OsRMC, a negative regulator of salt stress response in rice, is regulated by two AP2/ERF transcription factors

Plant Molecular Biology

Volumn 82, Issue 4-5, 2013, Pages 439-455

  Serra, Tânia S ^a,b   Figueiredo, Duarte D ^a,b   Cordeiro, André M ^a,b   Almeida, Diego M ^a,b   Lourenço, Tiago ^a,b   Abreu, Isabel A ^a,b   Sebastián, Alvaro ^c   Fernandes, Lisete ^d,e   Contreras Moreira, Bruno ^c,f   Oliveira, M Margarida ^a,b   Saibo, Nelson J M ^a,b  

^a INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

^b INSTITUTO DE BIOLOGIA EXPERIMENTAL E TECNOLÓGICA   (Portugal)

^c CSIC   (Spain)

^d INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

^e INSTITUTO POLITÉCNICO DE LISBOA   (Portugal)

^f FUNDACIÓN ARAID   (Spain)

Author keywords

ABA; Abiotic stress; Adverse environmental conditions; Cold; Drought; EMSA; EREBP; High salinity; Phosphorylation; Transcriptional regulation; Yeast one hybrid

Indexed keywords

ABSCISIC ACID; SODIUM CHLORIDE; TRANSCRIPTION FACTOR AP 2; VEGETABLE PROTEIN;

ARTICLE; DROUGHT; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; RICE;

ABSCISIC ACID; DROUGHTS; GENE EXPRESSION REGULATION, PLANT; ORYZA SATIVA; PLANT PROTEINS; SODIUM CHLORIDE; TRANSCRIPTION FACTOR AP-2;

EID: 84879163041     PISSN: 01674412     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11103-013-0073-9     Document Type: Article

References (78)

1. Agarwal PK, Jha B (2010) Transcription factors in plants and ABA dependent and independent abiotic stress signalling. Biol Plant 54(2): 201-212. doi: 10. 1007/s10535-010-0038-7.
2. Allen MD, Yamasaki K, Ohme-Takagi M, Tateno M, Suzuki M (1998) 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 17(18): 5484-5496. doi: 10. 1093/emboj/17. 18. 5484.
3. Anthony RG, Henriques R, Helfer A, Meszaros T, Rios G, Testerink C, Munnik T, Deak M, Koncz C, Bogre L (2004) A protein kinase target of a PDK1 signalling pathway is involved in root hair growth in Arabidopsis. EMBO J 23(3): 572-581. doi: 10. 1038/sj. emboj. 7600068.
4. Bossi F, Cordoba E, Dupre P, Mendoza MS, Roman CS, Leon P (2009) The Arabidopsis ABA-INSENSITIVE (ABI) 4 factor acts as a central transcription activator of the expression of its own gene, and for the induction of ABI5 and SBE2. 2 genes during sugar signaling. Plant J 59(3): 359-374. doi: 10. 1111/j. 1365-313X. 2009. 03877. x.
5. Cao YF, Wu YF, Zheng Z, Song FM (2005) Overexpression of the rice EREBP-like gene OsBIERF3 enhances disease resistance and salt tolerance in transgenic tobacco. Physiol Mol Plant P 67(3-5): 202-211. doi: 10. 1016/j. pmpp. 2006. 01. 004.
6. Cao Y, Song F, Goodman RM, Zheng Z (2006) Molecular characterization of four rice genes encoding ethylene-responsive transcriptional factors and their expressions in response to biotic and abiotic stress. J Plant Physiol 163(11): 1167-1178. doi: 10. 1016/j. jplph. 2005. 11. 004.
7. Chao DY, Luo YH, Shi M, Luo D, Lin HX (2005) Salt-responsive genes in rice revealed by cDNA microarray analysis. Cell Res 15(10): 796-810. doi: 10. 1038/sj. cr. 7290349.
8. Chen Z (2001) A superfamily of proteins with novel cysteine-rich repeats. Plant Physiol 126(2): 473-476. doi: 10. 1104/pp. 126. 2. 473.
9. Cheng C, Yun KY, Ressom HW, Mohanty B, Bajic VB, Jia Y, Yun SJ, de los Reyes BG (2007) An early response regulatory cluster induced by low temperature and hydrogen peroxide in seedlings of chilling-tolerant japonica rice. BMC Genomics 8: 175. doi: 10. 1186/1471-2164-8-175.
10. Cheong YH, Moon BC, Kim JK, Kim CY, Kim MC, Kim IH, Park CY, Kim JC, Park BO, Koo SC, Yoon HW, Chung WS, Lim CO, Lee SY, Cho MJ (2003) BWMK1, a rice mitogen-activated protein kinase, locates in the nucleus and mediates pathogenesis-related gene expression by activation of a transcription factor. Plant Physiol 132(4): 1961-1972. doi: 10. 1104/pp. 103. 023176.
11. Chung S, Parish RW (2008) Combinatorial interactions of multiple cis-elements regulating the induction of the Arabidopsis XERO2 dehydrin gene by abscisic acid and cold. Plant J 54(1): 15-29. doi: 10. 1111/j. 1365-313X. 2007. 03399. x.
12. Contreras-Moreira B (2010) 3D-footprint: a database for the structural analysis of protein-DNA complexes. Nucleic Acids Res 38(Database issue): D91-D97. doi: 10. 1093/nar/gkp781.
13. Cotsaftis O, Plett D, Johnson AA, Walia H, Wilson C, Ismail AM, Close TJ, Tester M, Baumann U (2011) Root-specific transcript profiling of contrasting rice genotypes in response to salinity stress. Mol Plant 4(1): 25-41. doi: 10. 1093/mp/ssq056ssq056.
14. + exclusion in rice explained by 3D modeling of HKT transporters and alternative splicing. PLoS ONE 7(7): e39865. doi: 10. 1371/journal. pone. 0039865.
15. Cutcliffe JW, Hellmann E, Heyl A, Rashotte AM (2011) CRFs form protein-protein interactions with each other and with members of the cytokinin signalling pathway in Arabidopsis via the CRF domain. J Exp Bot 62(14): 4995-5002. doi: 10. 1093/jxb/err199.
16. Dietz KJ, Vogel MO, Viehhauser A (2010) AP2/EREBP transcription factors are part of gene regulatory networks and integrate metabolic, hormonal and environmental signals in stress acclimation and retrograde signalling. Protoplasma 245(1-4): 3-14. doi: 10. 1007/s00709-010-0142-8.
17. Dixit R, Nasrallah ME, Nasrallah JB (2000) Post-transcriptional maturation of the S receptor kinase of Brassica correlates with co-expression of the S-locus glycoprotein in the stigmas of two Brassica strains and in transgenic tobacco plants. Plant Physiol 124(1): 297-311. doi: 10. 1104/pp. 124. 1. 297.
18. Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L (2010) MYB transcription factors in Arabidopsis. Trends Plant Sci 15(10): 573-581. doi: 10. 1016/j. tplants. 2010. 06. 005.
19. Figueiredo DD, Barros PM, Cordeiro AM, Serra TS, Lourenco T, Chander S, Oliveira MM, Saibo NJ (2012) Seven zinc-finger transcription factors are novel regulators of the stress responsive gene OsDREB1B. J Exp Bot 63(10): 3643-3656. doi: 10. 1093/jxb/ers035.
20. Fujimoto SY, Ohta M, Usui A, Shinshi H, Ohme-Takagi M (2000) Arabidopsis ethylene-responsive element binding factors act as transcriptional activators or repressors of GCC box-mediated gene expression. Plant Cell 12(3): 393-404. doi: 10. 2307/3870944.
21. Garvie CW, Wolberger C (2001) Recognition of specific DNA sequences. Mol Cell 8(5): 937-946. doi: 10. 1016/S1097-2765(01)00392-6.
22. Gutterson N, Reuber TL (2004) Regulation of disease resistance pathways by AP2/ERF transcription factors. Curr Opin Plant Biol 7(4): 465-471. doi: 10. 1016/j. pbi. 2004. 04. 007.
23. Ham BK, Park JM, Lee SB, Kim MJ, Lee IJ, Kim KJ, Kwon CS, Paek KH (2006) Tobacco Tsip1, a DnaJ-type Zn finger protein, is recruited to and potentiates Tsi1-mediated transcriptional activation. Plant Cell 18(8): 2005-2020. doi: 10. 1105/tpc. 106. 043158.
24. Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Ann Rev Plant Physiol Plant Mol Biol 51: 463-499. doi: 10. 1146/annurev. arplant. 51. 1. 463.
25. Hauser F, Horie T (2010) A conserved primary salt tolerance mechanism mediated by HKT transporters: a mechanism for sodium exclusion and maintenance of high K(+)/Na(+) ratio in leaves during salinity stress. Plant, Cell Environ 33(4): 552-565. doi: 10. 1111/j. 1365-3040. 2009. 02056. x.
26. Hu XJ, Zhang ZB, Xu P, Fu ZY, Hu SB, Song WY (2010) Multifunctional genes: the cross-talk among the regulation networks of abiotic stress responses. Biol Plant 54(2): 213-223. doi: 10. 1007/s10535-010-0039-6.
27. Huang Z, Zhang Z, Zhang X, Zhang H, Huang D, Huang R (2004) Tomato TERF1 modulates ethylene response and enhances osmotic stress tolerance by activating expression of downstream genes. FEBS Lett 573(1-3): 110-116. doi: 10. 1016/j. febslet. 2004. 07. 064.
28. Jeong S, Trotochaud AE, Clark SE (1999) The Arabidopsis CLAVATA2 gene encodes a receptor-like protein required for the stability of the CLAVATA1 receptor-like kinase. Plant Cell 11(10): 1925-1934. doi: 10. 2307/3871087.
29. Jiang J, Li J, Xu Y, Han Y, Bai Y, Zhou G, Lou Y, Xu Z, Chong K (2007) RNAi knockdown of Oryza sativaroot meander curling gene led to altered root development and coiling which were mediated by jasmonic acid signalling in rice. Plant, Cell Environ 30(6): 690-699. doi: 10. 1111/j. 1365-3040. 2007. 01663. x.
30. Kachroo A, Nasrallah ME, Nasrallah JB (2002) Self-incompatibility in the Brassicaceae: receptor-ligand signaling and cell-to-cell communication. Plant Cell 14: S227-S238. doi: 10. 1105/tpc. 010440.
31. Kader MA, Lindberg S (2005) Uptake of sodium in protoplasts of salt-sensitive and salt-tolerant cultivars of rice, Oryza sativa L. determined by the fluorescent dye SBFI. J Exp Bot 56(422): 3149-3158. doi: 10. 1093/jxb/eri312.
32. Kader MA, Seidel T, Golldack D, Lindberg S (2006) Expressions of OsHKT1, OsHKT2, and OsVHA are differentially regulated under NaCl stress in salt-sensitive and salt-tolerant rice (Oryza sativa L.) cultivars. J Exp Bot 57(15): 4257-4268. doi: 10. 1093/jxb/erl199.
33. Kazan K (2006) Negative regulation of defence and stress genes by EAR-motif-containing repressors. Trends Plant Sci 11(3): 109-112. doi: 10. 1016/j. tplants. 2006. 01. 004.
34. Kumari S, Sabharwal VP, Kushwaha HR, Sopory SK, Singla-Pareek SL, Pareek A (2009) Transcriptome map for seedling stage specific salinity stress response indicates a specific set of genes as candidate for saline tolerance in Oryza sativa L. Funct Integr Genomics 9(1): 109-123. doi: 10. 1007/s10142-008-0088-5.
35. Lee KS, Choi WY, Ko JC, Kim TS, Gregorio GB (2003) Salinity tolerance of japonica and indica rice (Oryza sativa L.) at the seedling stage. Planta 216(6): 1043-1046. doi: 10. 1007/s00425-002-0958-3.
36. Liu F, Xu W, Wei Q, Zhang Z, Xing Z, Tan L, Di C, Yao D, Wang C, Tan Y, Yan H, Ling Y, Sun C, Xue Y, Su Z (2010) Gene expression profiles deciphering rice phenotypic variation between Nipponbare (Japonica) and 93-11 (Indica) during oxidative stress. PLoS ONE 5(1): e8632. doi: 10. 1371/journal. pone. 0008632.
37. Mena M, Cejudo FJ, Isabel-Lamoneda I, Carbonero P (2002) A role for the DOF transcription factor BPBF in the regulation of gibberellin-responsive genes in barley aleurone. Plant Physiol 130(1): 111-119. doi: 10. 1104/pp. 005561.
38. Mito T, Seki M, Shinozaki K, Ohme-Takagi M, Matsui K (2011) Generation of chimeric repressors that confer salt tolerance in Arabidopsis and rice. Plant Biotechnol J 9(7): 736-746. doi: 10. 1111/j. 1467-7652. 2010. 00578. x.
39. Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) AP2/ERF family transcription factors in plant abiotic stress responses. Biochim Biophys Acta 1819(2): 86-96. doi: 10. 1016/j. bbagrm. 2011. 08. 004.
40. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59: 651-681. doi: 10. 1146/annurev. arplant. 59. 032607. 092911.
41. Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol 140(2): 411-432. doi: 10. 1104/pp. 105. 073783.
42. Negrão S, Courtois B, Ahmadi N, Abreu I, Saibo N, Oliveira MM (2011) Recent updates on salinity stress in rice: from physiological to molecular responses. Crit Rev Plant Sci 30(4): 329-377. doi: 10. 1080/07352689. 2011. 587725.
43. Negrão S, Almadanim MC, Pires IS, Abreu IA, Maroco J, Courtois B, Gregorio GB, McNally KL, Oliveira MM (2013) New allelic variants found in key rice salt-tolerance genes: an association study. Plant Biotechnol J 11(1): 87-100. doi: 10. 1111/pbi. 12010.
44. Okamuro JK, Caster B, Villarroel R, van Montagu M, Jofuku KD (1997) The AP2 domain of APETALA2 defines a large new family of DNA binding proteins in Arabidopsis. Proc Natl Acad Sci USA 94(13): 7076-7081. doi: 10. 1073/pnas. 94. 13. 7076.
45. Ouwerkerk PBF, Meijer AH (2001) Yeast One-Hybrid screening for DNA-protein interactions. Curr Protoc Mol Biol 12. 12. 11-12. 12. 22. doi: 10. 1002/0471142727. mb1212s55.
46. Pardo JM (2010) Biotechnology of water and salinity stress tolerance. Curr Opin Biotechnol 21(2): 185-196. doi: 10. 1016/j. copbio. 2010. 02. 005.
47. Park JM, Park CJ, Lee SB, Ham BK, Shin R, Paek KH (2001) Overexpression of the tobacco Tsi1 gene encoding an EREBP/AP2-type transcription factor enhances resistance against pathogen attack and osmotic stress in tobacco. Plant Cell 13(5): 1035-1046. doi: 10. 2307/3871362.
48. Rabbani MA, Maruyama K, Abe H, Khan MA, Katsura K, Ito Y, Yoshiwara K, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Monitoring expression profiles of rice genes under cold, drought, and high-salinity stresses and abscisic acid application using cDNA microarray and RNA gel-blot analyses. Plant Physiol 133(4): 1755-1767. doi: 10. 1104/pp. 103. 025742.
49. Rojo E, Sharma VK, Kovaleva V, Raikhel NV, Fletcher JC (2002) CLV3 is localized to the extracellular space, where it activates the Arabidopsis CLAVATA stem cell signaling pathway. Plant Cell 14(5): 969-977. doi: 10. 1105/tpc. 002196.
50. RoyChoudhury A, Gupta B, Sengupta DN (2008) Trans-acting factor designated OSBZ8 interacts with both typical abscisic acid responsive elements as well as abscisic acid responsive element-like sequences in the vegetative tissues of indica rice cultivars. Plant Cell Rep 27(4): 779-794. doi: 10. 1007/s00299-007-0498-1.
51. Sahi C, Singh A, Blumwald E, Grover A (2006) Beyond osmolytes and transporters: novel plant salt-stress tolerance-related genes from transcriptional profiling data. Physiol Plant 127(1): 1-9. doi: 10. 1111/j. 1399-3054. 2005. 00610. x.
52. Saibo NJ, Lourenco T, Oliveira MM (2009) Transcription factors and regulation of photosynthetic and related metabolism under environmental stresses. Ann Bot 103(4): 609-623. doi: 10. 1093/aob/mcn227.
53. Sattelmacher B (2001) The apoplast and its significance for plant mineral nutrition. New Phytol 149(2): 167-192. doi: 10. 1046/j. 1469-8137. 2001. 00034. x.
54. Shao HB, Guo QJ, Chu LY, Zhao XN, Su ZL, Hu YC, Cheng JF (2007) Understanding molecular mechanism of higher plant plasticity under abiotic stress. Colloids Surf B 54(1): 37-45. doi: 10. 1016/j. colsurfb. 2006. 07. 002.
55. Steffens NO, Galuschka C, Schindler M, Bulow L, Hehl R (2004) AthaMap: an online resource for in silico transcription factor binding sites in the Arabidopsis thaliana genome. Nucleic Acids Res 32(Database issue): D368-D372. doi: 10. 1093/nar/gkh017.
56. Takasaki H, Maruyama K, Kidokoro S, Ito Y, Fujita Y, Shinozaki K, Yamaguchi-Shinozaki K, Nakashima K (2010) The abiotic stress-responsive NAC-type transcription factor OsNAC5 regulates stress-inducible genes and stress tolerance in rice. Mol Genet Genomics 284(3): 173-183. doi: 10. 1007/s00438-010-0557-0.
57. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4. 0. Mol Biol Evol 24(8): 1596-1599. doi: 10. 1093/molbev/msm092.
58. Tang W, Ezcurra I, Muschietti J, McCormick S (2002) A cysteine-rich extracellular protein, LAT52, interacts with the extracellular domain of the pollen receptor kinase LePRK2. Plant Cell 14(9): 2277-2287. doi: 10. 1105/tpc. 003103.
59. + transport in higher plants. Ann Bot 91(5): 503-527. doi: 10. 1093/aob/mcg058.
60. Tieman DM, Taylor MG, Ciardi JA, Klee HJ (2000) The tomato ethylene receptors NR and LeETR4 are negative regulators of ethylene response and exhibit functional compensation within a multigene family. Proc Natl Acad Sci USA 97(10): 5663-5668. doi: 10. 1073/pnas. 090550597.
61. Tran LS, Urao T, Qin F, Maruyama K, Kakimoto T, Shinozaki K, Yamaguchi-Shinozaki K (2007) Functional analysis of AHK1/ATHK1 and cytokinin receptor histidine kinases in response to abscisic acid, drought, and salt stress in Arabidopsis. Proc Natl Acad Sci USA 104(51): 20623-20628. doi: 10. 1073/pnas. 0706547105.
62. Turatsinze JV, Thomas-Chollier M, Defrance M, van Helden J (2008) Using RSAT to scan genome sequences for transcription factor binding sites and cis-regulatory modules. Nat Protoc 3(10): 1578-1588. doi: 10. 1038/nprot. 2008. 97.
63. Walia H, Wilson C, Condamine P, Liu X, Ismail AM, Zeng L, Wanamaker SI, Mandal J, Xu J, Cui X, Close TJ (2005) Comparative transcriptional profiling of two contrasting rice genotypes under salinity stress during the vegetative growth stage. Plant Physiol 139(2): 822-835. doi: 10. 1104/pp. 105. 065961.
64. Walia H, Wilson C, Zeng L, Ismail AM, Condamine P, Close TJ (2007) Genome-wide transcriptional analysis of salinity stressed japonica and indica rice genotypes during panicle initiation stage. Plant Mol Biol 63(5): 609-623. doi: 10. 1007/s11103-006-9112-0.
65. Wang H, Huang Z, Chen Q, Zhang Z, Zhang H, Wu Y, Huang D, Huang R (2004) Ectopic overexpression of tomato JERF3 in tobacco activates downstream gene expression and enhances salt tolerance. Plant Mol Biol 55(2): 183-192. doi: 10. 1007/s11103-004-0113-6.
66. Wang D, Pan Y, Zhao X, Zhu L, Fu B, Li Z (2011) Genome-wide temporal-spatial gene expression profiling of drought responsiveness in rice. BMC Genomics 12: 149. doi: 10. 1186/1471-2164-12-149.
67. Wankhade SD, Bahaji A, Mateu-Andres I, Cornejo MJ (2010) Phenotypic indicators of NaCl tolerance levels in rice seedlings: variations in development and leaf anatomy. Acta Physiologiae Plantarum 32(6): 1161-1169. doi: 10. 1007/s11738-010-0511-0.
68. Wen JQ, Oono K, Imai R (2002) Two novel mitogen-activated protein signaling components, OsMEK1 and OsMAP1, are involved in a moderate low-temperature signaling pathway in rice. Plant Physiol 129(4): 1880-1891. doi: 10. 1104/pp. 006072.
69. Wu L, Chen X, Ren H, Zhang Z, Zhang H, Wang J, Wang XC, Huang R (2007) ERF protein JERF1 that transcriptionally modulates the expression of abscisic acid biosynthesis-related gene enhances the tolerance under salinity and cold in tobacco. Planta 226(4): 815-825. doi: 10. 1007/s00425-007-0528-9.
70. Xiong L, Lee H, Ishitani M, Zhu JK (2002) Regulation of osmotic stress-responsive gene expression by the LOS6/ABA1 locus in Arabidopsis. J Biol Chem 277(10): 8588-8596. doi: 10. 1074/jbc. M109275200.
71. Xu ZS, Xia LQ, Chen M, Cheng XG, Zhang RY, Li LC, Zhao YX, Lu Y, Ni ZY, Liu L, Qiu ZG, Ma YZ (2007) Isolation and molecular characterization of the Triticum aestivum L. ethylene-responsive factor 1 (TaERF1) that increases multiple stress tolerance. Plant Mol Biol 65(6): 719-732. doi: 10. 1007/s11103-007-9237-9.
72. Yamaguchi-Shinozaki K, Shinozaki K (2005) Organization of cis-acting regulatory elements in osmotic- and cold-stress-responsive promoters. Trends Plant Sci 10(2): 88-94. doi: 10. 1016/j. tplants. 2004. 12. 012.
73. Yoshida S, Foorno DA, Cock JH, Gomez KA (eds) (1976) Laboratory manual for physiological studies of rice, 3rd edn. International Rice Research Institute, Los Banos.
74. Zarei A, Korbes AP, Younessi P, Montiel G, Champion A, Memelink J (2011) Two GCC boxes and AP2/ERF-domain transcription factor ORA59 in jasmonate/ethylene-mediated activation of the PDF1. 2 promoter in Arabidopsis. Plant Mol Biol 75(4-5): 321-331. doi: 10. 1007/s11103-010-9728-y.
75. Zhang H, Huang Z, Xie B, Chen Q, Tian X, Zhang X, Lu X, Huang D, Huang R (2004) The ethylene-, jasmonate-, abscisic acid- and NaCl-responsive tomato transcription factor JERF1 modulates expression of GCC box-containing genes and salt tolerance in tobacco. Planta 220(2): 262-270. doi: 10. 1007/s00425-004-1347-x.
76. Zhang L, Tian LH, Zhao JF, Song Y, Zhang CJ, Guo Y (2009a) Identification of an apoplastic protein involved in the initial phase of salt stress response in rice root by two-dimensional electrophoresis. Plant Physiol 149(2): 916-928. doi: 10. 1104/pp. 108. 131144.
77. Zhang Y, Chen C, Jin XF, Xiong AS, Peng RH, Hong YH, Yao QH, Chen JM (2009b) Expression of a rice DREB1 gene, OsDREB1D, enhances cold and high-salt tolerance in transgenic Arabidopsis. Bmb Rep 42(8): 486-492. doi: 10. 5483/BMBRep. 2009. 42. 8. 486.
78. Zhao LF, Xu SB, Chai TY, Wang T (2006) OsAP2-1, an AP2-like gene from Oryza sativa, is required for flower development and male fertility. Sex Plant Reprod 19(4): 197-206. doi: 10. 1007/s00497-006-0036-2.