title: Comprehensive Profiling of Ethylene Response Factor Expression Identifies Ripening-Associated ERF Genes and Their Link to Key Regulators of Fruit Ripening in Tomato.
abstract: Our knowledge of the factors mediating ethylene-dependent ripening of climacteric fruit remains limited. The transcription of ethylene-regulated genes is mediated by ethylene response factors (ERFs), but mutants providing information on the specific role of the ERFs in fruit ripening are still lacking, likely due to functional redundancy among this large multigene family of transcription factors. We present here a comprehensive expression profiling of tomato (Solanum lycopersicum) ERFs in wild-type and tomato ripening-impaired tomato mutants (Never-ripe [Nr], ripening-inhibitor [rin], and non-ripening [nor]), indicating that out of the 77 ERFs present in the tomato genome, 27 show enhanced expression at the onset of ripening while 28 display a ripening-associated decrease in expression, suggesting that different ERFs may have contrasting roles in fruit ripening. Among the 19 ERFs exhibiting the most consistent up-regulation during ripening, the expression of 11 ERFs is strongly down-regulated in rin, nor, and Nr tomato ripening mutants, while only three are consistently up-regulated. Members of subclass E, SlERF.E1, SlERF.E2, and SlERF.E4, show dramatic down-regulation in the ripening mutants, suggesting that their expression might be instrumental in fruit ripening. This study illustrates the high complexity of the regulatory network connecting RIN and ERFs and identifies subclass E members as the most active ERFs in ethylene- and RIN/NOR-dependent ripening.
authors.affiliation: Key Laboratory of Bio-Resource and Eco-Environment of the Ministry of Education, College of Life Sciences, State Key Laboratory of Hydraulics and Mountain River Engineering, Sichuan University, Chengdu 610014, China (M.L.);Université de Toulouse, Institut National Polytechnique de Toulouse-Ecole Nationale Supérieure Agronomique, Unité Mixte de Recherche 990 Génomique et Biotechnologie des Fruits, Castanet-Tolosan, F-31326, France (M.L., B.L.G., I.M., P.F., E.M., M.Z., J.-P.R., M.B., J.P.);Institut National de la Recherche Agronomique, Unité Mixte de Recherche 990 Génomique et Biotechnologie des Fruits, Castanet-Tolosan, F-31326, France (M.L., B.L.G., I.M., P.F., E.M., M.Z., J.-P.R., M.B., J.P.);Department of Food and Experimental Nutrition, NAPAN/FoRC Food Research Center, Universidade de São Paulo, School of Pharmaceutical Sciences, 05508-000 Sao Paulo, Sao Paulo, Brazil (B.L.G., E.P.); andDepartamento de Ciências Biológicas, Escola Superior de Agricultura Luiz de Queiroz, Universidade de São Paulo, 13418-900 Piracicaba, Sao Paulo, Brazil (L.E.P.P.) liumingchun1982102@163.com julien.pirrello@ensat.fr.
authors.forename: Mingchun
authors.identifier: http://orcid.org/0000-0001-8004-1758
authors.initials: M
authors.lastname: Liu
authors.affiliation: Key Laboratory of Bio-Resource and Eco-Environment of the Ministry of Education, College of Life Sciences, State Key Laboratory of Hydraulics and Mountain River Engineering, Sichuan University, Chengdu 610014, China (M.L.);Université de Toulouse, Institut National Polytechnique de Toulouse-Ecole Nationale Supérieure Agronomique, Unité Mixte de Recherche 990 Génomique et Biotechnologie des Fruits, Castanet-Tolosan, F-31326, France (M.L., B.L.G., I.M., P.F., E.M., M.Z., J.-P.R., M.B., J.P.);Institut National de la Recherche Agronomique, Unité Mixte de Recherche 990 Génomique et Biotechnologie des Fruits, Castanet-Tolosan, F-31326, France (M.L., B.L.G., I.M., P.F., E.M., M.Z., J.-P.R., M.B., J.P.);Department of Food and Experimental Nutrition, NAPAN/FoRC Food Research Center, Universidade de São Paulo, School of Pharmaceutical Sciences, 05508-000 Sao Paulo, Sao Paulo, Brazil (B.L.G., E.P.); andDepartamento de Ciências Biológicas, Escola Superior de Agricultura Luiz de Queiroz, Universidade de São Paulo, 13418-900 Piracicaba, Sao Paulo, Brazil (L.E.P.P.).
authors.forename: Bruna Lima
authors.initials: BL
authors.lastname: Gomes
authors.affiliation: Key Laboratory of Bio-Resource and Eco-Environment of the Ministry of Education, College of Life Sciences, State Key Laboratory of Hydraulics and Mountain River Engineering, Sichuan University, Chengdu 610014, China (M.L.);Université de Toulouse, Institut National Polytechnique de Toulouse-Ecole Nationale Supérieure Agronomique, Unité Mixte de Recherche 990 Génomique et Biotechnologie des Fruits, Castanet-Tolosan, F-31326, France (M.L., B.L.G., I.M., P.F., E.M., M.Z., J.-P.R., M.B., J.P.);Institut National de la Recherche Agronomique, Unité Mixte de Recherche 990 Génomique et Biotechnologie des Fruits, Castanet-Tolosan, F-31326, France (M.L., B.L.G., I.M., P.F., E.M., M.Z., J.-P.R., M.B., J.P.);Department of Food and Experimental Nutrition, NAPAN/FoRC Food Research Center, Universidade de São Paulo, School of Pharmaceutical Sciences, 05508-000 Sao Paulo, Sao Paulo, Brazil (B.L.G., E.P.); andDepartamento de Ciências Biológicas, Escola Superior de Agricultura Luiz de Queiroz, Universidade de São Paulo, 13418-900 Piracicaba, Sao Paulo, Brazil (L.E.P.P.).
authors.forename: Isabelle
authors.initials: I
authors.lastname: Mila
authors.affiliation: Key Laboratory of Bio-Resource and Eco-Environment of the Ministry of Education, College of Life Sciences, State Key Laboratory of Hydraulics and Mountain River Engineering, Sichuan University, Chengdu 610014, China (M.L.);Université de Toulouse, Institut National Polytechnique de Toulouse-Ecole Nationale Supérieure Agronomique, Unité Mixte de Recherche 990 Génomique et Biotechnologie des Fruits, Castanet-Tolosan, F-31326, France (M.L., B.L.G., I.M., P.F., E.M., M.Z., J.-P.R., M.B., J.P.);Institut National de la Recherche Agronomique, Unité Mixte de Recherche 990 Génomique et Biotechnologie des Fruits, Castanet-Tolosan, F-31326, France (M.L., B.L.G., I.M., P.F., E.M., M.Z., J.-P.R., M.B., J.P.);Department of Food and Experimental Nutrition, NAPAN/FoRC Food Research Center, Universidade de São Paulo, School of Pharmaceutical Sciences, 05508-000 Sao Paulo, Sao Paulo, Brazil (B.L.G., E.P.); andDepartamento de Ciências Biológicas, Escola Superior de Agricultura Luiz de Queiroz, Universidade de São Paulo, 13418-900 Piracicaba, Sao Paulo, Brazil (L.E.P.P.).
authors.forename: Eduardo
authors.identifier: http://orcid.org/0000-0002-7372-1197
authors.initials: E
authors.lastname: Purgatto
authors.affiliation: Key Laboratory of Bio-Resource and Eco-Environment of the Ministry of Education, College of Life Sciences, State Key Laboratory of Hydraulics and Mountain River Engineering, Sichuan University, Chengdu 610014, China (M.L.);Université de Toulouse, Institut National Polytechnique de Toulouse-Ecole Nationale Supérieure Agronomique, Unité Mixte de Recherche 990 Génomique et Biotechnologie des Fruits, Castanet-Tolosan, F-31326, France (M.L., B.L.G., I.M., P.F., E.M., M.Z., J.-P.R., M.B., J.P.);Institut National de la Recherche Agronomique, Unité Mixte de Recherche 990 Génomique et Biotechnologie des Fruits, Castanet-Tolosan, F-31326, France (M.L., B.L.G., I.M., P.F., E.M., M.Z., J.-P.R., M.B., J.P.);Department of Food and Experimental Nutrition, NAPAN/FoRC Food Research Center, Universidade de São Paulo, School of Pharmaceutical Sciences, 05508-000 Sao Paulo, Sao Paulo, Brazil (B.L.G., E.P.); andDepartamento de Ciências Biológicas, Escola Superior de Agricultura Luiz de Queiroz, Universidade de São Paulo, 13418-900 Piracicaba, Sao Paulo, Brazil (L.E.P.P.).
authors.forename: Lázaro E P
authors.identifier: http://orcid.org/0000-0002-8761-5934
authors.initials: LE
authors.lastname: Peres
authors.affiliation: Key Laboratory of Bio-Resource and Eco-Environment of the Ministry of Education, College of Life Sciences, State Key Laboratory of Hydraulics and Mountain River Engineering, Sichuan University, Chengdu 610014, China (M.L.);Université de Toulouse, Institut National Polytechnique de Toulouse-Ecole Nationale Supérieure Agronomique, Unité Mixte de Recherche 990 Génomique et Biotechnologie des Fruits, Castanet-Tolosan, F-31326, France (M.L., B.L.G., I.M., P.F., E.M., M.Z., J.-P.R., M.B., J.P.);Institut National de la Recherche Agronomique, Unité Mixte de Recherche 990 Génomique et Biotechnologie des Fruits, Castanet-Tolosan, F-31326, France (M.L., B.L.G., I.M., P.F., E.M., M.Z., J.-P.R., M.B., J.P.);Department of Food and Experimental Nutrition, NAPAN/FoRC Food Research Center, Universidade de São Paulo, School of Pharmaceutical Sciences, 05508-000 Sao Paulo, Sao Paulo, Brazil (B.L.G., E.P.); andDepartamento de Ciências Biológicas, Escola Superior de Agricultura Luiz de Queiroz, Universidade de São Paulo, 13418-900 Piracicaba, Sao Paulo, Brazil (L.E.P.P.).
authors.forename: Pierre
authors.initials: P
authors.lastname: Frasse
authors.affiliation: Key Laboratory of Bio-Resource and Eco-Environment of the Ministry of Education, College of Life Sciences, State Key Laboratory of Hydraulics and Mountain River Engineering, Sichuan University, Chengdu 610014, China (M.L.);Université de Toulouse, Institut National Polytechnique de Toulouse-Ecole Nationale Supérieure Agronomique, Unité Mixte de Recherche 990 Génomique et Biotechnologie des Fruits, Castanet-Tolosan, F-31326, France (M.L., B.L.G., I.M., P.F., E.M., M.Z., J.-P.R., M.B., J.P.);Institut National de la Recherche Agronomique, Unité Mixte de Recherche 990 Génomique et Biotechnologie des Fruits, Castanet-Tolosan, F-31326, France (M.L., B.L.G., I.M., P.F., E.M., M.Z., J.-P.R., M.B., J.P.);Department of Food and Experimental Nutrition, NAPAN/FoRC Food Research Center, Universidade de São Paulo, School of Pharmaceutical Sciences, 05508-000 Sao Paulo, Sao Paulo, Brazil (B.L.G., E.P.); andDepartamento de Ciências Biológicas, Escola Superior de Agricultura Luiz de Queiroz, Universidade de São Paulo, 13418-900 Piracicaba, Sao Paulo, Brazil (L.E.P.P.).
authors.forename: Elie
authors.identifier: http://orcid.org/0000-0002-7351-6345
authors.initials: E
authors.lastname: Maza
authors.affiliation: Key Laboratory of Bio-Resource and Eco-Environment of the Ministry of Education, College of Life Sciences, State Key Laboratory of Hydraulics and Mountain River Engineering, Sichuan University, Chengdu 610014, China (M.L.);Université de Toulouse, Institut National Polytechnique de Toulouse-Ecole Nationale Supérieure Agronomique, Unité Mixte de Recherche 990 Génomique et Biotechnologie des Fruits, Castanet-Tolosan, F-31326, France (M.L., B.L.G., I.M., P.F., E.M., M.Z., J.-P.R., M.B., J.P.);Institut National de la Recherche Agronomique, Unité Mixte de Recherche 990 Génomique et Biotechnologie des Fruits, Castanet-Tolosan, F-31326, France (M.L., B.L.G., I.M., P.F., E.M., M.Z., J.-P.R., M.B., J.P.);Department of Food and Experimental Nutrition, NAPAN/FoRC Food Research Center, Universidade de São Paulo, School of Pharmaceutical Sciences, 05508-000 Sao Paulo, Sao Paulo, Brazil (B.L.G., E.P.); andDepartamento de Ciências Biológicas, Escola Superior de Agricultura Luiz de Queiroz, Universidade de São Paulo, 13418-900 Piracicaba, Sao Paulo, Brazil (L.E.P.P.).
authors.forename: Mohamed
authors.initials: M
authors.lastname: Zouine
authors.affiliation: Key Laboratory of Bio-Resource and Eco-Environment of the Ministry of Education, College of Life Sciences, State Key Laboratory of Hydraulics and Mountain River Engineering, Sichuan University, Chengdu 610014, China (M.L.);Université de Toulouse, Institut National Polytechnique de Toulouse-Ecole Nationale Supérieure Agronomique, Unité Mixte de Recherche 990 Génomique et Biotechnologie des Fruits, Castanet-Tolosan, F-31326, France (M.L., B.L.G., I.M., P.F., E.M., M.Z., J.-P.R., M.B., J.P.);Institut National de la Recherche Agronomique, Unité Mixte de Recherche 990 Génomique et Biotechnologie des Fruits, Castanet-Tolosan, F-31326, France (M.L., B.L.G., I.M., P.F., E.M., M.Z., J.-P.R., M.B., J.P.);Department of Food and Experimental Nutrition, NAPAN/FoRC Food Research Center, Universidade de São Paulo, School of Pharmaceutical Sciences, 05508-000 Sao Paulo, Sao Paulo, Brazil (B.L.G., E.P.); andDepartamento de Ciências Biológicas, Escola Superior de Agricultura Luiz de Queiroz, Universidade de São Paulo, 13418-900 Piracicaba, Sao Paulo, Brazil (L.E.P.P.).
authors.forename: Jean-Paul
authors.identifier: http://orcid.org/0000-0001-7707-7776
authors.initials: JP
authors.lastname: Roustan
authors.affiliation: Key Laboratory of Bio-Resource and Eco-Environment of the Ministry of Education, College of Life Sciences, State Key Laboratory of Hydraulics and Mountain River Engineering, Sichuan University, Chengdu 610014, China (M.L.);Université de Toulouse, Institut National Polytechnique de Toulouse-Ecole Nationale Supérieure Agronomique, Unité Mixte de Recherche 990 Génomique et Biotechnologie des Fruits, Castanet-Tolosan, F-31326, France (M.L., B.L.G., I.M., P.F., E.M., M.Z., J.-P.R., M.B., J.P.);Institut National de la Recherche Agronomique, Unité Mixte de Recherche 990 Génomique et Biotechnologie des Fruits, Castanet-Tolosan, F-31326, France (M.L., B.L.G., I.M., P.F., E.M., M.Z., J.-P.R., M.B., J.P.);Department of Food and Experimental Nutrition, NAPAN/FoRC Food Research Center, Universidade de São Paulo, School of Pharmaceutical Sciences, 05508-000 Sao Paulo, Sao Paulo, Brazil (B.L.G., E.P.); andDepartamento de Ciências Biológicas, Escola Superior de Agricultura Luiz de Queiroz, Universidade de São Paulo, 13418-900 Piracicaba, Sao Paulo, Brazil (L.E.P.P.).
authors.forename: Mondher
authors.initials: M
authors.lastname: Bouzayen
authors.affiliation: Key Laboratory of Bio-Resource and Eco-Environment of the Ministry of Education, College of Life Sciences, State Key Laboratory of Hydraulics and Mountain River Engineering, Sichuan University, Chengdu 610014, China (M.L.);Université de Toulouse, Institut National Polytechnique de Toulouse-Ecole Nationale Supérieure Agronomique, Unité Mixte de Recherche 990 Génomique et Biotechnologie des Fruits, Castanet-Tolosan, F-31326, France (M.L., B.L.G., I.M., P.F., E.M., M.Z., J.-P.R., M.B., J.P.);Institut National de la Recherche Agronomique, Unité Mixte de Recherche 990 Génomique et Biotechnologie des Fruits, Castanet-Tolosan, F-31326, France (M.L., B.L.G., I.M., P.F., E.M., M.Z., J.-P.R., M.B., J.P.);Department of Food and Experimental Nutrition, NAPAN/FoRC Food Research Center, Universidade de São Paulo, School of Pharmaceutical Sciences, 05508-000 Sao Paulo, Sao Paulo, Brazil (B.L.G., E.P.); andDepartamento de Ciências Biológicas, Escola Superior de Agricultura Luiz de Queiroz, Universidade de São Paulo, 13418-900 Piracicaba, Sao Paulo, Brazil (L.E.P.P.) liumingchun1982102@163.com julien.pirrello@ensat.fr.
authors.forename: Julien
authors.identifier: http://orcid.org/0000-0002-5725-885X
authors.initials: J
authors.lastname: Pirrello
mesh_terms: D016000:Cluster Analysis; D005030:Ethylenes / Q000494:pharmacology*; D005638:Fruit / Q000235:genetics* / Q000502:physiology; D020869:Gene Expression Profiling / Q000379:methods*; D018506:Gene Expression Regulation, Plant / Q000187:drug effects*; D053263:Gene Regulatory Networks; D017343:Genes, Plant / Q000235:genetics; D005809:Genes, Regulator / Q000235:genetics; D018551:Solanum lycopersicum / Q000235:genetics* / Q000502:physiology; D009154:Mutation; D010937:Plant Growth Regulators / Q000494:pharmacology; D010940:Plant Proteins / Q000235:genetics / Q000378:metabolism; D011401:Promoter Regions, Genetic / Q000235:genetics; D020218:Response Elements / Q000235:genetics*; D020133:Reverse Transcriptase Polymerase Chain Reaction
chemical_list: D005030:Ethylenes; D010937:Plant Growth Regulators; D010940:Plant Proteins; C036216:ethylene