A novel rice C2H2-type zinc finger protein, ZFP36, is a key player involved in abscisic acid-induced antioxidant defence and oxidative stress tolerance in rice

Journal of Experimental Botany

Volumn 65, Issue 20, 2014, Pages 5795-5809

  Zhang, Hong ^a   Liu, Yanpei ^a   Wen, Feng ^a   Yao, Dongmei ^a   Wang, Lu ^a   Guo, Jin ^a   Ni, Lan ^a   Zhang, Aying ^a   Tan, Mingpu ^a   Jiang, Mingyi ^a  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

Author keywords

Abscisic acid (ABA); antioxidant defence; C2H2 type zinc finger protein; oxidative stress; rice; water stress

Indexed keywords

ABSCISIC ACID; ANTIOXIDANT; ASCORBATE PEROXIDASE; HYDROGEN PEROXIDE; MITOGEN ACTIVATED PROTEIN KINASE; SUPEROXIDE DISMUTASE; VEGETABLE PROTEIN; ZINC FINGER PROTEIN;

ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; OXIDATIVE STRESS; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT LEAF; RICE; SIGNAL TRANSDUCTION; TRANSGENIC PLANT; UPREGULATION;

ABSCISIC ACID; ANTIOXIDANTS; ASCORBATE PEROXIDASES; GENE EXPRESSION REGULATION, PLANT; HYDROGEN PEROXIDE; MITOGEN-ACTIVATED PROTEIN KINASES; ORYZA SATIVA; OXIDATIVE STRESS; PLANT LEAVES; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; SUPEROXIDE DISMUTASE; UP-REGULATION; ZINC FINGERS;

EID: 84913554208     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/eru313     Document Type: Article

References (63)

1. Agarwal P, Arora R, Ray S, Singh AK, Singh VP, Takatsuji H, Kapoor S, Tyagi AK. 2007. Genome-wide identification of C2H2 zinc-finger gene family in rice and their phylogeny and expression analysis. Plant Molecular Biology 65, 467-485.
2. Bright J, Desikan R, Hancock JT, Weir IS, Neill SJ. 2006. ABAinduced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis. The Plant Journal 45, 113-122.
3. Cao JM, Yao DM, Lin F, Jiang MY. 2014. PEG-mediated transient gene expression and silencing system in maize mesophyll protoplasts: a valuable tool for signal transduction study in maize. Acta Physiologiae Plantarum 36, 1271-1281.
4. Ciftci-Yilmaz S, Mittler R. 2008. The zinc finger network of plants. Cellular and Molecular Life Sciences 65, 1150-1160.
5. Ciftci-Yilmaz S, Morsy MR, Song L, Coutu A, Krizek BA, Lewis MW, Warren D, Cushman J, Conn olly EL, Mittler R. 2007. The EAR-motif of the Cys2/His2-type zinc finger protein Zat7 plays a key role in the defense response of Arabidopsis to salinity stress. Journal of Biological Chemistry 282, 9260-9268.
6. Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR. 2010. Abscisic acid: emergence of a core signaling network. Annual Review of Plant Biology 61, 651-679.
7. Davletova S, Rizhsky L, Liang H, Shengqiang Z, Oliver DJ, Coutu J, Shulaev V, Schlauch K, Mittler R. 2005 a . Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. The Plant Cell 17, 268-281.
8. Davletova S, Schlauch K, Coutu J, Mittler R. 2005b . The zinc-finger protein Zat12 plays a central role in reactive oxygen and abiotic stress signaling in Arabidopsis. Plant Physiology 139, 847-856.
9. Ding YF, Cao JM, Ni L, Zhu Y, Zhang AY, Tan MP, Jiang MY. 2013. ZmCPK11 is involved in abscisic acid-induced antioxidant defense and functions upstream of ZmMPK5 in the abscisic acid signaling in maize. Journal of Exp erimental Botany 64, 871-884.
10. Fujita Y, Fujita M, Shinozaki K, Yamaguchi-Shinozaki K. 2011. ABAmediated transcriptional regulation in response to osmotic stress in plants. Journal of Plant Research 124 , 509-525.
11. Gao H, Song A, Zhu X, et al. 2012. The heterologous expression in Arabidopsis of a chrysanthemum Cys2/His2 zinc finger protein ge ne confers salinity and drought tolerance. Planta 235, 979-993.
12. Golldack D, Luking I, Yang O. 2011. Plant tolerance to drought and salinity: stress regulating transcription factors and their functional significance in the cellular transcriptional network. Plant Cell Reports 30, 13 83-1391.
13. Hiei Y, Ohta S, Komari T, Kumashiro T. 1994. Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. The Plant Journal 6, 271-282.
14. Hodges DM, DeLong JM, Forney CF, Prange PK. 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.
15. Huang J, Sun S, Xu D, Lan H, Sun H, Wang Z, Bao Y, Wang J, Tang H, Zhang H. 2012. A TFIIIA-type zinc finger protein confers multiple abiotic stre ss tolerances in transgenic rice (Oryza sativa L.). Plant Molecular Biology 80, 337-350.
16. Huang J, Sun SJ, Xu DQ, Yang X, Bao YM, Wang ZF, Tang HJ, Zhang HS. 2009. Increased tolerance of rice to cold, drought and oxidative stresses mediated by the overexpression of a gene that encodes the zinc finger protein ZFP245. Biochemical and Biophysical Research Communications 389, 556-561.
17. Huang J, Yang X, Wang M M, Tang HJ, Ding LY, Shen Y, Zhang HS. 2007. A novel rice C2H2-type zinc finger protein lacking DLN-box/EARmotif plays a role in salt tolerance. Biochimica et Biophysica Acta 1769, 220-227.
18. Huang XY , Chao DY, Gao JP, Zhu MZ, Shi M, Lin HX. 2009. A previously unknown zinc finger protein, DST, regulates drought and salt tolerance in rice via stomatal aperture control. Genes and Development 23, 1805-1817.
19. Hubbard KE, Nishimura N, Hitomi K, Getzoff ED, Schroeder JI. 2010. Early abscisic acid signal transduction mechanisms: newly discovered components and newly emerging questions. Genes and Development 24, 1 695-1708.
20. Iida A, Kazuoka T, Torikai S, Kikuchi H, Oeda K. 2000. A zinc finger protein RHL41 mediates the light acclimation response in Arabidopsis. The Plant Journal 24, 191-203.
21. Ja in D, Roy N, Chattopadhyay D. 2009. CaZF, a plant transcription factor functions through and parallel to HOG and calcineurin pathways in Saccharomyces cerevisiae to provide osmotolerance. PLoS One 4, e5154.
22. Jiang M, Zhang J. 2001. Effect of abscisic acid on active oxygen species, antioxidative defence system and oxidative damage in leaves of maize seedlings. Plant and Cell Physiology 42, 1265-1273.
23. Jiang M, Z hang J. 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.
24. Jiang M, Zhang J. 2002 b. W ater stress-induced abscisic acid accumulation triggers the increased generation of reactive oxygen species and up-regulates the activities of antioxidant enzymes in maize leaves. Journal of Experimental Botany 53, 2401-2410.
25. Jiang M, Zhang J. 2003. Cross-talk between calcium and reactive oxygen species originated from NADPH oxidase in abscisic acidinduced antioxidant defense in leaves of maize seedlings. Plant, Cell and Environment 26, 92 9-939.
26. Jiang M, Zhang J. 2004. Abscisic acid and antioxidant defense in plant cells. Acta Botanica Sinica 46, 1-9.
27. Kiefibowicz-Matuk A. 2012. Involvement of plant C2H2-type zinc finger transcription factors in stress responses. Plant Science 185-186, 78-85.
28. Kodaira KS, Qin F, Phan Tran LS, Maruyama K, Kidokoro S, Fujita Y, Shinozaki K, Yamaguchi-Shinozaki K. 2011. Arabidopsis Cys2/ His2 zinc-finger proteins AZF1 and AZF2 negatively regulate abscisic acidrepressive and auxin-inducible genes under abiotic stress conditions. Plant Physiology 157, 742-756.
29. Koussevitzky S, Nott A, Mockler TC, Hong F , Sachetto-Martins G, Surpin M, Lim J, Mittler R, Chory J. 2007. Multiple signals from damaged chloroplasts converge on a common pathway to regulate nuclear gene expression. Science 316, 715-719.
30. Kwak JM, Mori IC, Pei Z-M, Leonhardt N, Torres MA, Dangl JL, Bloom RE, Bodde S, Jones JDG Schroeder JI. 2003. NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO Journal 22, 2623-2633.
31. Lin F, Ding H, Wang J, Zhang H, Zhang A, Zhang Y, Tan M, Dong W, Jiang M. 2009. Positive feedback regulation of maize NADPH oxidase by mitogen-activated protein kina se cascade in abscisic acid signaling. Journal of Experimental Botany 60, 3221-3238.
32. Lindemose S, O?Shea C, Jensen MK, Skriver K. 2013. Structure, function and networks of transcription factors involved in abiotic stress responses. International Journal of Molecular Sciences 14, 5842-5878.
33. Ma FF, Lu R, Liu HY, Shi B, Zhang JH, Tan MP, Zhang AY, Jiang MY. 2012. Nitric oxide-activated calcium/ca lmodulin-dependent protein kinase regulates the abscisic acid-induced antioxidant defense in maize. Journal of Experimental Botany 63, 4835-4847.
34. Miao Y, Lu D, Wang P, Wang X, Chen J, Miao C, Song CP . 2006. An Arabidopsis glutathione peroxidase functions as both a redox transducer and a scavenger in abscisic acid and drought stress responses. The Plant Cell 18, 2749-2766.
35. Miller G, Shulaev V, Mittler R . 2008. Reactive oxygen signaling and abiotic stress. Physiologia Plantarum 133, 481-489.
36. Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R. 2010. Reactive oxygen species homeostasis and signaling dur ing drought and salinity stresses. Plant, Cell and Environment 33, 453-467.
37. Mittler R, Kim Y, Song L, Coutu J, Coutu A, Ciftci-Yilmaz S, Lee H, Stevenson B, Zhu JK. 2006. Gain-and lo ss-of-function mutations in Zat10 enhance the tolerance of plants to abiotic stress. FEBS Letters 580, 6537-6542.
38. Mustilli AC, Merlot S, Vavasseur A, Fenzi F, Giraudat J. 2002. Arabidopsis OST1 prot ein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. The Plant Cell 14, 3089-3099.
39. Nakashima K, Ito Y, Yamaguchi-Shinozaki K. 2009. Transcriptional regulatory networks in response to abiotic stresses in Arabidopsis and grasses. Plant Physiology 149, 88-95.
40. Neill S, Barros R, Bright J, Desi kan R, Hancock J, Harrison J, Morris P, Ribeiro D, Wilson I. 2008. Nitric oxide, stomatal closure, and abiotic stress. Journal of Experimental Botany 59, 165-176.
41. Rao MV Lee H Creelman RA Mullet JE Davis KR. 2000 Jasmonic acid signaling modulates ozone-induced hypersensitive cell death The Plant Cell 12 1633-1646.
42. Reyna NS, Yang Y. 2006. Molecular analysis of the rice MAP kinase gene family in relation to Magnaporthe grisea infection. Molecular Plant-Microbe Interactions 19, 530-540.
43. Rizhsky L, Davletova S, Liang H, Mittler R. 2004. The zinc finger protein Zat12 is re quired for cytosolic ascorbate peroxidase 1 expression during oxidative stress in Arabidopsis. Journal of Biological Chemistry 279, 11736-11743.
44. Rossel JB, Wilson PB, Hussain D, Woo NS, Gordon MJ, Mewett OP, Howell KA, Whelan J, Kazan K, Pogson BJ. 2007. Systemic and intracellular responses to photooxidative stress in Arabidopsis. The Plant Cell 19, 4091-4110.
45. Sakamoto H, Maruyama K, Sakuma Y, Meshi T, Iwabuchi M, Shinozaki K, Yamaguchi-Shinozaki K. 2004. Arabidopsis Cys2/His2-type zinc-finger proteins function as transcription repressors under drought, cold, and high-salinity stress conditions. Plant Physiolog y 136, 2734-2746.
46. Shi B, Ni L, Liu YP, Zhang AY, Tan MP, Jiang MY. 2014. OsDMI3-mediated activation of OsMPK1 regulates the activities of antioxidant enzymes in abscisic acid signaling in rice. Plant, Cell and Environment 37, 341-352.
47. Shi B, Ni L, Zhang AY, Cao JM, Zhang H, Qin TT, Tan MP, Zhang JH, Jiang MY. 2012. OsDMI3 is a novel component of abscisic acid signaling in the induct ion of antioxidant defense in leaves of rice. Molecular Plant 5, 1359-1374.
48. Sirichandra C, Gu D, Hu HC, et al. 2009. Phosphorylation of the Arabidopsis AtrbohF NADPH oxidase by OST1 protein kinase. FEBS Letters 583, 2982-2986.
49. Sugano S, Kaminaka H, Rybka Z, Catala R, Salinas J, Matsui K, Ohme-Takagi M, Takatsuji H. 2003. Stress-responsive zinc finger gene ZPT2-3 plays a role in drought tole rance in petunia. The Plant Journal 36, 830-841.
50. Sun SJ, Guo SQ, Yang X, Bao YM, Tang HJ, Sun H, Huang J, Zhang HS. 2010. Functional analysis of a novel Cys2/His2-type zinc finger protein in volved in salt tolerance in rice. Journal of Experimental Botany 61, 2807-2818.
51. Umezawa T, Nakashima K, Miyakawa T, Kuromori T, Tanokura M, Shinozaki K, Yamaguchi-Shinozaki K. 2010. Molecular ba sis of the core regulatory network in ABA responses: sensing, signaling and transport. Plant and Cell Physiology 51, 1821- 1839.
52. Vogel JT, Zarka DG, Van Buskirk HA, Fowler SG, Thomashow MF. 2005. Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis. The Plant Journal 41, 1 95-211.
53. Wong HL, Pinontoan R, Hayashi K, et al. 2007. Regulation of rice NADPH oxidase by binding of Rac GTPase to its N-terminal extension. The Plant Cell 19, 4022-4034.
54. Xing Y, Jia W, Zhang J. 2007. AtMEK1 mediates stress-induced gene expression of CAT1 catalase by triggering H2O2 production in Arabidopsis. Journal of Experimental Botany 58, 2969-2981.
55. Xing Y, Jia W, Zhang J. 2008. AtMKK1 mediates ABA-induced CAT1 expression and H2O2 production via AtMPK6-coupled signaling in Arabidopsis. The Plant Journal 54, 440-451.
56. Xu DQ, Huang J, Guo SQ, Yang X, Bao YM, Tang HJ, Zhang HS. 2008. Overexpression of a TFIIIA-type zinc finger protein gene ZFP252 enhances drought and salt tolerance in rice (Oryza sativa L.). FEBS Letters 582, 1037-1043.
57. Xu S, Wang X , Chen J. 2007. Zinc finger protein 1 (ThZF1) from salt cress (Thellungiella halophila) is a Cys-2/His-2-type transcription factor involved in drought and salt stress. Plant Cell Reports 26, 497-506.
58. Yamaguchi- Shinozaki K, Shinozaki K. 2006. Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annual Review of Plant Biology 57, 781-803.
59. Ye N, Zhu G, Liu Y, Li Y, Zhang J. 2011. ABA controls H2O2 accumulation through the induction of OsCATB in rice leaves under water stress. Plant and Cell Physiology 52, 689-698.
60. Zhai Z, Sooksa-nguan T, Vatamaniuk OK. 2009. Establishing RNA interference as a reverse-genetic approach for functional analysis in protoplasts. Plant Physiology 149, 642-652.
61. Zhang A, Jiang M, Zhang J, Ding H, Xu S, Hu X, Tan M. 2007. Nitric oxide induced by hydrogen peroxide mediates abscisic acid-induced activation of the mitogen-activated protein kinase cascade involved in antioxidant defense in maize leaves. New Phytologist 175, 36-50.
62. Zhang A Jiang M Zhang J Tan M Hu X. 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 P hysiology 141 475-487.
63. Zhang H, Ni L, Liu YP, Wang YF, Zhang AY, Tan MP, Jiang MY. 2012. The C2H2-type zinc finger protein ZFP182 is involved in abscisic acidinduced antioxidant defense in rice. Journal of Integrative Plant Biology 54, 500-510.