/ calmodulin-dependent protein kinases: from biochemistry to pharmacology. Pharmacol. Therapeut. 100, 291-305. (Pubitemid 37494910)
24. Jiang, M.Y., and Zhang, J.H. (2001). Effect of abscisic acid on active oxygen species, antioxidative defence system and oxidative damage in leaves of maize seedlings. Plant Cell Physiol. 42, 1265-1273.
25. Jiang, M.Y., and Zhang, J.H. (2002a). Involvement of plasma membrane NADPH oxidase in abscisic acid- and water stress-induced antioxidant defense in leaves of maize seedlings. Planta. 215, 1022-1030.
26. Jiang, M.Y., and Zhang, J.H. (2002b). Role of abscisic acid in water stress-induced antioxidant defense in leaves of maize seedlings. Free Radic. Res. 36, 1001-1015.
27. Jiang, M.Y., and Zhang, J.H. (2002c). Water stress-induced abscisic acid accumulation triggers the increased generation of reactive oxygen species and up-regulates the activities of antioxidant enzymes in maize leaves. J. Exp. Bot. 53, 2401-2410.
28. Jiang, M.Y., and Zhang, J.H. (2003). Cross-talk between calcium and reactive oxygen species originated from NADPH oxidase in abscisic acid-induced antioxidant defense in leaves of maize seedlings. Plant Cell Environ. 26, 929-939.
29. Jiang, M.Y., and Zhang, J.H. (2004). Abscisic acid and antioxidant defense in plant cells. Acta Bot. Sin. 46, 1-9.
30. Joshi-Saha, A., Valon, C., and Leung, J. (2011). Abscisic acid signal off the starting block. Mol. Plant. 4, 562-580.
31. Kalo, P., et al. (2005). Nodulation signaling in legumes requires NSP2, a member of the GRAS family of transcriptional regulators. Science. 308, 1786-1789. (Pubitemid 40848006)
32. Kang, H., Zhu, H., Chu, X., Yang, Z., Yuan, S., Yu, D., Wang, C., Hong, Z., and Zhang, Z. (2011). A novel interaction between CCaMK and a protein containing the Scythe-N ubiquitin-like domain in Lotus japonicus. Plant Physiol. 155, 1312-1324.
33. Kim, M.C., Chung, W.S., Yun, D.-J., and Cho, M.J. (2009). Calcium and calmodulin-mediated regulation of gene expression in plants. Mol. Plant. 2, 13-21.
34. Kwak, J.M., et al. (2003). NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J. 22, 2623-2633. (Pubitemid 36712360)
35. Lecourieux, D., Ranjeva, R., and Pugin, A. (2006). Calcium in plant defence-signaling pathways. New Phytol. 171, 249-269.
36. Levy, A., Erlanger, M., Rosenthal, M., And Epel, B.L. (2007). A plasmodesmata-associated ?-1,3-glucanase in Arabidopsis. Plant J. 49, 669-682.
37. Levy, J., et al. (2004). A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science. 303, 1361-1364. (Pubitemid 38269427)
38. Lin, F., Ding, H.D., Wang, J.X., Zhang, H., Zhang, A.Y., Zhang, Y., Tan, M.P., Dong, W., and Jiang, M.Y. (2009). Positive feedback regulation of maize NADPH oxidase by mitogen- activated protein kinase cascade in abscisic acid signaling. J. Exp. Bot. 60, 3221-3238.
39. Ma, L., Liang, S., Jones, R.L., and Lu, Y.T. (2004). Characterization of a novel calcium/calmodulin-dependent protein kinase from tobacco. Plant Physiol. 135, 1280-1293. (Pubitemid 39009377)
40. Messinese, E., et al. (2007). A novel nuclear protein interacts with the symbiotic DMI3 calcium- and calmodulin-dependent protein kinase of Medicago truncatula. Mol. Plant-Microbe Interact. 20, 912-921. (Pubitemid 47105724)
41. Miller, G., Shulaev, V., and Mittler, R. (2008). Reactive oxygen signaling and abiotic stress. Physiol. Plant. 133, 481-489. (Pubitemid 351841674)
42. Miller, G., Suzuki, N., Ciftci-Yilmaz, S., and Mittler, R. (2010). Reactive oxygen species homeostasis and signaling during drought and salinity stresses. Plant Cell Environ. 33, 453-467.
43. Mitra, R.M., Gleason, C.A., Edwards, A., Hadfield, J., Downie, J.A., Oldroyd, G.E.D., and Long, S.R. (2004). A Ca2+/calmodulindependent protein kinase required for symbiotic nodule development: gene identification by transcript-based cloning. Proc. Natl Acad. Sci. U S A. 101, 4701-4705. (Pubitemid 38437474)
44. Mittler, R., Vanderauwera, S., Suzuki, N., Miller, G., Tognetti, V.B., Vandepoele, K., Gollery, M., Shulaev, V., and Van Breusegem, F. (2011). ROS signaling: the new wave? Trends Plant Sci. 16, 300-309.
45. Neill, S., Barros, R., Bright, J., Desikan, R., Hancock, J., Harrison, J., Morris, P., Ribeiro, D., and Wilson, I. (2008). Nitric oxide, stomatal closure, and abiotic stress. J. Exp. Bot. 59, 165-176. (Pubitemid 351651356)
46. Nguyen, A., Chen, P., and Cai, H. (2004). Role of CaMKII in hydrogen peroxide activation of ERK1/2, p38MAPK, HSP27 and actin reorganization in endothelial cells. FEBS Lett. 572, 307-313. (Pubitemid 39092554)
47. Orozco-Cárdenas, M.L., and Ryan, C. (1999). Hydrogen peroxide is generated systemically in plant leaves by wounding and systemin via the octadecanoid pathway. Proc. Natl Acad. Sci. U S A. 96, 6553-6557. (Pubitemid 29256704)
48. Palomeque, J., Rueda, O.V., Sapia, L., Valverde, C.A., Salas, M., Petroff, M.V., and Mattiazzi, A. (2009). Angiotensin II-induced oxidative stress resets the Ca2+ dependence of Ca2+-calmodulin protein kinase II and promotes a death pathway conserved across different species. Circ. Res. 105, 1204-1212.
49. Patil, S., Takezawa, D., and Poovaiah, B.W. (1995). Chimeric plant calcium/calmodulin-dependent protein kinase gene with a neural visinin-like calcium-binding domain. Proc. Natl Acad. Sci. U S A. 92, 4897-4901.
50. Poovaiah, B., Xia, M., Liu, Z., Wang, W., Yang, T., Sathyanarayanan, P., and Franceschi, V. (1999). Developmental regulation of the gene for chimeric calcium/calmodulin-dependent protein kinase in anthers. Planta. 209, 161-171.
51. Sakamoto, H., Maruyama, K., Sakuma, Y., Meshi, T., Iwabuchi, M., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2004). Arabidopsis Cys2/His2-type zinc-finger proteins function as transcription repressors under drought, cold, and high-salinity stress conditions. Plant Physiol. 136, 2734-2746. (Pubitemid 41071312)
52. Sang, J.R., Zhang, A.Y., Lin, F., Tan, M.P., and Jiang, M.Y. (2008). Cross-talk between calcium-calmodulin and nitric oxide in abscisic acid signaling in leaves of maize plants. Cell Res. 18, 577-588. (Pubitemid 351630943)
53. Seki, M., Umezawa, T., Urano, K., and Shinozaki, K. (2007). Regulatory metabolic networks in drought stress responses. Curr. Opin. Plant Biol. 10, 296-302. (Pubitemid 46710486)
54. Smit, P., Raedts, J., Portyanko, V., Debelle, F., Gough, C., Bisseling, T., and Geurts, R. (2005). NSP1 of the GRAS protein family is essential for rhizobial Nod factor-induced transcription. Science. 308, 1789-1791. (Pubitemid 40848007)
55. Sun, S.J., Guo, S.Q., Yang, X., Bao, Y.M., Tang, H.J., Sun, H., Huang, J., and Zhang, H.S. (2010). Functional analysis of a novel Cys2/ His2-type zinc finger protein involved in salt tolerance in rice. J. Exp. Bot. 61, 2807-2818.
56. Swulius, M.T., and Waxham, M.N. (2008). Ca2+/calmodulin-dependent protein kinases. Cell. Mol. Life Sci. 65, 2637-2657.
57. Tirichine, L., et al. (2006). Deregulation of a Ca2+/calmodulindependent kinase leads to spontaneous nodule development. Nature. 441, 1153-1156. (Pubitemid 43990736)
58. Wang, P., and Song, C.P. (2008). Guard-cell signalling for hydrogen peroxide and abscisic acid. New Phytol. 178, 703-718. (Pubitemid 351670108)
59. Wong, H.L., et al. (2007). Regulation of rice NADPH oxidase by binding of Rac GTPase to its N-terminal extension. Plant Cell. 19, 4022-4034. (Pubitemid 351253117)
60. Yang, C., et al. (2011). Overexpression of a wheat CCaMK gene reduces ABA sensitivity of Arabidopsis thaliana during seed germination and seedling growth. Plant Mol. Biol. Rep. 29, 681-692.
61. Yang, T., and Poovaiah, B.W. (2002). Hydrogen peroxide homeostasis: activation of plant catalase by calcium/calmodulin. Proc. Natl Acad. Sci. U S A. 99, 4097-4102. (Pubitemid 34252235)
62. Yang, T., and Poovaiah, B.W. (2003). Calcium/calmodulin-mediated signal network in plants. Trends Plant Sci. 8, 505-512. (Pubitemid 37325561)
63. Yang, T., Du, L., and Poovaiah, B.W. (2007). Concept of redesigning proteins by manipulating calcium/calmodulin-binding domains to engineer plants with altered traits. Funct. Plant Biol. 34, 343-352. (Pubitemid 46641464)
64. Yano, K., et al. (2008). CYCLOPS, a mediator of symbiotic intracellular accommodation. Proc. Natl Acad. Sci. U S A. 105, 20540-20545.
65. Yoo, S.D., Cho, Y.H., and Sheen, J. (2007). Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat. Protoc. 2, 1565-1572. (Pubitemid 47028844)
66. Zelazny, E., Borst, J.W., Muylaert, M., Batoko, H., Hemminga, M.A., and Chaumont, F. (2007). FRET imaging in living maize cells reveals that plasma membrane aquaporins interact to regulate their subcellular localization. Proc. Natl Acad. Sci. U S A. 104, 12359-12364. (Pubitemid 47206142)
67. Zhai, Z., Sooksa-nguan, T., and Vatamaniuk, O.K. (2009). Establishing RNA interference as a reverse-genetic approach for functional analysis in protoplasts. Plant Physiol. 149, 642-652.
68. Zhang, A.Y., Jiang, M.Y., Zhang, J.H., Tan, M.P., and Hu, X.L. (2006). Mitogen-activated protein kinase is involved in abscisic acid-induced antioxidant defense and acts downstream of reactive oxygen species production in leaves of maize plants. Plant Physiol. 141, 475-487.
69. Zhang, L., and Lu, Y.T. (2003). Calmodulin-binding protein kinases in plants. Trends Plant Sci. 8, 123-127. (Pubitemid 36726468)