title: The Tomato MIXTA-Like Transcription Factor Coordinates Fruit Epidermis Conical Cell Development and Cuticular Lipid Biosynthesis and Assembly.
abstract: The epidermis of aerial plant organs is the primary source of building blocks forming the outer surface cuticular layer. To examine the relationship between epidermal cell development and cuticle assembly in the context of fruit surface, we investigated the tomato (Solanum lycopersicum) MIXTA-like gene. MIXTA/MIXTA-like proteins, initially described in snapdragon (Antirrhinum majus) petals, are known regulators of epidermal cell differentiation. Fruit of transgenically silenced SlMIXTA-like tomato plants displayed defects in patterning of conical epidermal cells. They also showed altered postharvest water loss and resistance to pathogens. Transcriptome and cuticular lipids profiling coupled with comprehensive microscopy revealed significant modifications to cuticle assembly and suggested SlMIXTA-like to regulate cutin biosynthesis. Candidate genes likely acting downstream of SlMIXTA-like included cytochrome P450s (CYPs) of the CYP77A and CYP86A subfamilies, LONG-CHAIN ACYL-COA SYNTHETASE2, GLYCEROL-3-PHOSPHATE SN-2-ACYLTRANSFERASE4, and the ATP-BINDING CASSETTE11 cuticular lipids transporter. As part of a larger regulatory network of epidermal cell patterning and L1-layer identity, we found that SlMIXTA-like acts downstream of SlSHINE3 and possibly cooperates with homeodomain Leu zipper IV transcription factors. Hence, SlMIXTA-like is a positive regulator of both cuticle and conical epidermal cell formation in tomato fruit, acting as a mediator of the tight association between fruit cutin polymer formation, cuticle assembly, and epidermal cell patterning.
authors.affiliation: Department of Plant Sciences (J.L., A.Ad., O.L., N.A., T.T., J.-P.F.-M., A.Ah.) andChemical Research Support (K.R.), Weizmann Institute of Science, Rehovot 76100, Israel;Research and Innovation Centre, Foundation Edmund Mach, I-38010 San Michele all'Adige, Trento, Italy (J.L., F.C.);Institute for Wine Biotechnology, Stellenbosch University, Stellenbosch 7602, South Africa (J.L.);Department of Postharvest Science of Fresh Fruit, The Volcani Center, Agricultural Research Organization, Bet Dagan 50250, Israel (N.A.);Department of Plant Breeding and Biotechnology, Instituto de Biología Molecular y Celular de Plantas, 46022 Valencia, Spain (J.-P.F.-M., A.G.); andDépartement Réseaux Métaboliques chez les Végétaux, Institut de Biologie Molééculaire des Plantes, Centre National de la Recherche Scientifique, Unité Propre de Recherche 2357, Université de Strasbourg, 67083 Strasbourg cedex, France (E.W., B.G., F.P.).
authors.forename: Justin
authors.identifier: http://orcid.org/0000-0003-4511-4215
authors.initials: J
authors.lastname: Lashbrooke
authors.affiliation: Department of Plant Sciences (J.L., A.Ad., O.L., N.A., T.T., J.-P.F.-M., A.Ah.) andChemical Research Support (K.R.), Weizmann Institute of Science, Rehovot 76100, Israel;Research and Innovation Centre, Foundation Edmund Mach, I-38010 San Michele all'Adige, Trento, Italy (J.L., F.C.);Institute for Wine Biotechnology, Stellenbosch University, Stellenbosch 7602, South Africa (J.L.);Department of Postharvest Science of Fresh Fruit, The Volcani Center, Agricultural Research Organization, Bet Dagan 50250, Israel (N.A.);Department of Plant Breeding and Biotechnology, Instituto de Biología Molecular y Celular de Plantas, 46022 Valencia, Spain (J.-P.F.-M., A.G.); andDépartement Réseaux Métaboliques chez les Végétaux, Institut de Biologie Molééculaire des Plantes, Centre National de la Recherche Scientifique, Unité Propre de Recherche 2357, Université de Strasbourg, 67083 Strasbourg cedex, France (E.W., B.G., F.P.).
authors.forename: Avital
authors.identifier: http://orcid.org/0000-0002-7430-0079
authors.initials: A
authors.lastname: Adato
authors.affiliation: Department of Plant Sciences (J.L., A.Ad., O.L., N.A., T.T., J.-P.F.-M., A.Ah.) andChemical Research Support (K.R.), Weizmann Institute of Science, Rehovot 76100, Israel;Research and Innovation Centre, Foundation Edmund Mach, I-38010 San Michele all'Adige, Trento, Italy (J.L., F.C.);Institute for Wine Biotechnology, Stellenbosch University, Stellenbosch 7602, South Africa (J.L.);Department of Postharvest Science of Fresh Fruit, The Volcani Center, Agricultural Research Organization, Bet Dagan 50250, Israel (N.A.);Department of Plant Breeding and Biotechnology, Instituto de Biología Molecular y Celular de Plantas, 46022 Valencia, Spain (J.-P.F.-M., A.G.); andDépartement Réseaux Métaboliques chez les Végétaux, Institut de Biologie Molééculaire des Plantes, Centre National de la Recherche Scientifique, Unité Propre de Recherche 2357, Université de Strasbourg, 67083 Strasbourg cedex, France (E.W., B.G., F.P.).
authors.forename: Orfa
authors.initials: O
authors.lastname: Lotan
authors.affiliation: Department of Plant Sciences (J.L., A.Ad., O.L., N.A., T.T., J.-P.F.-M., A.Ah.) andChemical Research Support (K.R.), Weizmann Institute of Science, Rehovot 76100, Israel;Research and Innovation Centre, Foundation Edmund Mach, I-38010 San Michele all'Adige, Trento, Italy (J.L., F.C.);Institute for Wine Biotechnology, Stellenbosch University, Stellenbosch 7602, South Africa (J.L.);Department of Postharvest Science of Fresh Fruit, The Volcani Center, Agricultural Research Organization, Bet Dagan 50250, Israel (N.A.);Department of Plant Breeding and Biotechnology, Instituto de Biología Molecular y Celular de Plantas, 46022 Valencia, Spain (J.-P.F.-M., A.G.); andDépartement Réseaux Métaboliques chez les Végétaux, Institut de Biologie Molééculaire des Plantes, Centre National de la Recherche Scientifique, Unité Propre de Recherche 2357, Université de Strasbourg, 67083 Strasbourg cedex, France (E.W., B.G., F.P.).
authors.forename: Noam
authors.initials: N
authors.lastname: Alkan
authors.affiliation: Department of Plant Sciences (J.L., A.Ad., O.L., N.A., T.T., J.-P.F.-M., A.Ah.) andChemical Research Support (K.R.), Weizmann Institute of Science, Rehovot 76100, Israel;Research and Innovation Centre, Foundation Edmund Mach, I-38010 San Michele all'Adige, Trento, Italy (J.L., F.C.);Institute for Wine Biotechnology, Stellenbosch University, Stellenbosch 7602, South Africa (J.L.);Department of Postharvest Science of Fresh Fruit, The Volcani Center, Agricultural Research Organization, Bet Dagan 50250, Israel (N.A.);Department of Plant Breeding and Biotechnology, Instituto de Biología Molecular y Celular de Plantas, 46022 Valencia, Spain (J.-P.F.-M., A.G.); andDépartement Réseaux Métaboliques chez les Végétaux, Institut de Biologie Molééculaire des Plantes, Centre National de la Recherche Scientifique, Unité Propre de Recherche 2357, Université de Strasbourg, 67083 Strasbourg cedex, France (E.W., B.G., F.P.).
authors.forename: Tatiana
authors.initials: T
authors.lastname: Tsimbalist
authors.affiliation: Department of Plant Sciences (J.L., A.Ad., O.L., N.A., T.T., J.-P.F.-M., A.Ah.) andChemical Research Support (K.R.), Weizmann Institute of Science, Rehovot 76100, Israel;Research and Innovation Centre, Foundation Edmund Mach, I-38010 San Michele all'Adige, Trento, Italy (J.L., F.C.);Institute for Wine Biotechnology, Stellenbosch University, Stellenbosch 7602, South Africa (J.L.);Department of Postharvest Science of Fresh Fruit, The Volcani Center, Agricultural Research Organization, Bet Dagan 50250, Israel (N.A.);Department of Plant Breeding and Biotechnology, Instituto de Biología Molecular y Celular de Plantas, 46022 Valencia, Spain (J.-P.F.-M., A.G.); andDépartement Réseaux Métaboliques chez les Végétaux, Institut de Biologie Molééculaire des Plantes, Centre National de la Recherche Scientifique, Unité Propre de Recherche 2357, Université de Strasbourg, 67083 Strasbourg cedex, France (E.W., B.G., F.P.).
authors.forename: Katya
authors.initials: K
authors.lastname: Rechav
authors.affiliation: Department of Plant Sciences (J.L., A.Ad., O.L., N.A., T.T., J.-P.F.-M., A.Ah.) andChemical Research Support (K.R.), Weizmann Institute of Science, Rehovot 76100, Israel;Research and Innovation Centre, Foundation Edmund Mach, I-38010 San Michele all'Adige, Trento, Italy (J.L., F.C.);Institute for Wine Biotechnology, Stellenbosch University, Stellenbosch 7602, South Africa (J.L.);Department of Postharvest Science of Fresh Fruit, The Volcani Center, Agricultural Research Organization, Bet Dagan 50250, Israel (N.A.);Department of Plant Breeding and Biotechnology, Instituto de Biología Molecular y Celular de Plantas, 46022 Valencia, Spain (J.-P.F.-M., A.G.); andDépartement Réseaux Métaboliques chez les Végétaux, Institut de Biologie Molééculaire des Plantes, Centre National de la Recherche Scientifique, Unité Propre de Recherche 2357, Université de Strasbourg, 67083 Strasbourg cedex, France (E.W., B.G., F.P.).
authors.forename: Josefina-Patricia
authors.initials: JP
authors.lastname: Fernandez-Moreno
authors.affiliation: Department of Plant Sciences (J.L., A.Ad., O.L., N.A., T.T., J.-P.F.-M., A.Ah.) andChemical Research Support (K.R.), Weizmann Institute of Science, Rehovot 76100, Israel;Research and Innovation Centre, Foundation Edmund Mach, I-38010 San Michele all'Adige, Trento, Italy (J.L., F.C.);Institute for Wine Biotechnology, Stellenbosch University, Stellenbosch 7602, South Africa (J.L.);Department of Postharvest Science of Fresh Fruit, The Volcani Center, Agricultural Research Organization, Bet Dagan 50250, Israel (N.A.);Department of Plant Breeding and Biotechnology, Instituto de Biología Molecular y Celular de Plantas, 46022 Valencia, Spain (J.-P.F.-M., A.G.); andDépartement Réseaux Métaboliques chez les Végétaux, Institut de Biologie Molééculaire des Plantes, Centre National de la Recherche Scientifique, Unité Propre de Recherche 2357, Université de Strasbourg, 67083 Strasbourg cedex, France (E.W., B.G., F.P.).
authors.forename: Emilie
authors.initials: E
authors.lastname: Widemann
authors.affiliation: Department of Plant Sciences (J.L., A.Ad., O.L., N.A., T.T., J.-P.F.-M., A.Ah.) andChemical Research Support (K.R.), Weizmann Institute of Science, Rehovot 76100, Israel;Research and Innovation Centre, Foundation Edmund Mach, I-38010 San Michele all'Adige, Trento, Italy (J.L., F.C.);Institute for Wine Biotechnology, Stellenbosch University, Stellenbosch 7602, South Africa (J.L.);Department of Postharvest Science of Fresh Fruit, The Volcani Center, Agricultural Research Organization, Bet Dagan 50250, Israel (N.A.);Department of Plant Breeding and Biotechnology, Instituto de Biología Molecular y Celular de Plantas, 46022 Valencia, Spain (J.-P.F.-M., A.G.); andDépartement Réseaux Métaboliques chez les Végétaux, Institut de Biologie Molééculaire des Plantes, Centre National de la Recherche Scientifique, Unité Propre de Recherche 2357, Université de Strasbourg, 67083 Strasbourg cedex, France (E.W., B.G., F.P.).
authors.forename: Bernard
authors.initials: B
authors.lastname: Grausem
authors.affiliation: Department of Plant Sciences (J.L., A.Ad., O.L., N.A., T.T., J.-P.F.-M., A.Ah.) andChemical Research Support (K.R.), Weizmann Institute of Science, Rehovot 76100, Israel;Research and Innovation Centre, Foundation Edmund Mach, I-38010 San Michele all'Adige, Trento, Italy (J.L., F.C.);Institute for Wine Biotechnology, Stellenbosch University, Stellenbosch 7602, South Africa (J.L.);Department of Postharvest Science of Fresh Fruit, The Volcani Center, Agricultural Research Organization, Bet Dagan 50250, Israel (N.A.);Department of Plant Breeding and Biotechnology, Instituto de Biología Molecular y Celular de Plantas, 46022 Valencia, Spain (J.-P.F.-M., A.G.); andDépartement Réseaux Métaboliques chez les Végétaux, Institut de Biologie Molééculaire des Plantes, Centre National de la Recherche Scientifique, Unité Propre de Recherche 2357, Université de Strasbourg, 67083 Strasbourg cedex, France (E.W., B.G., F.P.).
authors.forename: Franck
authors.initials: F
authors.lastname: Pinot
authors.affiliation: Department of Plant Sciences (J.L., A.Ad., O.L., N.A., T.T., J.-P.F.-M., A.Ah.) andChemical Research Support (K.R.), Weizmann Institute of Science, Rehovot 76100, Israel;Research and Innovation Centre, Foundation Edmund Mach, I-38010 San Michele all'Adige, Trento, Italy (J.L., F.C.);Institute for Wine Biotechnology, Stellenbosch University, Stellenbosch 7602, South Africa (J.L.);Department of Postharvest Science of Fresh Fruit, The Volcani Center, Agricultural Research Organization, Bet Dagan 50250, Israel (N.A.);Department of Plant Breeding and Biotechnology, Instituto de Biología Molecular y Celular de Plantas, 46022 Valencia, Spain (J.-P.F.-M., A.G.); andDépartement Réseaux Métaboliques chez les Végétaux, Institut de Biologie Molééculaire des Plantes, Centre National de la Recherche Scientifique, Unité Propre de Recherche 2357, Université de Strasbourg, 67083 Strasbourg cedex, France (E.W., B.G., F.P.).
authors.forename: Antonio
authors.identifier: http://orcid.org/0000-0003-4266-9581
authors.initials: A
authors.lastname: Granell
authors.affiliation: Department of Plant Sciences (J.L., A.Ad., O.L., N.A., T.T., J.-P.F.-M., A.Ah.) andChemical Research Support (K.R.), Weizmann Institute of Science, Rehovot 76100, Israel;Research and Innovation Centre, Foundation Edmund Mach, I-38010 San Michele all'Adige, Trento, Italy (J.L., F.C.);Institute for Wine Biotechnology, Stellenbosch University, Stellenbosch 7602, South Africa (J.L.);Department of Postharvest Science of Fresh Fruit, The Volcani Center, Agricultural Research Organization, Bet Dagan 50250, Israel (N.A.);Department of Plant Breeding and Biotechnology, Instituto de Biología Molecular y Celular de Plantas, 46022 Valencia, Spain (J.-P.F.-M., A.G.); andDépartement Réseaux Métaboliques chez les Végétaux, Institut de Biologie Molééculaire des Plantes, Centre National de la Recherche Scientifique, Unité Propre de Recherche 2357, Université de Strasbourg, 67083 Strasbourg cedex, France (E.W., B.G., F.P.).
authors.forename: Fabrizio
authors.initials: F
authors.lastname: Costa
authors.affiliation: Department of Plant Sciences (J.L., A.Ad., O.L., N.A., T.T., J.-P.F.-M., A.Ah.) andChemical Research Support (K.R.), Weizmann Institute of Science, Rehovot 76100, Israel;Research and Innovation Centre, Foundation Edmund Mach, I-38010 San Michele all'Adige, Trento, Italy (J.L., F.C.);Institute for Wine Biotechnology, Stellenbosch University, Stellenbosch 7602, South Africa (J.L.);Department of Postharvest Science of Fresh Fruit, The Volcani Center, Agricultural Research Organization, Bet Dagan 50250, Israel (N.A.);Department of Plant Breeding and Biotechnology, Instituto de Biología Molecular y Celular de Plantas, 46022 Valencia, Spain (J.-P.F.-M., A.G.); andDépartement Réseaux Métaboliques chez les Végétaux, Institut de Biologie Molééculaire des Plantes, Centre National de la Recherche Scientifique, Unité Propre de Recherche 2357, Université de Strasbourg, 67083 Strasbourg cedex, France (E.W., B.G., F.P.) asaph.aharoni@weizmann.ac.il.
authors.forename: Asaph
authors.initials: A
authors.lastname: Aharoni
mesh_terms: D005638:Fruit / Q000235:genetics* / Q000254:growth & development / Q000378:metabolism; D008055:Lipids / Q000096:biosynthesis*; D018551:Solanum lycopersicum / Q000235:genetics* / Q000254:growth & development / Q000378:metabolism; D010641:Phenotype; D019441:Plant Epidermis / Q000235:genetics / Q000254:growth & development / Q000378:metabolism; D010940:Plant Proteins / Q000235:genetics / Q000378:metabolism; D030821:Plants, Genetically Modified; D014157:Transcription Factors / Q000235:genetics / Q000378:metabolism*
chemical_list: D008055:Lipids; D010940:Plant Proteins; D014157:Transcription Factors