Conserved miR164-targeted NAC genes negatively regulate drought resistance in rice

Journal of Experimental Botany

Volumn 65, Issue 8, 2014, Pages 2119-2135

  Fang, Yujie ^a   Xie, Kabin ^a,b   Xiong, Lizhong ^a  

^a HUAZHONG AGRICULTURAL UNIVERSITY   (China)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

Abiotic stress; miRNA; NAC; Oryza sativa; transactivation

Indexed keywords

MICRORNA; PLANT RNA; TRANSCRIPTION FACTOR; VEGETABLE PROTEIN;

ACCLIMATIZATION; AMINO ACID SEQUENCE; CHEMISTRY; DROUGHT; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; RICE; SEQUENCE ALIGNMENT;

ACCLIMATIZATION; AMINO ACID SEQUENCE; BASE SEQUENCE; DROUGHTS; GENE EXPRESSION REGULATION, PLANT; MICRORNAS; MOLECULAR SEQUENCE DATA; ORYZA SATIVA; PLANT PROTEINS; RNA, PLANT; SEQUENCE ALIGNMENT; TRANSCRIPTION FACTORS;

EID: 84898939935     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/eru072     Document Type: Article

References (85)

1. Bao N, Lye KW, Barton MK. 2004. MicroRNA binding sites in Arabidopsis class III HD-ZIP mRNAs are required for methylation of the template chromosome. Developmental Cell 7, 653-662
2. Bari R, Datt Pant B, Stitt M, Scheible WR. 2006. PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiology 141, 988-999
3. Bartel DP. 2004. MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell 116, 281-297
4. Barth O, Zschiesche W, Siersleben S, Humbeck K. 2004. Isolation of a novel barley cDNA encoding a nuclear protein involved in stress response and leaf senescence. Physiologia Plantarum 121, 282-293
5. Bazzini AA, Almasia NI, Manacorda CA, et al. 2009. Virus infection elevates transcriptional activity of miR164a promoter in plants. BMC Plant Biology 9, 152
6. Brodersen P, Sakvarelidze-Achard L, Bruun-Rasmussen M, Dunoyer P, Yamamoto YY, Sieburth L, Voinnet O. 2008. Widespread translational inhibition by plant miRNAs and siRNAs. Science 320, 1185-1190
7. Cheong YH, Chang H-S, Gupta R, Wang X, Zhu T, Luan S. 2002. Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiology 129, 661-677
8. Chiou TJ, Aung K, Lin SI, Wu CC, Chiang SF, Su CL. 2006. Regulation of phosphate homeostasis by MicroRNA in Arabidopsis. The Plant Cell 18, 412-421
9. Decreux A, Messiaen J. 2005. Wall-Associated kinase WAK1 interacts with cell wall pectins in a calcium-induced conformation. Plant and Cell Physiology 46, 268-278
10. 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
11. Fujii H, Chiou TJ, Lin SI, Aung K, Zhu JK. 2005. A miRNA involved in phosphate-starvation response in Arabidopsis. Current Biology 15, 2038-2043
12. 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
13. Griffiths-Jones S. 2006. miRBase: The microRNA sequence database. Methods in Molecular Biology 342, 129-138
14. Guo HS, Xie Q, Fei JF, Chua NH. 2005. MicroRNA directs mRNA cleavage of the transcription factor NAC1 to downregulate auxin signals for arabidopsis lateral root development. The Plant Cell 17, 1376-1386
15. He XF, Fang YY, Feng L, Guo HS. 2008. Characterization of conserved and novel microRNAs and their targets, including a TuMV-induced TIRNBS-LRR class R gene-Derived novel miRNA in Brassica. FEBS Letters 582, 2445-2452
16. Hibara K, Takada S, Tasaka M. 2003. CUC1 gene activates the expression of SAM-related genes to induce adventitious shoot formation. The Plant Journal 36, 687-696
17. 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
18. 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
19. 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
20. 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
21. 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
22. Jia X, Mendu V, Tang G. 2010. An array platform for identification of stress-responsive microRNAs in plants. Methods in Molecular Biology 639, 253-269
23. Jia X, Ren L, Chen QJ, Li R, Tang G. 2009. UV-B-responsive microRNAs in Populus tremula. Journal of Plant Physiology 166, 2046-2057
24. Jones-Rhoades MW, Bartel DP. 2004. Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Molecular Cell 14, 787-799
25. Khraiwesh B, Arif MA, Seumel GI, Ossowski S, Weigel D, Reski R, Frank W. 2010. Transcriptional control of gene expression by microRNAs. Cell 140, 111-122
26. Khraiwesh B, Zhu JK, Zhu J. 2012. Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. Biochimica et Biophysica Acta 1819, 137-148
27. Kim JH, Woo HR, Kim J, Lim PO, Lee IC, Choi SH, Hwang D, Nam HG. 2009. Trifurcate feed-forward regulation of age-Dependent cell death involving miR164 in Arabidopsis. Science 323, 1053-1057
28. Kleinow T, Himbert S, Krenz B, Jeske H, Koncz C. 2009. NAC domain transcription factor ATAF1 interacts with SNF1-related kinases and silencing of its subfamily causes severe developmental defects in Arabidopsis. Plant Science 177, 360-370
29. Laufs P, Peaucelle A, Morin H, Traas J. 2004. MicroRNA regulation of the CUC genes is required for boundary size control in Arabidopsis meristems. Development 131, 4311-4322
30. Li B, Yin W, Xia X. 2009. Identification of microRNAs and their targets from Populus euphratica. Biochemical and Biophysical Research Communications 388, 272-277
31. Li J, Guo G, Guo W, Tong D, Ni Z, Sun Q, Yao Y. 2012. miRNA164-Directed cleavage of ZmNAC1 confers lateral root development in maize (Zea mays L). BMC Plant Biology 12, 220
32. Li T, Li H, Zhang YX, Liu JY. 2011. Identification and analysis of seven H2O2-responsive miRNAs and 32 new miRNAs in the seedlings of rice (Oryza sativa L. ssp. indica). Nucleic Acids Research 39, 2821-2833
33. Li WX, Oono Y, Zhu J, He XJ, Wu JM, Iida K, Lu XY, Cui X, Jin H, Zhu JK. 2008. The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and posttranscriptionally to promote drought resistance. The Plant Cell 20, 2238-2251
34. Li YF, Zheng Y, Addo-Quaye C, Zhang L, Saini A, Jagadeeswaran G, Axtell MJ, Zhang W, Sunkar R. 2010. Transcriptome-wide identification of microRNA targets in rice. The Plant Journal 62, 742-759
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. 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
37. Lu S, Sun YH, Chiang VL. 2008. Stress-responsive microRNAs in Populus. The Plant Journal 55, 131-151
38. Lu S, Sun YH, Shi R, Clark C, Li L, Chiang VL. 2005. Novel and mechanical stress-responsive microRNAs in Populus trichocarpa that are absent from Arabidopsis. The Plant Cell 17, 2186-2203
39. Lu XY, Huang XL. 2008. Plant miRNAs and abiotic stress responses. Biochemical and Biophysical Research Communications 368, 458-462
40. Lv DK, Bai X, Li Y, Ding XD, Ge Y, Cai H, Ji W, Wu N, Zhu YM. 2010. Profiling of cold-stress-responsive miRNAs in rice by microarrays. Gene 459, 39-47
41. Mallory AC, Dugas DV, Bartel DP, Bartel B. 2004. MicroRNA regulation of NAC-Domain targets is required for proper formation and separation of adjacent embryonic, vegetative, and floral organs. Current Biology 14, 1035-1046
42. Murgia I, Tarantino D, Vannini C, Bracale M, Carravieri S, Soave C. 2004. Arabidopsis thaliana plants overexpressing thylakoidal ascorbate peroxidase show increased resistance to Paraquat-induced photooxidative stress and to nitric oxide-induced cell death. The Plant Journal 38, 940-953
43. Murray MG, Thompson WF. 1980. Rapid isolation of high molecular weight plant DNA. Nucleic Acids Research 8, 4321-4325
44. Nakashima K, Takasaki H, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K. 2012. NAC transcription factors in plant abiotic stress responses. Biochimica et Biophysica Acta 1819, 97-103
45. Nakashima K, Tran LS, 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. The Plant Journal 51, 617-630
46. Narusaka Y, Narusaka M, Seki M, Umezawa T, Ishida J, Nakajima M, Enju A, Shinozaki K. 2004. Crosstalk in the responses to abiotic and biotic stresses in Arabidopsis: Analysis of gene expression in cytochrome P450 gene superfamily by cDNA microarray. Plant Molecular Biology 55, 327-342
47. Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, Estelle M, Voinnet O, Jones JD. 2006. A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312, 436-439
48. Nikovics K, Blein T, Peaucelle A, Ishida T, Morin H, Aida M, Laufs P. 2006. The balance between the MIR164A and CUC2 genes controls leaf margin serration in Arabidopsis. The Plant Cell 18, 2929-2945
49. Nuruzzaman M, Manimekalai R, Sharoni AM, Satoh K, Kondoh H, Ooka H, Kikuchi S. 2010. Genome-wide analysis of NAC transcription factor family in rice. Gene 465, 30-44
50. Nuruzzaman M, Sharoni AM, Kikuchi S. 2013. Roles of NAC transcription factors in the regulation of biotic and abiotic stress responses in plants. Frontiers in Microbiology 4, 248
51. Olsen AN, Ernst HA, Leggio LL, Skriver K. 2005. NAC transcription factors: Structurally distinct, functionally diverse. Trends in Plant Science 10, 79-87
52. Palatnik JF, Allen E, Wu X, Schommer C, Schwab R, Carrington JC, Weigel D. 2003. Control of leaf morphogenesis by microRNAs. Nature 425, 257-263
53. Peaucelle A, Morin H, Traas J, Laufs P. 2007. Plants expressing a miR164-resistant CUC2 gene reveal the importance of post-meristematic maintenance of phyllotaxy in Arabidopsis. Development 134, 1045-1050
54. Puranik S, Sahu PP, Srivastava PS, Prasad M. 2012. NAC proteins: Regulation and role in stress tolerance. Trends in Plant Science 17, 369-381
55. Reyes JL, Chua NH. 2007. ABA induction of miR159 controls transcript levels of two MYB factors during Arabidopsis seed germination. The Plant Journal 49, 592-606
56. Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, Bartel DP. 2002. Prediction of plant microRNA targets. Cell 110, 513-520
57. Sanan-Mishra N, Kumar V, Sopory SK, Mukherjee SK. 2009. Cloning and validation of novel miRNA from basmati rice indicates cross talk between abiotic and biotic stresses. Molecular Genetics and Genomics 282, 463-474
58. Shabala S, Cuin TA. 2008. Potassium transport and plant salt tolerance. Physiologia Plantarum 133, 651-669
59. Sieber P, Wellmer F, Gheyselinck J, Riechmann JL, Meyerowitz EM. 2007. Redundancy and specialization among plant microRNAs: Role of the MIR164 family in developmental robustness. Development 134, 1051-1060
60. Sivaguru M, Ezaki B, He ZH, Tong H, Osawa H, Baluska F, Volkmann D, Matsumoto H. 2003. Aluminum-induced gene expression and protein localization of a cell wall-Associated receptor kinase in Arabidopsis. Plant Physiology 132, 2256-2266
61. Sperotto RA, Ricachenevsky FK, Duarte GL, Boff T, Lopes KL, Sperb ER, Grusak MA, Fett JP. 2009. Identification of up-regulated genes in flag leaves during rice grain filling and characterization of OsNAC5, a new ABAdependent transcription factor. Planta 230, 985-1002
62. Sunkar R, Zhou X, Zheng Y, Zhang W, Zhu JK. 2008. Identification of novel and candidate miRNAs in rice by high throughput sequencing. BMC Plant Biology 8, 25
63. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. 1997. The CLUSTAL-X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 4876-4882
64. Tran LS, Nakashima K, Sakuma Y, Osakabe Y, Qin F, Simpson SD, Maruyama K, Fujita Y, Shinozaki K, Yamaguchi-Shinozaki K. 2007. Co-expression of the stress-inducible zinc finger homeodomain ZFHD1 and NAC transcription factors enhances expression of the ERD1 gene in Arabidopsis. The Plant Journal 49, 46-63
65. 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
66. Vasudevan S, Tong Y, Steitz JA. 2007. Switching from repression to activation: MicroRNAs can up-regulate translation. Science 318, 1931-1934
67. Vinocur B, Altman A. 2005. Recent advances in engineering plant tolerance to abiotic stress: Achievements and limitations. Current Opinion in Biotechnology 16, 123-132
68. Wang W, Vinocur B, Shoseyov O, Altman A. 2004. Role of plant heatshock proteins and molecular chaperones in the abiotic stress response. Trends in Plant Science 9, 244-252
69. Wang XJ, Reyes JL, Chua NH, Gaasterland T. 2004. Prediction and identification of Arabidopsis thaliana microRNAs and their mRNA targets. Genome Biology 5, R65
70. Winkel-Shirley B. 2002. Biosynthesis of flavonoids and effects of stress. Current Opinion in Plant Biology 5, 218-223
71. Wu L, Zhang Q, Zhou H, Ni F, Wu X, Qi Y. 2009. Rice MicroRNA effector complexes and targets. The Plant Cell 21, 3421-3435
72. Wu L, Zhou H, Zhang Q, Zhang J, Ni F, Liu C, Qi Y. 2010. DNA methylation mediated by a microRNA pathway. Molecular Cell 38, 465-475
73. Xie Q, Frugis G, Colgan D, Chua NH. 2000. Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development. Genes and Development 14, 3024-3036
74. Xie Q, Guo HS, Dallman G, Fang S, Weissman AM, Chua NH. 2002. SINAT5 promotes ubiquitin-related degradation of NAC1 to attenuate auxin signals. Nature 419, 167-170
75. Xin M, Wang Y, Yao Y, Xie C, Peng H, Ni Z, Sun Q. 2010. Diverse set of microRNAs are responsive to powdery mildew infection and heat stress in wheat (Triticum aestivum L). BMC Plant Biology 10, 123
76. Xue W, Xing Y, Weng X, Zhao Y, Tang W, Wang L, Zhou H, Yu S, Xu C, Li X, Zhang Q. 2008. Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nature Genetics 40, 761-767
77. Yang T, Poovaiah BW. 2002. A calmodulin-binding/CGCG box DNAbinding protein family involved in multiple signaling pathways in plants. Journal of Biological Chemistry 277, 45049-45058
78. Yoo SD, Cho YH, Sheen J. 2007. Arabidopsis mesophyll protoplasts: A versatile cell system for transient gene expression analysis. Nature Protocols 2, 1565-1572
79. Yoo SY, Kim Y, Kim SY, Lee JS, Ahn JH. 2007. Control of flowering time and cold response by a NAC-Domain protein in Arabidopsis. PLoS One 2, e642
80. Yoon HK, Kim SG, Kim SY, Park CM. 2008. Regulation of leaf senescence by NTL9-mediated osmotic stress signaling in Arabidopsis. Molecules and Cells 25, 438-445
81. Zhao B, Ge L, Liang R, Li W, Ruan K, Lin H, Jin Y. 2009. Members of miR-169 family are induced by high salinity and transiently inhibit the NF-YA transcription factor. BMC Molecular Biology 10, 29
82. Zhao JP, Jiang XL, Zhang BY, Su XH. 2012. Involvement of microRNAmediated gene expression regulation in the pathological development of stem canker disease in Populus trichocarpa. PLoS One 7, e44968
83. Zheng X, Chen B, Lu G, Han B. 2009. Overexpression of a NAC transcription factor enhances rice drought and salt tolerance. Biochemical and Biophysical Research Communications 379, 985-989
84. 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
85. Zhou M, Gu L, Li P, Song X, Wei L, Chen Z, Cao X. 2010. Degradome sequencing reveals endogenous small RNA targets in rice (Oryza sativa L. ssp. indica). Frontiers in Biology 5, 67-90