title: Nitric Oxide, Ethylene, and Auxin Cross Talk Mediates Greening and Plastid Development in Deetiolating Tomato Seedlings.
abstract: The transition from etiolated to green seedlings involves the conversion of etioplasts into mature chloroplasts via a multifaceted, light-driven process comprising multiple, tightly coordinated signaling networks. Here, we demonstrate that light-induced greening and chloroplast differentiation in tomato (Solanum lycopersicum) seedlings are mediated by an intricate cross talk among phytochromes, nitric oxide (NO), ethylene, and auxins. Genetic and pharmacological evidence indicated that either endogenously produced or exogenously applied NO promotes seedling greening by repressing ethylene biosynthesis and inducing auxin accumulation in tomato cotyledons. Analysis performed in hormonal tomato mutants also demonstrated that NO production itself is negatively and positively regulated by ethylene and auxins, respectively. Representing a major biosynthetic source of NO in tomato cotyledons, nitrate reductase was shown to be under strict control of both phytochrome and hormonal signals. A close NO-phytochrome interaction was revealed by the almost complete recovery of the etiolated phenotype of red light-grown seedlings of the tomato phytochrome-deficient aurea mutant upon NO fumigation. In this mutant, NO supplementation induced cotyledon greening, chloroplast differentiation, and hormonal and gene expression alterations similar to those detected in light-exposed wild-type seedlings. NO negatively impacted the transcript accumulation of genes encoding phytochromes, photomorphogenesis-repressor factors, and plastid division proteins, revealing that this free radical can mimic transcriptional changes typically triggered by phytochrome-dependent light perception. Therefore, our data indicate that negative and positive regulatory feedback loops orchestrate ethylene-NO and auxin-NO interactions, respectively, during the conversion of colorless etiolated seedlings into green, photosynthetically competent young plants.
authors.affiliation: Department of Botany, University of São Paulo, Sao Paulo 05508-090, Brazil (N.K.G.M., R.E.B., B.S.L., P.M.R.O., R.Z., D.L.O.D., D.D., M.R., L.F.); andDepartment of Biological Sciences, Escola Superior de Agricultura Luiz de Queiroz, University of São Paulo, Piracicaba 13418-900, Brazil (L.E.P.P.).
authors.forename: Nielda K G
authors.initials: NK
authors.lastname: Melo
authors.affiliation: Department of Botany, University of São Paulo, Sao Paulo 05508-090, Brazil (N.K.G.M., R.E.B., B.S.L., P.M.R.O., R.Z., D.L.O.D., D.D., M.R., L.F.); andDepartment of Biological Sciences, Escola Superior de Agricultura Luiz de Queiroz, University of São Paulo, Piracicaba 13418-900, Brazil (L.E.P.P.).
authors.forename: Ricardo E
authors.initials: RE
authors.lastname: Bianchetti
authors.affiliation: Department of Botany, University of São Paulo, Sao Paulo 05508-090, Brazil (N.K.G.M., R.E.B., B.S.L., P.M.R.O., R.Z., D.L.O.D., D.D., M.R., L.F.); andDepartment of Biological Sciences, Escola Superior de Agricultura Luiz de Queiroz, University of São Paulo, Piracicaba 13418-900, Brazil (L.E.P.P.).
authors.forename: Bruno S
authors.identifier: 0000-0002-0820-6682
authors.initials: BS
authors.lastname: Lira
authors.affiliation: Department of Botany, University of São Paulo, Sao Paulo 05508-090, Brazil (N.K.G.M., R.E.B., B.S.L., P.M.R.O., R.Z., D.L.O.D., D.D., M.R., L.F.); andDepartment of Biological Sciences, Escola Superior de Agricultura Luiz de Queiroz, University of São Paulo, Piracicaba 13418-900, Brazil (L.E.P.P.).
authors.forename: Paulo M R
authors.initials: PM
authors.lastname: Oliveira
authors.affiliation: Department of Botany, University of São Paulo, Sao Paulo 05508-090, Brazil (N.K.G.M., R.E.B., B.S.L., P.M.R.O., R.Z., D.L.O.D., D.D., M.R., L.F.); andDepartment of Biological Sciences, Escola Superior de Agricultura Luiz de Queiroz, University of São Paulo, Piracicaba 13418-900, Brazil (L.E.P.P.).
authors.forename: Rafael
authors.identifier: 0000-0003-0912-9065
authors.initials: R
authors.lastname: Zuccarelli
authors.affiliation: Department of Botany, University of São Paulo, Sao Paulo 05508-090, Brazil (N.K.G.M., R.E.B., B.S.L., P.M.R.O., R.Z., D.L.O.D., D.D., M.R., L.F.); andDepartment of Biological Sciences, Escola Superior de Agricultura Luiz de Queiroz, University of São Paulo, Piracicaba 13418-900, Brazil (L.E.P.P.).
authors.forename: Devisson L O
authors.identifier: 0000-0002-3230-6544
authors.initials: DL
authors.lastname: Dias
authors.affiliation: Department of Botany, University of São Paulo, Sao Paulo 05508-090, Brazil (N.K.G.M., R.E.B., B.S.L., P.M.R.O., R.Z., D.L.O.D., D.D., M.R., L.F.); andDepartment of Biological Sciences, Escola Superior de Agricultura Luiz de Queiroz, University of São Paulo, Piracicaba 13418-900, Brazil (L.E.P.P.).
authors.forename: Diego
authors.initials: D
authors.lastname: Demarco
authors.affiliation: Department of Botany, University of São Paulo, Sao Paulo 05508-090, Brazil (N.K.G.M., R.E.B., B.S.L., P.M.R.O., R.Z., D.L.O.D., D.D., M.R., L.F.); andDepartment of Biological Sciences, Escola Superior de Agricultura Luiz de Queiroz, University of São Paulo, Piracicaba 13418-900, Brazil (L.E.P.P.).
authors.forename: Lazaro E P
authors.identifier: 0000-0002-8761-5934
authors.initials: LE
authors.lastname: Peres
authors.affiliation: Department of Botany, University of São Paulo, Sao Paulo 05508-090, Brazil (N.K.G.M., R.E.B., B.S.L., P.M.R.O., R.Z., D.L.O.D., D.D., M.R., L.F.); andDepartment of Biological Sciences, Escola Superior de Agricultura Luiz de Queiroz, University of São Paulo, Piracicaba 13418-900, Brazil (L.E.P.P.).
authors.forename: Magdalena
authors.identifier: 0000-0003-3650-772X
authors.initials: M
authors.lastname: Rossi
authors.affiliation: Department of Botany, University of São Paulo, Sao Paulo 05508-090, Brazil (N.K.G.M., R.E.B., B.S.L., P.M.R.O., R.Z., D.L.O.D., D.D., M.R., L.F.); andDepartment of Biological Sciences, Escola Superior de Agricultura Luiz de Queiroz, University of São Paulo, Piracicaba 13418-900, Brazil (L.E.P.P.) freschi@usp.br.
authors.forename: Luciano
authors.identifier: 0000-0002-0737-3438
authors.initials: L
authors.lastname: Freschi
mesh_terms: D001664:Biliverdine / Q000031:analogs & derivatives / Q000378:metabolism; D002454:Cell Differentiation / Q000235:genetics / Q000528:radiation effects; D002734:Chlorophyll / Q000378:metabolism; D018548:Cotyledon / Q000378:metabolism / Q000528:radiation effects / Q000648:ultrastructure; D015536:Down-Regulation / Q000235:genetics / Q000528:radiation effects; D005030:Ethylenes / Q000378:metabolism*; D064527:Etiolation; D005651:Fumigation; D018506:Gene Expression Regulation, Plant / Q000528:radiation effects; D017343:Genes, Plant; D007210:Indoleacetic Acids / Q000378:metabolism*; D008027:Light; D018551:Solanum lycopersicum / Q000235:genetics / Q000378:metabolism / Q000502:physiology* / Q000528:radiation effects; D009024:Morphogenesis / Q000528:radiation effects; D009154:Mutation / Q000235:genetics; D050901:Nitrate Reductase / Q000378:metabolism; D009569:Nitric Oxide / Q000378:metabolism*; D018087:Plastids / Q000378:metabolism* / Q000528:radiation effects / Q000648:ultrastructure; D012333:RNA, Messenger / Q000235:genetics / Q000378:metabolism; D036226:Seedlings / Q000378:metabolism* / Q000528:radiation effects
chemical_list: D005030:Ethylenes; D007210:Indoleacetic Acids; D012333:RNA, Messenger; D002734:Chlorophyll; C075811:phytochromobilin; D009569:Nitric Oxide; C036216:ethylene; D050901:Nitrate Reductase; D001664:Biliverdine
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