Cloning and Expression Analysis of an AP2/ERF Gene and Its Responses to Phytohormones and Abiotic Stresses in Rice

doi:10.1016/S1672-6308(08)60098-0

Abstract

Abstract: Ethylene response factors (ERFs) play important roles in response to plant biotic and abiotic stresses. In this study, a gene encoding a putative AP2/ERF domain-containing protein was isolated by screening a SSH cDNA library from rice and designated as Oryza sativa AP2/ERF-like protein (OsAP2LP) gene. OsAP2LP is 1491 bp in length, interrupted by seven introns, and encodes a putative protein of 348 amino acids. Temporal and spatial expression analysis showed that the OsAP2LP gene was preferentially expressed in roots, panicles, mature embryos and seeds in rice. Real-time quantitative PCR analysis indicated that the expression levels of the OsAP2LP gene were increased under the treatments of drought and gibberellin but decreased under the treatments of low temperature, salt, abscisic acid (ABA) and zeatin. Taken together, these results suggest that OsAP2LP might be involved in stress responses, and probably plays roles as a transcription regulator when plants response to cold, salt and drought stresses through ABA and gibberellin pathways.

Key words: AP2/ERF gene, gene cloning, transcription factor, phytohormone, abiotic stress, rice (Oryza sativa)

MA Hao-li, ZHOU Han-lin, ZHANG Huai-yu, ZHAO Jie. Cloning and Expression Analysis of an AP2/ERF Gene and Its Responses to Phytohormones and Abiotic Stresses in Rice[J]. RICE SCIENCE, 2010, 17(1): 1-9 .

References

1 Reymond P, Farmer E E. Jasmonate and salicylate as global signals for defense gene expression. Curr Opin Plant Biol, 1998, 1: 404–411.
2 Gutterson N, Reuber T L. Regulation of disease resistance pathways by ERF/AP2 transcription factors. Curr Opin Plant Biol, 2004, 7: 465–471.
3 Chen W, Provart N J, Glazebrook J, Katagiri F, Chang H S, Eulgem T, Mauch F, Luan S, Zou G, Whitham S A, Budworth P R, Tao Y, Xie Z, Chen X, Lam S, Kreps J A, Harper J F, Si-Ammour A, Mauch-Mani B, Heinlein M, Kobayashi K, Hohn T, Dangl J L, Wang X, Zhu T. Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses. Plant Cell, 2002, 14: 559–574.
4 Lee J H, Hong J P, Oh S K, Lee S, Choi D, Kim W. The ethylene-responsive factor like protein1 (CaERFLP1) of hot pepper (Capsicum annuum L.) interacts in vitro with both GCC and DRE/CRT sequences with diVerent binding affinities: Possible biological roles of CaERFLP1 in response to pathogen infection and high salinity conditions in transgenic tobacco plants. Plant Mol Biol, 2004, 5: 61–81.
5 Zhu J, Verslues P E, Zheng X, Lee B, Zhan X, Manabe Y, Sokolchik I, Zhu Y, Dong C H, Zhu J K, Hasegawa P M, Bressan R A. HOS10 encodes an R2R3-type MYB transcription factor essential for cold acclimation in plants. Proc Natl Acad Sci USA, 2005, 102: 9966–9971.
6 Nakano T, Suzuki K, Fujimura T, Shinshi H. Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol, 2006, 140: 411–432.
7 Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi- Shinozaki K, Hinozaki K. 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, 1998, 10: 1391–1406.
8 Haake V, Cook D, Riechmann J L, Pineda O, Thomashow M F, Zhang J Z. Transcription factor CBF4 is a regulator of drought adaptation in Arabidopsis. Plant Physiol, 2002, 130: 639–648.
9 Dubouzet J G, Sakuma Y, Ito Y, Kasuga M, Dubouzet E G, Miura S, Seki M, Shinozaki K, Yamaguchi-shinozaki K. OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt- and cold- responsive gene expression. Plant J, 2003, 33: 751–763.
10 Yang H J, Shen H, Chen L, Xing Y Y, Wang Z Y, Zhang J L, Hong M M. The OsEBP-89 gene of rice encodes a putative EREBP transcription factor and is temporally expressed in developing endosperm and intercalary meristem. Plant Mol Biol, 2002, 50: 379–391.
11 Chen J Q, Dong Y, Wang Y J, Liu Q, Zhang J S, Chen S Y. An AP2/EREBP-type transcription-factor gene from rice is cold- inducible and encodes a nuclear-localized protein. Theor Appl Genet, 2003, 107: 972–979.
12 Tian X H, Li X P, Zhou H L, Zhang J S, Gong Z Z, Chen S Y. OsDREB4 genes in rice encode AP2-containing proteins that bind specifically to the dehydration-responsive element. J Integ Plant Biol, 2005, 47: 467–476.
13 Cao Y F, Song F M, Goodman R M, Zheng Z. Molecular characterization of four rice genes encoding ethylene-responsive transcriptional factors and their expressions in response to biotic and abiotic stress. Plant Physiol, 2006, 163: 1167–1178.
14 Zhao L F, Xu S B, Chai T Y, Wang T. OsAP2-1, an AP2-like gene from Oryza sativa, is required for flower development and male fertility. Sex Plant Reprod, 2006, 19: 197–206.
15 Liu J G, Zhang Z, Qin Q L, Peng R H, Xiong A S, Chen J M, Xu F, Zhu H, Yao Q H. Isolated and characterization of a cDNA encoding ethylene-responsive element binding protein (EREBP)/AP2-type protein, RCBF2, in Oryza sativa L. Biotechnol Lett, 2007, 29: 165–173.
16 Kim S, Soltis P S, Wall K, Soltis D E. Phylogeny and domain evolution in the APETALA2-like gene family. Mol Biol Evol, 2006, 23: 107–120.
17 Allen M D, Yamasaki K, Ohme-Takagi M, Tateno M, Suzuki M. A novel mode of DNA recognition by a beta sheet revealed by the solution structure of the GCC-box binding domain in complex with DNA. EMBO J, 1998, 17: 5484– 5496.
18 Sakuma Y, Liu Q, Dubouzet J G, Abe H, Shinozaki K, Yamaguchi-Shinozaki K. DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold-inducible gene expression. Biochem Biophys Res Comm, 2002, 290: 998–1009.
19 Cao Z F, Li J, Chen F, Li Y Q, Zhou H M, Liu Q. Effect of two conserved amino acid residues on DREB1A function. Biochemistry (Mosc), 2001, 66: 623–627.
20 Liu Y, Zhao T J, Liu J M, Liu W Q, Liu Q, Yan Y B, Zhou H M. The conserved Ala37 in the ERF/AP2 domain is essential for binding with the DRE element and the GCC box. FEBS Lett, 2006, 580: 1303–1308.
21 Moose S P, Sisco P H. Glossy15, an APETALA2-like gene from maize that regulates leaf epidermal cell identity. Genes Dev, 1996, 10: 3018–3027.
22 Chuck G, Meeley R B, Hake S. The control of maize spikelet meristem fate by the APETALA2-like gene indeterminate spikelet1. Genes Dev, 1998, 12: 1145–1154.
23 Prestridge D S. SIGNAL SCAN: A computer program that scans DNA sequences for eukaryotic transcriptional elements. CABIOS, 1991, : 03-206.
24 Higo K, Ugawa Y, Iwamoto M, Korenaga T. Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucl Acids Res, 1999, 27: 297–300.
25 Chinnusamy V, Ohta M, Kanrar S, Lee B H, Hong X, Agarwal M, Zhu J K. ICE1: A regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genes Dev, 2003, 17: 1043–1054.
26 Agarwal M, Hao Y, Kapoor A, Dong C H, Fujii H, Zheng X, Zhu J K. A R2R3 type MYB transcription factor is involved in the cold regulation of CBF genes and in acquired freezing tolerance. J Biol Chem, 2006, 281: 37636–37645.
27 Shinozaki K, Yamaguchi-Shinozaki K. Molecular response to dehydration and low temperature: Differences and cross-talk between two stress signaling pathways. Curr Opin Plant Biol, 2000, 3: 217–223.
28 Zhu J K. Salt and drought stress signal transduction in plants. Ann Rev Plant Biol, 2002, 53: 247–273.
29 Robert-Seilaniantz A, Navarro L, Bari R, Jones J D. Pathological hormone imbalances. Curr Opin Plant Biol, 2007, 10: 372– 379.
30 Jain M, Nijhawan A, Arora R, Agarwal P, Ray S, Sharma P, Kapoor S, Tyagi A K, Khurana J P. F-box proteins in rice: Genome-wide analysis, classification, temporal and spatial gene expression during panicle and seed development, and regulation by light and abiotic stress. Plant Physiol, 2007, 143: 1467–1483.
31 Oka A, Sakai H, Iwakoshi S. His-Asp phosphorelay signal transduction in higher plants receptors and response regulators for cytokinin signaling in Arabidopsis thaliana. Genes Genet Syst, 2002, 77: 383–391.
32 Taniguchi M, Sasaki N, Tsuge T, Aoyama T, Oka A. ARR1 directly activates cytokinin response genes that encode proteins with diverse regulatory functions. Plant Cell Physiol, 2007, 48: 263–277.

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