A dominant repressor version of the tomato Sl-ERF.B3 gene confers ethylene hypersensitivity via feedback regulation of ethylene signaling and response components

Plant Journal

Volumn 76, Issue 3, 2013, Pages 406-419

  Liu, Mingchun ^a,b   Pirrello, Julien ^a,b   Kesari, Ravi ^a,b   Mila, Isabelle ^a,b   Roustan, Jean Paul ^a,b   Li, Zhengguo ^c   Latché, Alain ^a,b   Pech, Jean Claude ^a,b   Bouzayen, Mondher ^a,b   Regad, Farid ^a,b  

^a GRENOBLE INSTITUTE OF TECHNOLOGY   (France)

^b Centre National de la Recherche Scientifique   (France)

^c CHONGQING UNIVERSITY   (China)

Author keywords

dominant repressor; ethylene; ethylene response factor; hormone signaling; tomato (Solanum lycopersicum)

Indexed keywords

DOMINANT REPRESSOR; DOWNSTREAM COMPONENTS; ETHYLENE BIOSYNTHESIS; ETHYLENE RESPONSE FACTOR; FUNCTIONAL REDUNDANCY; HORMONE SIGNALING; SIGNAL TRANSDUCTION PATHWAYS; SOLANUM LYCOPERSICUM;

BINDING ENERGY; FRUITS; GAS EMISSIONS; GENES; NUCLEOTIDES; PLANTS (BOTANY); TRANSCRIPTION;

ETHYLENE;

LYCOPERSICON ESCULENTUM;

CELL SURFACE RECEPTOR; ETHYLENE; ETHYLENE DERIVATIVE; ETHYLENE RECEPTORS, PLANT; REPRESSOR PROTEIN; VEGETABLE PROTEIN;

ARTICLE; BIOSYNTHESIS; DOMINANT REPRESSOR; ETHYLENE RESPONSE FACTOR; GENE EXPRESSION REGULATION; GENETICS; HORMONE SIGNALING; METABOLISM; PHENOTYPE; PLEIOTROPY; SEEDLING; SIGNAL TRANSDUCTION; TOMATO; TOMATO (SOLANUM LYCOPERSICUM); TRANSGENIC PLANT;

DOMINANT REPRESSOR; ETHYLENE; ETHYLENE RESPONSE FACTOR; HORMONE SIGNALING; TOMATO (SOLANUM LYCOPERSICUM);

ETHYLENES; GENE EXPRESSION REGULATION, PLANT; GENETIC PLEIOTROPY; LYCOPERSICON ESCULENTUM; PHENOTYPE; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; RECEPTORS, CELL SURFACE; REPRESSOR PROTEINS; SEEDLING; SIGNAL TRANSDUCTION;

EID: 84885673745     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12305     Document Type: Article

References (52)

1. Achard, P., Baghour, M., Chapple, A., Hedden, P., Van Der Straeten, D., Genschik, P., Moritz, T., and, Harberd, N.P., (2007) The plant stress hormone ethylene controls floral transition via DELLA-dependent regulation of floral meristem-identity genes. Proc. Natl Acad. Sci. USA, 104, 6484-6489.
2. Allen, M.D., Yamasaki, K., Ohme-Takagi, M., Tateno, M., and, 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, 5484-5496.
3. Alonso, J.M., Stepanova, A.N., Leisse, T.J., et al. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science, 301, 653-657.
4. Benavente, L.M., and, Alonso, J.M., (2006) Molecular mechanisms of ethylene signaling in Arabidopsis. Mol. BioSyst. 2, 165-173.
5. Berrocal-Lobo, M., Molina, A., and, Solano, R., (2002) Constitutive expression of ETHYLENE-RESPONSE-FACTOR1 in Arabidopsis confers resistance to several necrotrophic fungi. Plant J. 29, 23-32.
6. Bleecker, A.B., and, Kende, H., (2000) Ethylene: a gaseous signal molecule in plants. Annu. Rev. Cell Dev. Biol. 16, 1-18.
7. Brown, R.L., Kazan, K., McGrath, K.C., Maclean, D.J., and, Manners, J.M., (2003) A role for the GCC-box in jasmonate-mediated activation of the PDF1.2 gene of Arabidopsis. Plant Physiol. 132, 1020-1032.
8. Chakravarthy, S., Tuori, R.P., D'Ascenzo, M.D., Fobert, P.R., Despres, C., and, Martin, G.B., (2003) The tomato transcription factor Pti4 regulates defense-related gene expression via GCC box and non-GCC box cis elements. Plant Cell, 15, 3033-3050.
9. Chao, Q., Rothenberg, M., Solano, R., Roman, G., Terzaghi, W., and, Ecker, J.R., (1997) Activation of the ethylene gas response pathway in Arabidopsis by the nuclear protein ETHYLENE-INSENSITIVE3 and related proteins. Cell, 89, 1133-1144.
10. Dubois, M., Skirycz, A., Claeys, H., et al. (2013) Ethylene Response Factor 6 acts as a central regulator of leaf growth under water-limiting conditions in Arabidopsis. Plant Physiol. 162, 319-332.
11. van der Fits, L., and, Memelink, J., (2000) ORCA3, a jasmonate-responsive transcriptional regulator of plant primary and secondary metabolism. Science, 289, 295-297.
12. Fujimoto, S.Y., Ohta, M., Usui, A., Shinshi, H., and, 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, 393-404.
13. Gu, Y.Q., Yang, C., Thara, V.K., Zhou, J., and, Martin, G.B., (2000) Pti4 is induced by ethylene and salicylic acid, and its product is phosphorylated by the Pto kinase. Plant Cell, 12, 771-786.
14. Gu, Y.Q., Wildermuth, M.C., Chakravarthy, S., Loh, Y.T., Yang, C., He, X., Han, Y., and, Martin, G.B., (2002) Tomato transcription factors pti4, pti5, and pti6 activate defense responses when expressed in Arabidopsis. Plant Cell, 14, 817-831.
15. Hall, A.E., and, Bleecker, A.B., (2003) Analysis of combinatorial loss-of-function mutants in the Arabidopsis ethylene receptors reveals that the ers1 etr1 double mutant has severe developmental defects that are EIN2 dependent. Plant Cell, 15, 2032-2041.
16. Hao, D., Yamasaki, K., Sarai, A., and, Ohme-Takagi, M., (2002) Determinants in the sequence specific binding of two plant transcription factors, CBF1 and NtERF2, to the DRE and GCC motifs. Biochemistry, 41, 4202-4208.
17. Heyl, A., Ramireddy, E., Brenner, W.G., Riefler, M., Allemeersch, J., and, Schmülling, T., (2008) The transcriptional repressor ARR1-SRDX suppresses pleiotropic cytokinin activities in Arabidopsis. Plant Physiol. 147, 1380-1395.
18. Hiratsu, K., Matsui, K., Koyama, T., and, Ohme-Takagi, M., (2003) Dominant repression of target genes by chimeric repressors that include the EAR motif, a repression domain, in Arabidopsis. Plant J. 34, 733-739.
19. Hua, J., and, Meyerowitz, E.M., (1998) Ethylene responses are negatively regulated by a receptor gene family in Arabidopsis thaliana. Cell, 94, 261-271.
20. Johnson, P.R., and, Ecker, J.R., (1998) The ethylene gas signal transduction pathway: a molecular perspective. Annu. Rev. Genet. 32, 227-254.
21. Ju, C., Yoon, G.M., Shemansky, J.M., et al. (2012) CTR1 phosphorylates the central regulator EIN2 to control ethylene hormone signaling from the ER membrane to the nucleus in Arabidopsis. Proc. Natl Acad. Sci. USA, 109, 19486-19491.
22. Kevany, B., and, Klee, H., (2007) Changes in ethylene sensitivity by regulated expression of the tomato ethylene receptor family. In Advances in Plant Ethylene Research (, Ramina, A., Chang, C., Giovannoni, J., Klee, H., Perata, P., and, Woltering, E., eds). Netherlands: Springer, pp. 123-128.
23. Kevany, B.M., Tieman, D.M., Taylor, M.G., Cin, V.D., and, Klee, H.J., (2007) Ethylene receptor degradation controls the timing of ripening in tomato fruit. Plant J. 51, 458-467.
24. Kieber, J.J., Rothenberg, M., Roman, G., Feldmann, K.A., and, Ecker, J.R., (1993) CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the raf family of protein kinases. Cell, 72, 427-441.
25. Leclercq, J., Ranty, B., Sanchez-Ballesta, M.-T., et al. (2005) Molecular and biochemical characterization of LeCRK1, a ripening-associated tomato CDPK-related kinase. J. Exp. Bot. 56, 25-35.
26. Lee, J.M., Joung, J.-G., McQuinn, R., Chung, M.-Y., Fei, Z., Tieman, D., Klee, H., and, Giovannoni, J., (2012) Combined transcriptome, genetic diversity and metabolite profiling in tomato fruit reveals that the ethylene response factor SlERF6 plays an important role in ripening and carotenoid accumulation. Plant J. 70, 191-204.
27. Li, Y., Zhu, B., Xu, W., Zhu, H., Chen, A., Xie, Y., Shao, Y., and, Luo, Y., (2007) LeERF1 positively modulated ethylene triple response on etiolated seedling, plant development and fruit ripening and softening in tomato. Plant Cell Rep. 26, 1999-2008.
28. Lin, Z., Zhong, S., and, Grierson, D., (2009) Recent advances in ethylene research. J. Exp. Bot. 60, 3311-3336.
29. Magome, H., Yamaguchi, S., Hanada, A., Kamiya, Y., and, Oda, K., (2004) Dwarf and delayed-flowering 1, a novel Arabidopsis mutant deficient in gibberellin biosynthesis because of over-expression of a putative AP2 transcription factor. Plant J. 37, 720-729.
30. Matsui, K., and, Ohme-Takagi, M., (2010) Detection of protein-protein interactions in plants using the transrepressive activity of the EAR motif repression domain. Plant J. 61, 570-578.
31. Matsui, K., Hiratsu, K., Koyama, T., Tanaka, H., and, Ohme-Takagi, M., (2005) A chimeric AtMYB23 repressor induces hairy roots, elongation of leaves and stems, and inhibition of the deposition of mucilage on seed coats in Arabidopsis. Plant Cell Physiol. 46, 147-155.
32. McGrath, K.C., Dombrecht, B., Manners, J.M., Schenk, P.M., Edgar, C.I., Maclean, D.J., Scheible, W.-R., Udvardi, M.K., and, Kazan, K., (2005) Repressor- and activator-type ethylene response factors functioning in jasmonate signaling and disease resistance identified via a genome-wide screen of Arabidopsis transcription factor gene expression. Plant Physiol. 139, 949-959.
33. Mitsuda, N., Hiratsu, K., Todaka, D., Nakashima, K., Yamaguchi-Shinozaki, K., and, Ohme-Takagi, M., (2006) Efficient production of male and female sterile plants by expression of a chimeric repressor in Arabidopsis and rice. Plant Biotechnol. J. 4, 325-332.
34. Nakano, T., Suzuki, K., Fujimura, T., and, Shinshi, H., (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol. 140, 411-432.
35. Ohme-Takagi, M., and, Shinshi, H., (1995) Ethylene-inducible DNA binding proteins that interact with an ethylene-responsive element. Plant Cell, 7, 173-182.
36. Oñate-Sánchez, L., Anderson, J.P., Young, J., and, Singh, K.B., (2007) AtERF14, a member of the ERF family of transcription factors, plays a nonredundant role in plant defense. Plant Physiol. 143, 400-409.
37. Pan, Y., Seymour, G.B., Lu, C., Hu, Z., Chen, X., and, Chen, G., (2012) An ethylene response factor (ERF5) promoting adaptation to drought and salt tolerance in tomato. Plant Cell Rep. 31, 349-360.
38. Pirrello, J., Jaimes-Miranda, F., Sanchez-Ballesta, M.T., Tournier, B., Khalil-Ahmad, Q., Regad, F., Latché, A., Pech, J.C., and, Bouzayen, M., (2006) Sl-ERF2, a tomato ethylene response factor involved in ethylene response and seed germination. Plant Cell Physiol. 47, 1195-1205.
39. Pirrello, J., Prasad, B.C.N., Zhang, W., et al. (2012) Functional analysis and binding affinity of tomato ethylene response factors provide insight on the molecular bases of plant differential responses to ethylene. BMC Plant Biol. 12, 190.
40. Pré, M., Atallah, M., Champion, A., Vos, M.D., Pieterse, C.M.J., and, Memelink, J., (2008) The AP2/ERF domain transcription factor ORA59 integrates jasmonic acid and ethylene signals in plant defense. Plant Physiol. 147, 1347-1357.
41. Riechmann, J.L., Heard, J., Martin, G., et al. (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science, 290, 2105-2110.
42. Sasaki, K., Mitsuhara, I., Seo, S., Ito, H., Matsui, H., and, Ohashi, Y., (2007) Two novel AP2/ERF domain proteins interact with cis-element VWRE for wound-induced expression of the Tobacco tpoxN1 gene. Plant J. 50, 1079-1092.
43. Solano, R., and, Ecker, J.R., (1998) Ethylene gas: perception, signaling and response. Curr. Opin. Plant Biol. 1, 393-398.
44. Solano, R., Stepanova, A., Chao, Q., and, Ecker, J.R., (1998) Nuclear events in ethylene signaling: a transcriptional cascade mediated by ETHYLENE-INSENSITIVE3 and ETHYLENE-RESPONSE-FACTOR1. Genes Dev. 12, 3703-3714.
45. Tieman, D.M., Taylor, M.G., Ciardi, J.A., and, Klee, H.J., (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, 5663-5668.
46. Tieman, D.M., Ciardi, J.A., Taylor, M.G., and, Klee, H.J., (2001) Members of the tomato LeEIL (EIN3-like) gene family are functionally redundant and regulate ethylene responses throughout plant development. Plant J. 26, 47-58.
47. Tournier, B., Sanchez-Ballesta, M.T., Jones, B., Pesquet, E., Regad, F., Latché, A., Pech, J.-C., and, Bouzayen, M., (2003) New members of the tomato ERF family show specific expression pattern and diverse DNA-binding capacity to the GCC box element. FEBS Lett. 550, 149-154.
48. Trujillo, L.E., Sotolongo, M., Menéndez, C., et al. (2008) SodERF3, a novel sugarcane ethylene responsive factor (ERF), enhances salt and drought tolerance when overexpressed in tobacco plants. Plant Cell Physiol. 49, 512-525.
49. Wang, H., Jones, B., Li, Z., et al. (2005) The tomato Aux/IAA transcription factor IAA9 is involved in fruit development and leaf morphogenesis. Plant Cell, 17, 2676-2692.
50. Wuriyanghan, H., Zhang, B., Cao, W.H., et al. (2009) The ethylene receptor ETR2 delays floral transition and affects starch accumulation in rice. Plant Cell, 21, 1473-1494.
51. Yokotani, N., Tamura, S., Nakano, R., Inaba, A., and, Kubo, Y., (2003) Characterization of a novel tomato EIN3-like gene (LeEIL4). J. Exp. Bot. 54, 2775-2776.
52. Zhang, Z., Zhang, H., Quan, R., Wang, X.-C., and, Huang, R., (2009) Transcriptional regulation of the ethylene response factor LeERF2 in the expression of ethylene biosynthesis genes controls ethylene production in tomato and tobacco. Plant Physiol. 150, 365-377.