The transcriptional regulatory network in the drought response and its crosstalk in abiotic stress responses including drought, cold, and heat

Frontiers in Plant Science

Volumn 5, Issue MAY, 2014, Pages

  Nakashima, Kazuo ^a   Yamaguchi Shinozaki, Kazuko ^b   Shinozaki, Kazuo ^c  

^a JAPAN INTERNATIONAL RESEARCH CENTER FOR AGRICULTURAL SCIENCES   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c RIKEN Center for Sustainable Resource Science   (Japan)

Author keywords

ABA; Abiotic stress; Drought; Signal transduction; Transcription factor

Indexed keywords

EID: 84901024283     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00170     Document Type: Review

References (79)

1. Alonso-Blanco, C., Gomez-Mena, C., Llorente, F., Koornneef, M., Salinas, J., and Martinez-Zapater, J. M. (2005). Genetic and molecular analyses of natural variation indicate CBF2 as a candidate gene for underlying a freezing tolerance quantitative trait locus in Arabidopsis. Plant Physiol. 139, 1304-1312. doi: 10.1104/pp.105.068510
2. Bang, S. W., Park, S. H., Jeong, J. S., Kim, Y. S., Jung, H., Ha, S. H., et al. (2013). Characterization of the stress-inducible OsNCED3 promoter in different transgenic rice organs and over three homozygous generations. Planta 237, 211-224. doi: 10.1007/s00425-012-1764-1
3. Barbosa, E. G. G., Leite, J. P., Marin, S. R. R., Marinho, J. P., Fátima Corrêa Carvalho, J., Fuganti-Pagliarini, R., et al. (2013). Overexpression of the ABA-dependent AREB1 transcription factor from Arabidopsis thaliana improves soybean tolerance to water deficit. Plant Mol. Biol. Rep. 31, 719-730. doi: 10.1007/s11105-012-0541-4
4. Behnam, B., Kikuchi, A., Celebi-Toprak, F., Kasuga, M., Yamaguchi-Shinozaki, K., and Watanabe, K. N. (2007). Arabidopsis rd29A::DREB1A enhances freezing tolerance in transgenic potato. Plant Cell Rep. 26, 1275-1282. doi: 10.1007/s00299-007-0360-5
5. Bhatnagar-Mathur, P., Devi, M. J., Reddy, D. S., Lavanya, M., Vadez, V., Serraj, R., et al. (2007). Stress-inducible expression of At DREB1A in transgenic peanut (Arachis hypogaea L.) increases transpiration efficiency under water-limiting conditions. Plant Cell Rep. 26, 2071-2082. doi: 10.1007/s00299-007-0406-8
6. Bhatnagar-Mathur, P., Rao, J. S., Vadez, V., Dumbala, S. R., Rathore, A., Yamaguchi-Shinozaki, K., et al. (2013). Transgenic peanut overexpressing the DREB1A transcription factor has higher yields under drought stress. Mol. Breed. 33, 327-340. doi: 10.1007/s11032-013-9952-7
7. Bray, E. A., Bailey-Serres, J., and Weretilnyk, E. (2000). "Responses to abiotic stresses, " in Biochemistry and Molecular Biology of Plants, eds B. B. Buchanan, W. Gruissem, and R. L. Jones (Rockville: American Society of Plant Physiologists), 1158-1203.
8. Cheng, M. C., Liao, P. M., Kuo, W. W., and Lin, T. P. (2013). The Arabidopsis ETHYLENE RESPONSE FACTOR1 regulates abiotic stress-responsive gene expression by binding to different cis-acting elements in response to different stress signals. Plant Physiol. 162, 1566-1582. doi: 10.1104/pp.113.221911
9. 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. doi: 10.1146/annurev-arplant-042809-112122
10. Datta, K., Baisakh, N., Ganguly, M., Krishnan, S., Yamaguchi Shinozaki, K., and Datta, S. K. (2012). Overexpression of Arabidopsis and rice stress genes' inducible transcription factor confers drought and salinity tolerance to rice. Plant Biotechnol. J. 10, 579-586. doi: 10.1111/j.1467-7652.2012.00688.x
11. de Paiva Rolla, A. A., de Fatima Correa Carvalho, J., Fuganti-Pagliarini, R., Engels, C., Do Rio, A., Marin, S. R., et al. (2013). Phenotyping soybean plants transformed with rd29A:AtDREB1A for drought tolerance in the greenhouse and field. Transgenic Res. 23, 75-87. doi: 10.1007/s11248-013-9723-6
12. Edmeades, G. O. (2013). Progress in Achieving and Delivering Drought Tolerance in Maize-An Update. Ithaca, NY: ISAAA
13. Engels, C., Fuganti-Pagliarini, R., Marin, S. R. R., Marcelino-Guimarães, F. C., Oliveira, M. C. N., Kanamori, N., et al. (2013). Introduction of the rd29A:AtDREB2A CA gene into soybean (Glycine max L. Merril) and its molecular characterization in the leaves and roots during dehydration. Genet. Mol. Biol. 36, 556-565. doi: 10.1590/S1415-47572013000400015
14. Finkelstein, R. R., Gampala, S. S., and Rock, C. D. (2002). Abscisic acid signaling in seeds and seedlings. Plant Cell 14(Suppl.), S15-S45. doi: 10.1105/tpc.010441
15. Francia, E., Barabaschi, D., Tondelli, A., Laido, G., Rizza, F., Stanca, A. M., et al. (2007). Fine mapping of a HvCBF gene cluster at the frost resistance locus Fr-H2 in barley. Theor. Appl. Genet. 115, 1083-1091. doi: 10.1007/s00122-007-0634-x
16. Fujita, Y., Fujita, M., Satoh, R., Maruyama, K., Parvez, M. M., Seki, M., et al. (2005). AREB1 is a transcription activator of novel ABRE-dependent ABA signaling that enhances drought stress tolerance in Arabidopsis. Plant Cell 17, 3470-3488. doi: 10.1105/tpc.105.035659
17. Fujita, Y., Fujita, M., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2011). ABA-mediated transcriptional regulation in response to osmotic stress in plants. J. Plant Res. 124, 509-525. doi: 10.1007/s10265-011-0412-3
18. Fujita, Y., Nakashima, K., Yoshida, T., Katagiri, T., Kidokoro, S., Kanamori, N., et al. (2009). Three SnRK2 protein kinases are the main positive regulators of abscisic acid signaling in response to water stress in Arabidopsis. Plant Cell Physiol. 50, 2123-2132. doi: 10.1093/pcp/pcp147
19. Fujita, Y., Yoshida, T., and Yamaguchi-Shinozaki, K. (2013). Pivotal role of the AREB/ABF-SnRK2 pathway in ABRE-mediated transcription in response to osmotic stress in plants. Physiol. Plant. 147, 15-27. doi: 10.1111/j.1399-3054.2012.01635.x
20. Furihata, T., Maruyama, K., Fujita, Y., Umezawa, T., Yoshida, R., Shinozaki, K., et al. (2006). Abscisic acid-dependent multisite phosphorylation regulates the activity of a transcription activator AREB1. Proc. Natl. Acad. Sci. U.S.A. 103, 1988-1993. doi: 10.1073/pnas.0505667103
21. Ganguly, M., Roychoudhury, A., Sarkar, S. N., Sengupta, D. N., Datta, S. K., and Datta, K. (2011). Inducibility of three salinity/abscisic acid-regulated promoters in transgenic rice with gusA reporter gene. Plant Cell Rep. 30, 1617-1625. doi: 10.1007/s00299-011-1072-4
22. Hong, B., Tong, Z., Ma, N., Li, J., Kasuga, M., Yamaguchi-Shinozaki, K., et al. (2006). Heterologous expression of the AtDREB1A gene in chrysanthemum increases drought and salt stress tolerance. Sci. China C Life Sci. 49, 436-445. doi: 10.1007/s11427-006-2014-1
23. Hsieh, T. H., Lee, J. T., Charng, Y. Y., and Chan, M. T. (2002a). Tomato plants ectopically expressing Arabidopsis CBF1 show enhanced resistance to water deficit stress. Plant Physiol. 130, 618-626. doi: 10.1104/pp.006783
24. Hsieh, T. H., Lee, J. T., Yang, P. T., Chiu, L. H., Charng, Y. Y., Wang, Y. C., et al. (2002b). Heterology expression of the Arabidopsis C-repeat/dehydration response element binding factor 1 gene confers elevated tolerance to chilling and oxidative stresses in transgenic tomato. Plant Physiol. 129, 1086-1094. doi: 10.1104/pp.003442
25. Hu, H., Dai, M., Yao, J., Xiao, B., Li, X., Zhang, Q., et al. (2006). Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proc. Natl. Acad. Sci. U.S.A. 103, 12987-12992. doi: 10.1073/pnas.0604882103
26. Ishizaki, T., Maruyama, K., Obara, M., Fukutani, A., Yamaguchi-Shinozaki, K., Ito, Y., et al. (2012). Expression of Arabidopsis DREB1C improves survival, growth, and yield of upland New Rice for Africa (NERICA) under drought. Mol. Breed. 31, 255-264. doi: 10.1007/s11032-012-9785-9
27. Ito, Y., Katsura, K., Maruyama, K., Taji, T., Kobayashi, M., Seki, M., et al. (2006). Functional analysis of rice DREB1/CBF-type transcription factors involved in cold-responsive gene expression in transgenic rice. Plant Cell Physiol. 47, 141-153. doi: 10.1093/pcp/pci230
28. Iwaki, T., Guo, L., Ryals, J. A., Yasuda, S., Shimazaki, T., Kikuchi, A., et al. (2013). Metabolic profiling of transgenic potato tubers expressing Arabidopsis dehydration response element-binding protein 1A (DREB1A). J. Agric. Food Chem. 61, 893-900. doi: 10.1021/jf304071n
29. Jensen, M. K., Lindemose, S., de Masi, F., Reimer, J. J., Nielsen, M., Perera, V., et al. (2013). ATAF1 transcription factor directly regulates abscisic acid biosynthetic gene NCED3 in Arabidopsis thaliana. FEBS Open Bio 3, 321-327. doi: 10.1016/j.fob.2013.07.006
30. Jeong, J. S., Kim, Y. S., Baek, K. H., Jung, H., Ha, S. H., Do Choi, Y., et al. (2010). Root-specific expression of OsNAC10 improves drought tolerance and grain yield in rice under field drought conditions. Plant Physiol. 153, 185-197. doi: 10.1104/pp.110.154773
31. Jeong, J. S., Kim, Y. S., Redillas, M. C., Jang, G., Jung, H., Bang, S. W., et al. (2013). OsNAC5 overexpression enlarges root diameter in rice plants leading to enhanced drought tolerance and increased grain yield in the field. Plant Biotechnol. J. 11, 101-114. doi: 10.1111/pbi.12011
32. Kasuga, M., Liu, Q., Miura, S., Yamaguchi-Shinozaki, K., and Shinozaki, K. (1999). Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat. Biotechnol. 17, 287-291. doi: 10.1038/7036
33. Kasuga, M., Miura, S., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2004). A combination of the Arabidopsis DREB1A gene and stress-inducible rd29A promoter improved drought-and low-temperature stress tolerance in tobacco by gene transfer. Plant Cell Physiol. 45, 346-350. doi: 10.1093/pcp/pch037
34. Kim, J. S., Mizoi, J., Yoshida, T., Fujita, Y., Nakajima, J., Ohori, T., et al. (2011). An ABRE promoter sequence is involved in osmotic stress-responsive expression of the DREB2A gene, which encodes a transcription factor regulating drought-inducible genes in Arabidopsis. Plant Cell Physiol. 52, 2136-2146. doi: 10.1093/pcp/pcr143
35. Knox, A. K., Li, C., Vagujfalvi, A., Galiba, G., Stockinger, E. J., and Dubcovsky, J. (2008). Identification of candidate CBF genes for the frost tolerance locus Fr-Am2 in Triticum monococcum. Plant Mol. Biol. 67, 257-270. doi: 10.1007/s11103-008-9316-6
36. Komatsu, K., Suzuki, N., Kuwamura, M., Nishikawa, Y., Nakatani, M., Ohtawa, H., et al. (2013). Group A PP2Cs evolved in land plants as key regulators of intrinsic desiccation tolerance. Nat. Commun. 4, 2219. doi: 10.1038/ncomms3219
37. Lee, S. J., Kang, J. Y., Park, H. J., Kim, M. D., Bae, M. S., Choi, H. I., et al. (2010). DREB2C interacts with ABF2, a bZIP protein regulating abscisic acid-responsive gene expression, and its overexpression affects abscisic acid sensitivity. Plant Physiol. 153, 716-727. doi: 10.1104/pp.110.154617
38. Liu, Q., Kasuga, M., Sakuma, Y., Abe, H., Miura, S., Yamaguchi-Shinozaki, K., et al. (1998). Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought-and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10, 1391-1406. doi: 10.1105/tpc.10.8.1391
39. Liu, S., Wang, X., Wang, H., Xin, H., Yang, X., Yan, J., et al. (2013). Genome-wide analysis of ZmDREB genes and their association with natural variation in drought tolerance at seedling stage of Zea mays L. PLoS Genet. 9:e1003790. doi: 10.1371/journal.pgen.1003790
40. Maruyama, K., Takeda, M., Kidokoro, S., Yamada, K., Sakuma, Y., Urano, K., et al. (2009). Metabolic pathways involved in cold acclimation identified by integrated analysis of metabolites and transcripts regulated by DREB1A and DREB2A. Plant Physiol. 150, 1972-1980. doi: 10.1104/pp.109.135327
41. Maruyama, K., Todaka, D., Mizoi, J., Yoshida, T., Kidokoro, S., Matsukura, S., et al. (2012). Identification of cis-acting promoter elements in cold-and dehydration-induced transcriptional pathways in Arabidopsis, rice, and soybean. DNA Res. 19, 37-49. doi: 10.1093/dnares/dsr040
42. Miyakawa, T., Fujita, Y., Yamaguchi-Shinozaki, K., and Tanokura, M. (2013). Structure and function of abscisic acid receptors. Trends Plant Sci. 18, 259-266. doi: 10.1016/j.tplants.2012.11.002
43. Mizoi, J., Ohori, T., Moriwaki, T., Kidokoro, S., Todaka, D., Maruyama, K., et al. (2013). GmDREB2A;2, a canonical DEHYDRATION-RESPONSIVE ELEMENT-BINDING PROTEIN2-type transcription factor in soybean, is posttranslationally regulated and mediates dehydration-responsive element-dependent gene expression. Plant Physiol. 161, 346-361. doi: 10.1104/pp.112.204875
44. Mizoi, J., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2012). AP2/ERF family transcription factors in plant abiotic stress responses. Biochim. Biophys. Acta 1819, 86-96. doi: 10.1016/j.bbagrm.2011.08.004
45. Nakashima, K., Fujita, Y., Kanamori, N., Katagiri, T., Umezawa, T., Kidokoro, S., et al. (2009a). Three Arabidopsis SnRK2 protein kinases, SRK2D/SnRK2.2, SRK2E/SnRK2.6/OST1 and SRK2I/SnRK2.3, involved in ABA signaling are essential for the control of seed development and dormancy. Plant Cell Physiol. 50, 1345-1363. doi: 10.1093/pcp/pcp083
46. Nakashima, K., Ito, Y., and Yamaguchi-Shinozaki, K. (2009b). Transcriptional regulatory networks in response to abiotic stresses in Arabidopsis and grasses. Plant Physiol. 149, 88-95. doi: 10.1104/pp.108.129791
47. Nakashima, K., Jan, A., Todaka, D., Maruyama, K., Goto, S., Shinozaki, K., et al. (2014). Comparative functional analysis of six drought-responsive promoters in transgenic rice. Planta 239, 47-60. doi: 10.1007/s00425-013-1960-7
48. Nakashima, K., Takasaki, H., Mizoi, J., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2012). NAC transcription factors in plant abiotic stress responses. Biochim. Biophys. Acta 1819, 97-103. doi: 10.1016/j.bbagrm.2011.10.005
49. Nakashima, K., Tran, L. S., Van Nguyen, D., Fujita, M., Maruyama, K., Todaka, D., et al. (2007). Functional analysis of a NAC-type transcription factor OsNAC6 involved in abiotic and biotic stress-responsive gene expression in rice. Plant J. 51, 617-630. doi: 10.1111/j.1365-313X.2007.03168.x
50. Nakashima, K., and Yamaguchi-Shinozaki, K. (2013). ABA signaling in stress-response and seed development. Plant Cell Rep. 32, 959-970. doi: 10.1007/s00299-013-1418-1
51. Narusaka, Y., Nakashima, K., Shinwari, Z. K., Sakuma, Y., Furihata, T., Abe, H., et al. (2003). Interaction between two cis-acting elements, ABRE and DRE, in ABA-dependent expression of Arabidopsis rd29A gene in response to dehydration and high-salinity stresses. Plant J. 34, 137-148. doi: 10.1046/j.1365-313X.2003.01708.x
52. Oh, S. J., Song, S. I., Kim, Y. S., Jang, H. J., Kim, S. Y., Kim, M., et al. (2005). Arabidopsis CBF3/DREB1A and ABF3 in transgenic rice increased tolerance to abiotic stress without stunting growth. Plant Physiol. 138, 341-351. doi: 10.1104/pp.104.059147
53. Pellegrineschi, A., Reynolds, M., Pacheco, M., Brito, R. M., Almeraya, R., Yamaguchi-Shinozaki, K., et al. (2004). Stress-induced expression in wheat of the Arabidopsis thaliana DREB1A gene delays water stress symptoms under greenhouse conditions. Genome 47, 493-500. doi: 10.1139/g03-140
54. Pennisi, E. (2008). Plant genetics. The blue revolution, drop by drop, gene by gene. Science 320, 171-173. doi: 10.1126/science.320.5873.171
55. Pizzio, G. A., Rodriguez, L., Antoni, R., Gonzalez-Guzman, M., Yunta, C., Merilo, E., et al. (2013). The PYL4 A194T mutant uncovers a key role of PYR1-LIKE4/PROTEIN PHOSPHATASE 2CA interaction for abscisic acid signaling and plant drought resistance. Plant Physiol. 163, 441-455. doi: 10.1104/pp.113.224162
56. Polizel, A. M., Medri, M. E., Nakashima, K., Yamanaka, N., Farias, J. R., De Oliveira, M. C., et al. (2011). Molecular, anatomical and physiological properties of a genetically modified soybean line transformed with rd29A:AtDREB1A for the improvement of drought tolerance. Genet. Mol. Res. 10, 3641-3656. doi: 10.4238/2011
57. Qin, F., Sakuma, Y., Tran, L. S., Maruyama, K., Kidokoro, S., Fujita, Y., et al. (2008). Arabidopsis DREB2A-interacting proteins function as RING E3 ligases and negatively regulate plant drought stress-responsive gene expression. Plant Cell 20, 1693-1707. doi: 10.1105/tpc.107.057380
58. Raghavendra, A. S., Gonugunta, V. K., Christmann, A., and Grill, E. (2010). ABA perception and signalling. Trends Plant Sci. 15, 395-401. doi: 10.1016/j.tplants.2010.04.006
59. Rai, M., He, C., and Wu, R. (2009). Comparative functional analysis of three abiotic stress-inducible promoters in transgenic rice. Transgenic Res. 18, 787-799. doi: 10.1007/s11248-009-9263-2
60. Redillas, M. C., Jeong, J. S., Kim, Y. S., Jung, H., Bang, S. W., Choi, Y. D., et al. (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, 792-805. doi: 10.1111/j.1467-7652.2012.00697.x
61. Rusconi, F., Simeoni, F., Francia, P., Cominelli, E., Conti, L., Riboni, M., et al. (2013). The Arabidopsis thaliana MYB60 promoter provides a tool for the spatio-temporal control of gene expression in stomatal guard cells. J. Exp. Bot. 64, 3361-3371. doi: 10.1093/jxb/ert180
62. Saint Pierre, C., Crossa, J. L., Bonnett, D., Yamaguchi-Shinozaki, K., and Reynolds, M. P. (2012). Phenotyping transgenic wheat for drought resistance. J. Exp. Bot. 63, 1799-1808. doi: 10.1093/jxb/err385
63. Sakuma, Y., Maruyama, K., Osakabe, Y., Qin, F., Seki, M., Shinozaki, K., et al. (2006a). Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in drought-responsive gene expression. Plant Cell 18, 1292-1309. doi: 10.1105/tpc.105.035881
64. Sakuma, Y., Maruyama, K., Qin, F., Osakabe, Y., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2006b). Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stress-responsive gene expression. Proc. Natl. Acad. Sci. U.S.A. 103, 18822-18827. doi: 10.1073/pnas.0605639103
65. Swamy, B. P. M., Ahmed, H. U., Henry, A., Mauleon, R., Dixit, S., Vikram, P., et al. (2013). Genetic, physiological, and gene expression analyses reveal that multiple QTL enhance yield of rice mega-variety IR64 under drought. PLoS ONE 8:e62795. doi: 10.1371/journal.pone.0062795
66. Takasaki, H., Maruyama, K., Kidokoro, S., Ito, Y., Fujita, Y., Shinozaki, K., et al. (2010). The abiotic stress-responsive NAC-type transcription factor OsNAC5 regulates stress-inducible genes and stress tolerance in rice. Mol. Genet. Genomics 284, 173-183. doi: 10.1007/s00438-010-0557-0
67. Tran, L. S., Nakashima, K., Sakuma, Y., Simpson, S. D., Fujita, Y., Maruyama, K., et al. (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. Plant Cell 16, 2481-2498. doi: 10.1105/tpc.104.022699
68. Uga, Y., Sugimoto, K., Ogawa, S., Rane, J., Ishitani, M., Hara, N., et al. (2013). Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions. Nat. Genet. 45, 1097-1102. doi: 10.1038/ng.2725
69. Umezawa, T., Nakashima, K., Miyakawa, T., Kuromori, T., Tanokura, M., Shinozaki, K., et al. (2010). Molecular basis of the core regulatory network in ABA responses: sensing, signaling and transport. Plant Cell Physiol. 51, 1821-1839. doi: 10.1093/pcp/pcq156
70. Umezawa, T., Sugiyama, N., Takahashi, F., Anderson, J. C., Ishihama, Y., Peck, S. C., et al. (2013). Genetics and phosphoproteomics reveal a protein phosphorylation network in the abscisic acid signaling pathway in Arabidopsis thaliana. Sci. Signal. 6:rs8. doi: 10.1126/scisignal.2003509
71. Vágújfalvi, A., Galiba, G., Cattivelli, L., and Dubcovsky, J. (2003). The cold-regulated transcriptional activator Cbf3 is linked to the frost-tolerance locus Fr-A2 on wheat chromosome 5A. Mol. Genet. Genomics 269, 60-67. doi: 10.1007/s00438-003-0806-6
72. Weiner, J. J., Peterson, F. C., Volkman, B. F., and Cutler, S. R. (2010). Structural and functional insights into core ABA signaling. Curr. Opin. Plant Biol. 13, 495-502. doi: 10.1016/j.pbi.2010.09.007
73. Wu, X., Shiroto, Y., Kishitani, S., Ito, Y., and Toriyama, K. (2009). Enhanced heat and drought tolerance in transgenic rice seedlings overexpressing OsWRKY11 under the control of HSP101 promoter. Plant Cell Rep. 28, 21-30. doi: 10.1007/s00299-008-0614-x
74. Xiao, B. Z., Chen, X., Xiang, C. B., Tang, N., Zhang, Q. F., and Xiong, L. Z. (2009). Evaluation of seven function-known candidate genes for their effects on improving drought resistance of transgenic rice under field conditions. Mol. Plant 2, 73-83. doi: 10.1093/mp/ssn068
75. Xu, Z. Y., Kim, S. Y., Hyeon Do, Y., Kim, D. H., Dong, T., Park, Y., et al. (2013). The Arabidopsis NAC transcription factor ANAC096 cooperates with bZIP-type transcription factors in dehydration and osmotic stress responses. Plant Cell 25, 4708-4724. doi: 10.1105/tpc.113.119099
76. Yamaguchi-Shinozaki, K., and Shinozaki, K. (2006). Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu. Rev. Plant Biol. 57, 781-803. doi: 10.1146/annurev.arplant.57.032905.105444
77. Yang, M., and Xiong, L. (2011). Isolation and characterization of a drought-inducible promoter Oshox24P in rice. J. Huazhong Agric. Univ. 30, 525-531.
78. Yi, N., Kim, Y. S., Jeong, M. H., Oh, S. J., Jeong, J. S., Park, S. H., et al. (2010). Functional analysis of six drought-inducible promoters in transgenic rice plants throughout all stages of plant growth. Planta 232, 743-754. doi: 10.1007/s00425-010-1212-z
79. Yoshida, T., Fujita, Y., Sayama, H., Kidokoro, S., Maruyama, K., Mizoi, J., et al. (2010). AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation. Plant J. 61, 672-685. doi: 10.1111/j.1365-313X.2009.04092.x