A stress-responsive NAC transcription factor SNAC3 confers heat and drought tolerance through modulation of reactive oxygen species in rice

Journal of Experimental Botany

Volumn 66, Issue 21, 2015, Pages 6803-6817

  Fang, Yujie ^a   Liao, Kaifeng ^a   Du, Hao ^a   Xu, Yan ^a   Song, Huazhi ^a   Li, Xianghua ^a   Xiong, Lizhong ^a  

^a HUAZHONG AGRICULTURAL UNIVERSITY   (China)

Author keywords

Abiotic stress; NAC; Oryza sativa; ROS; Transcription factors

Indexed keywords

PLANT PROTEIN; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR;

DROUGHT; GENE EXPRESSION REGULATION; GENETICS; HEAT; METABOLISM; ORYZA; PHYSIOLOGICAL STRESS; TRANSGENIC PLANT;

DROUGHTS; GENE EXPRESSION REGULATION, PLANT; HOT TEMPERATURE; ORYZA; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; REACTIVE OXYGEN SPECIES; STRESS, PHYSIOLOGICAL; TRANSCRIPTION FACTORS;

EID: 84948437972     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erv386     Document Type: Article

References (66)

1. Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K. 2003. Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. The Plant Cell 15, 63-78.
2. Abe H, Yamaguchi-Shinozaki K, Urao T, Iwasaki T, Hosokawa D, Shinozaki K. 1997. Role of arabidopsis MYC and MYB homologs in drought- and abscisic acid-regulated gene expression. The Plant Cell 9, 1859-1868.
3. Agarie S, Hanaoka N, Ueno O, Miyazaki A, Kubota F, Agata W, Kaufman PB. 1998. Effects of silicon on tolerance to water deficit and heat stress in rice plants (Oryza sativa L.), monitored by electrolyte leakage. Plant Production Science 1, 96-103.
4. Apel K, Hirt H. 2004. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology 55, 373-399.
5. Bajji M, Kinet J M, Lutts S. 2002. The use of the electrolyte leakage method for assessing cell membrane stability as a water stress tolerance test in durum wheat. Plant Growth Regulation 36, 61-70.
6. Barnabás B, Jäger K, Fehér A. 2008. The effect of drought and heat stress on reproductive processes in cereals. Plant, Cell and Environment 31, 11-38.
7. Baxter A, Mittler R, Suzuki N. 2014. ROS as key players in plant stress signalling. Journal of Experimental Botany 65, 1229-1240.
8. Bechtold U, Albihlal WS, Lawson T, et al. 2013. Arabidopsis HEAT SHOCK TRANSCRIPTION FACTORA1b overexpression enhances water productivity, resistance to drought, and infection. Journal of Experimental Botany 64, 3467-3481.
9. Bray EA. 2004. Genes commonly regulated by water-deficit stress in Arabidopsis thaliana. Journal of Experimental Botany 55, 2331-2341.
10. De Clercq I, Vermeirssen V, Van Aken O, et al. 2013. The membranebound NAC transcription factor ANAC013 functions in mitochondrial retrograde regulation of the oxidative stress response in Arabidopsis. The Plant Cell 25, 3472-3490.
11. Ding X, Cao Y, Huang L, Zhao J, Xu C, Li X, Wang S. 2008. Activation of the indole-3-acetic acid-amido synthetase GH3-8 suppresses expansin expression and promotes salicylate- and jasmonate-independent basal immunity in rice. The Plant Cell 20, 228-240.
12. Du H, Wang N, Cui F, Li X, Xiao J, Xiong L. 2010. Characterization of the beta-carotene hydroxylase gene DSM2 conferring drought and oxidative stress resistance by increasing xanthophylls and abscisic acid synthesis in rice. Plant Physiology 154, 1304-1318.
13. Ernst HA, Olsen AN, Larsen S, Lo Leggio L. 2004. Structure of the conserved domain of ANAC, a member of the NAC family of transcription factors. EMBO Reports 5, 297-303.
14. Fang Y, You J, Xie K, Xie W, Xiong L. 2008. Systematic sequence analysis and identification of tissue-specific or stress-responsive genes of NAC transcription factor family in rice. Molecular Genetics and Genomics 280, 547-563.
15. Fujita M, Fujita Y, Maruyama K, Seki M, Hiratsu K, Ohme-Takagi M, Tran LS, Yamaguchi-Shinozaki K, Shinozaki K. 2004. A dehydrationinduced NAC protein, RD26, is involved in a novel ABA-dependent stresssignaling pathway. The Plant Journal 39, 863-876.
16. Fujita Y, Fujita M, Satoh R, Maruyama K, Parvez MM, Seki M, Hiratsu K, Ohme-Takagi M, Shinozaki K, Yamaguchi-Shinozaki K. 2005. AREB1 is a transcription activator of novel ABRE-dependent ABA signaling that enhances drought stress tolerance in Arabidopsis. The Plant Cell 17, 3470-3488.
17. Guo Y, Gan S. 2006. AtNAP, a NAC family transcription factor, has an important role in leaf senescence. The Plant Journal 46, 601-612.
18. Haake V, Cook D, Riechmann JL, Pineda O, Thomashow MF, Zhang JZ. 2002. Transcription factor CBF4 is a regulator of drought adaptation in Arabidopsis. Plant Physiology 130, 639-648.
19. Hirayama T, Shinozaki K. 2010. Research on plant abiotic stress responses in the post-genome era: past, present and future. The Plant Journal 61, 1041-1052.
20. Hu H, Dai M, Yao J, Xiao B, Li X, Zhang Q, Xiong L. 2006. Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proceedings of the National Academy of Sciences, USA 103, 12987-12992.
21. Hu H, You J, Fang Y, Zhu X, Qi Z, Xiong L. 2008. Characterization of transcription factor gene SNAC2 conferring cold and salt tolerance in rice. Plant Molecular Biology 67, 169-181.
22. Huang Y, Xiao B, Xiong L. 2007. Characterization of a stress responsive proteinase inhibitor gene with positive effect in improving drought resistance in rice. Planta 226, 73-85.
23. Ishizaki K, Schauer N, Larson TR, Graham IA, Fernie AR, Leaver CJ. 2006. The mitochondrial electron transfer flavoprotein complex is essential for survival of Arabidopsis in extended darkness. The Plant Journal 47, 751-760.
24. Jeong DH, German MA, Rymarquis LA, Thatcher SR, Green PJ. 2010. Abiotic stress-associated miRNAs: detection and functional analysis. Methods in Molecular Biology 592, 203-230.
25. Jeong JS, Kim YS, Baek KH, Jung H, Ha SH, Do Choi Y, Kim M, Reuzeau C, Kim JK. 2010. Root-specific expression of OsNAC10 improves drought tolerance and grain yield in rice under field drought conditions. Plant Physiology 153, 185-197.
26. Jeong JS, Kim YS, Redillas MC, Jang G, Jung H, Bang SW, Choi YD, Ha SH, Reuzeau C, Kim JK. 2013. OsNAC5 overexpression enlarges root diameter in rice plants leading to enhanced drought tolerance and increased grain yield in the field. Plant Biotechnology Journal 11, 101-114.
27. Jeong JS, Park YT, Jung H, Park SH, Kim JK. 2009. Rice NAC proteins act as homodimers and heterodimers. Plant Biotechnology Reports 3, 127-134.
28. Kalbina I, Strid A. 2006. The role of NADPH oxidase and MAP kinase phosphatase in UV-B-dependent gene expression in Arabidopsis. Plant, Cell and Environment 29, 1783-1793.
29. Karimi M, Bleys A, Vanderhaeghen R, Hilson P. 2007. Building blocks for plant gene assembly. Plant Physiology 145, 1183-1191.
30. Kim S, Kang JY, Cho DI, Park JH, Kim SY. 2004. ABF2, an ABREbinding bZIP factor, is an essential component of glucose signaling and its overexpression affects multiple stress tolerance. The Plant Journal 40, 75-87.
31. Kim YS, Kim SG, Park JE, Park HY, Lim MH, Chua NH, Park CM. 2006. A membrane-bound NAC transcription factor regulates cell division in Arabidopsis. The Plant Cell 18, 3132-3144.
32. Kosova K, Vitamvas P, Prasil IT, Renaut J. 2011. Plant proteome changes under abiotic stress-contribution of proteomics studies to understanding plant stress response. Journal of Proteomics 74, 1301-1322.
33. Lee S, Seo PJ, Lee HJ, Park CM. 2012. A NAC transcription factor NTL4 promotes reactive oxygen species production during drought-induced leaf senescence in Arabidopsis. The Plant Journal 70, 831-844.
34. Lee SC, Choi DS, Hwang IS, Hwang BK. 2010. The pepper oxidoreductase CaOXR1 interacts with the transcription factor CaRAV1 and is required for salt and osmotic stress tolerance. Plant Molecular Biology 73, 409-424.
35. Lin YJ, Zhang Q. 2005. Optimising the tissue culture conditions for high efficiency transformation of indica rice. Plant Cell Reports 23, 540-547.
36. Liu H, Li X, Xiao J, Wang S. 2012. A convenient method for simultaneous quantification of multiple phytohormones and metabolites: application in study of rice-bacterium interaction. Plant Methods 8, 2.
37. Liu JQ, Allan DL, Vance CP. 2010. Systemic signaling and local sensing of phosphate in common bean: cross-talk between photosynthate and microRNA399. Molecular Plant 3, 428-437.
38. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402-408.
39. Maruta T, Tanouchi A, Tamoi M, Yabuta Y, Yoshimura K, Ishikawa T, Shigeoka S. 2010. Arabidopsis chloroplastic ascorbate peroxidase isoenzymes play a dual role in photoprotection and gene regulation under photooxidative stress. Plant and Cell Physiology 51, 190-200.
40. Mittler R. 2002. Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science 7, 405-410.
41. Narsai R, Wang C, Chen J, Wu J, Shou H, Whelan J. 2013. Antagonistic, overlapping and distinct responses to biotic stress in rice (Oryza sativa) and interactions with abiotic stress. BMC Genomics 14, 93.
42. Ning J, Li X, Hicks LM, Xiong L. 2010. A Raf-like MAPKKK gene DSM1 mediates drought resistance through reactive oxygen species scavenging in rice. Plant Physiology 152, 876-890.
43. Pan X, Welti R, Wang X. 2008. Simultaneous quantification of major phytohormones and related compounds in crude plant extracts by liquid chromatography-electrospray tandem mass spectrometry. Phytochemistry 69, 1773-1781.
44. Puranik S, Sahu PP, Srivastava PS, Prasad M. 2012. NAC proteins: regulation and role in stress tolerance. Trends in Plant Science 17, 369-381.
45. 2-induced cell death. The Plant Journal 52, 640-657.
46. Sacar MD, Hamzeiy H, Allmer J. 2013. Can MiRBase provide positive data for machine learning for the detection of MiRNA hairpins? Journal of Integrative Bioinformatics 10, 215.
47. Schroeder JI, Kwak JM, Allen GJ. 2001. Guard cell abscisic acid signalling and engineering drought hardiness in plants. Nature 410, 327-330.
48. Shahnejat-Bushehri S, Balazadeh S, Mueller-Roeber B. 2012. Arabidopsis NAC transcription factor JUNGBRUNNEN1 affects thermomemory-associated genes and enhances heat stress tolerance in primed and unprimed conditions. Plant Signaling Behavior 7, 1518-1521.
49. Shi H, Wang X, Ye T, Chen F, Deng J, Yang P, Zhang Y, Chan Z. 2014. The Cysteine2/Histidine2-Type transcription factor ZINC FINGER OF ARABIDOPSIS THALIANA6 modulates biotic and abiotic stress responses by activating salicylic acid-related genes and C-REPEAT-BINDING FACTOR genes in Arabidopsis. Plant Physiology 165, 1367-1379.
50. Shinozaki K, Yamaguchi-Shinozaki K. 2007. Gene networks involved in drought stress response and tolerance. Journal of Experimental Botany 58, 221-227.
51. Smirnoff N. 1993. The role of active oxygen in the response of plants to water deficit and desiccation. New Phytologist 125, 27-58.
52. Suzuki N, Miller G, Morales J, Shulaev V, Torres MA, Mittler R. 2011. Respiratory burst oxidases: the engines of ROS signaling. Current Opinion in Plant Biology 14, 691-699.
53. Tahtiharju S, Palva T. 2001. Antisense inhibition of protein phosphatase 2C accelerates cold acclimation in Arabidopsis thaliana. The Plant Journal 26, 461-470.
54. Takada S, Hibara K, Ishida T, Tasaka M. 2001. The CUP-SHAPED COTYLEDON1 gene of Arabidopsis regulates shoot apical meristem formation. Development 128, 1127-1135.
55. Tang N, Zhang H, Li X, Xiao J, Xiong L. 2012. Constitutive activation of transcription factor OsbZIP46 improves drought tolerance in rice. Plant Physiology 158, 1755-1768.
56. Tran LS, Nakashima K, Sakuma Y, Simpson SD, Fujita Y, Maruyama K, Fujita M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K. 2004. Isolation and functional analysis of Arabidopsis stress-inducible NAC transcription factors that bind to a drought-responsive cis-element in the early responsive to dehydration stress 1 promoter. The Plant Cell 16, 2481-2498.
57. Uauy C, Distelfeld A, Fahima T, Blechl A, Dubcovsky J. 2006. A NAC gene regulating senescence improves grain protein, zinc, and iron content in wheat. Science 314, 1298-1301.
58. 2-induced leaf cell death and the crosstalk of reactive nitric/oxygen species. Journal of Integrative Plant Biology 55, 202-208.
59. Wu A, Allu AD, Garapati P, et al. 2012. JUNGBRUNNEN1, a reactive oxygen species-responsive NAC transcription factor, regulates longevity in Arabidopsis. The Plant Cell 24, 482-506.
60. Xiong L, Schumaker KS, Zhu JK. 2002. Cell signaling during cold, drought, and salt stress. The Plant Cell 14 Suppl, S165-S183.
61. Xue W, Xing Y, Weng X, et al. 2008. Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nature Genetics 40, 761-767.
62. You J, Zong W, Li X, Ning J, Hu H, Xiao J, Xiong L. 2013. The SNAC1-targeted gene OsSRO1c modulates stomatal closure and oxidative stress tolerance by regulating hydrogen peroxide in rice. Journal of Experimental Botany 64, 569-583.
63. Yuan B, Shen X, Li X, Xu C, Wang S. 2007. Mitogen-activated protein kinase OsMPK6 negatively regulates rice disease resistance to bacterial pathogens. Planta 226, 953-960.
64. Zhang H, Jin J, Tang L, Zhao Y, Gu X, Gao G, Luo J. 2011. PlantTFDB 2.0: update and improvement of the comprehensive plant transcription factor database. Nucleic Acids Research 39, 1114-1117.
65. Zhong R, Demura T, Ye ZH. 2006. SND1, a NAC domain transcription factor, is a key regulator of secondary wall synthesis in fibers of Arabidopsis. The Plant Cell 18, 3158-3170.
66. Zhou J, Wang X, Jiao Y, et al. 2007. Global genome expression analysis of rice in response to drought and high-salinity stresses in shoot, flag leaf, and panicle. Plant Molecular Biology 63, 591-608.