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TOMATO AGAMOUS1 and ARLEQUIN/TOMATO AGAMOUS-LIKE1 MADS-box genes have redundant and divergent functions required for tomato reproductive development

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TOMATO AGAMOUS1 and ARLEQUIN/TOMATO AGAMOUS-LIKE1 MADS-box genes have redundant and divergent functions required for tomato reproductive development

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dc.contributor.author Giménez Caminero, Maria Estela es_ES
dc.contributor.author Castañeda, Laura es_ES
dc.contributor.author Pineda Chaza, Benito José es_ES
dc.contributor.author Pan, Irvin L. es_ES
dc.contributor.author Moreno Ferrero, Vicente es_ES
dc.contributor.author Angosto, Trinidad es_ES
dc.contributor.author Lozano, Rafael es_ES
dc.date.accessioned 2022-05-11T18:06:28Z
dc.date.available 2022-05-11T18:06:28Z
dc.date.issued 2016-07 es_ES
dc.identifier.issn 0167-4412 es_ES
dc.identifier.uri http://hdl.handle.net/10251/182548
dc.description.abstract [EN] Within the tomato MADS-box gene family, TOMATO AGAMOUS1 (TAG1) and ARLEQUIN/TOMATO AGAMOUS LIKE1 (hereafter referred to as TAGL1) are, respectively, members of the euAG and PLE lineages of the AGAMOUS clade. They perform crucial functions specifying stamen and carpel development in the flower and controlling late fruit development. To gain insight into the roles of TAG1 and TAGL1 genes and to better understand their functional redundancy and diversification, we characterized single and double RNAi silencing lines of these genes and analyzed expression profiles of regulatory genes involved in reproductive development. Double RNAi lines did show cell abnormalities in stamens and carpels and produced extremely small fruit-like organs displaying some sepaloid features. Expression analyses indicated that TAG1 and TAGL1 act together to repress fourth whorl sepal development, most likely through the MACROCALYX gene. Results also proved that TAG1 and TAGL1 have diversified their functions in fruit development: while TAG1 controls placenta and seed formation, TAGL1 participates in cuticle development and lignin biosynthesis inhibition. It is noteworthy that both TAG1 and double RNAi plants lacked seed development due to abnormalities in pollen formation. This seedless phenotype was not associated with changes in the expression of B-class stamen identity genes Tomato MADS-box 6 and Tomato PISTILLATA observed in silencing lines, suggesting that other regulatory factors should participate in pollen formation. Taken together, results here reported support the idea that both redundant and divergent functions of TAG1 and TAGL1 genes are needed to control tomato reproductive development. es_ES
dc.description.sponsorship This work was supported by the Spanish Ministry of Economy and Competitiveness (Grant Numbers AGL2012-40150-C03-01, AGL2012-40150-C03-02 and AGL2015-64991-C3-1-R); and the European Commission through the JAE-Doc Program of the Spanish National Research Council (CSIC) (Grant Number AGL2012-40150-C03-01 to B.P.). es_ES
dc.language Inglés es_ES
dc.publisher Springer-Verlag es_ES
dc.relation.ispartof Plant Molecular Biology es_ES
dc.rights Reserva de todos los derechos es_ES
dc.subject Functional diversification es_ES
dc.subject Redundancy es_ES
dc.subject Reproductive development es_ES
dc.subject Solanum lycopersicum es_ES
dc.subject TAG1 es_ES
dc.subject TAGL1 es_ES
dc.subject.classification GENETICA es_ES
dc.title TOMATO AGAMOUS1 and ARLEQUIN/TOMATO AGAMOUS-LIKE1 MADS-box genes have redundant and divergent functions required for tomato reproductive development es_ES
dc.type Artículo es_ES
dc.identifier.doi 10.1007/s11103-016-0485-4 es_ES
dc.relation.projectID info:eu-repo/grantAgreement/MINECO//AGL2015-64991-C3-1-R/ES/GENOMICA FUNCIONAL Y MEJORA GENETICA DE LA PRODUCTIVIDAD DE TOMATE: IMPORTANCIA AGRONOMICA DEL BALANCE DESARROLLO-ESTRES ABIOTICO/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/MINECO//AGL2012-40150-C03-02/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/MINECO//AGL2012-40150-C03-01//Identificación, etiquetado y análisis funcional de genes implicados en el cuajado del fruto de tomate y tolerancia a la salinidad en especies silvestres relacionadas/ es_ES
dc.rights.accessRights Abierto es_ES
dc.contributor.affiliation Universitat Politècnica de València. Departamento de Biotecnología - Departament de Biotecnologia es_ES
dc.description.bibliographicCitation Giménez Caminero, ME.; Castañeda, L.; Pineda Chaza, BJ.; Pan, IL.; Moreno Ferrero, V.; Angosto, T.; Lozano, R. (2016). TOMATO AGAMOUS1 and ARLEQUIN/TOMATO AGAMOUS-LIKE1 MADS-box genes have redundant and divergent functions required for tomato reproductive development. Plant Molecular Biology. 91(4-5):513-531. https://doi.org/10.1007/s11103-016-0485-4 es_ES
dc.description.accrualMethod S es_ES
dc.relation.publisherversion https://doi.org/10.1007/s11103-016-0485-4 es_ES
dc.description.upvformatpinicio 513 es_ES
dc.description.upvformatpfin 531 es_ES
dc.type.version info:eu-repo/semantics/publishedVersion es_ES
dc.description.volume 91 es_ES
dc.description.issue 4-5 es_ES
dc.identifier.pmid 27125648 es_ES
dc.relation.pasarela S\327313 es_ES
dc.contributor.funder MINISTERIO DE ECONOMIA Y EMPRESA es_ES
dc.contributor.funder Ministerio de Economía y Competitividad es_ES
dc.description.references Adamczyk BJ, Fernandez DE (2009) MIKC* MADS domain heterodimers are required for pollen maturation and tube growth in Arabidopsis. Plant Physiol 149:1713–1723 es_ES
dc.description.references Alvarez-Buylla ER, Liljegren SJ, Pelaz S, Gold SJ, Burgeff C, Ditta GS, Vergara F, Yanofsky MF (2000a) MADS-box gene evolution beyond flowers: expression in pollen, endosperm, guard cells, roots and trichomes. Plant J 24:457–466 es_ES
dc.description.references Alvarez-Buylla ER, Pelaz S, Liljegren SJ, Gold SE, Burgeff C, Ditta GS, Ribas de Pouplana L, Martinez-Castilla L, Yanofsky MF (2000b) An ancestral MADS-box gene duplication occurred before the divergence of plants and animals. Proc Natl Acad Sci USA 97:5328–5333 es_ES
dc.description.references Becker A, Theissen G (2003) The major clades of MADS-box genes and their role in the development and evolution of flowering plants. Mol Phylogenet Evol 29:464–489 es_ES
dc.description.references Boss P, Vivier M, Matsumoto S, Dry I, Thomas M (2001) A cDNA from grapevine (Vitis vinifera L.), which shows homology to AGAMOUS and SHATTERPROOF, is not only expressed in flowers but also throughout berry development. Plant Mol Biol 45:541–553 es_ES
dc.description.references Bowman JL, Smyth DR, Meyerowitz EM (1989) Genes directing flower development in Arabidopsis. Plant Cell 1:37–52 es_ES
dc.description.references Bowman JL, Smyth DR, Meyerowitzt EM (1991) Genetic interactions among floral homeotic genes of Arabidopsis. Development 112:1–20 es_ES
dc.description.references Bradley D, Carpenter R, Sommer H, Hartley N, Coen E (1993) Complementary floral homeotic phenotypes result from opposite orientations of a transposon at the plena locus of antirrhinum. Cell 72:85–95 es_ES
dc.description.references Brukhin V, Hernould M, Gonzalez N, Chevalier C, Mouras A (2003) Flower development schedule in tomato Lycopersicon esculentum cv. sweet cherry. Sex Plant Reprod 15:311–320 es_ES
dc.description.references Busi MV, Bustamante C, D’Angelo C, Hidalgo-Cuevas M, Boggio SB, Valle EM, Zabaleta E (2003) MADS-box genes expressed during tomato seed and fruit development. Plant Mol Biol 52:801–815 es_ES
dc.description.references Carpenter R, Coen ES (1990) Floral homeotic mutations produced by transposon-mutagenesis in Antirrhinum majus. Genes Dev 4:1483–1493 es_ES
dc.description.references Causier B, Castillo R, Zhou J, Ingram R, Xue Y, Schwarz-Sommer Z, Davies B (2005) Evolution in action: following function in duplicated floral homeotic genes. Curr Biol 15:1508–1512 es_ES
dc.description.references Coen E, Meyerowitz EM (1991) The war of the whorls: genetic interactions controlling flower development. Nature 353:31–37 es_ES
dc.description.references Davies B, Motte P, Keck E, Saedler H, Sommer H, Schwarz-Sommer Z (1999) PLENA and FARINELLI: redundancy and regulatory interactions between two antirrhinum MADS-box factors controlling flower development. EMBO J 18:4023–4034 es_ES
dc.description.references di Martino G, Pan I, Emmanuel E, Levy A, Irish V (2006) Functional analyses of two tomato APETALA3 genes demonstrate diversification in their roles in regulating floral development. Plant Cell 18:1833–1845 es_ES
dc.description.references Favaro R, Pinyopich A, Battaglia R, Kooiker M, Borghi L, Ditta G, Yanofsky MF, Kater MM, Colombo L (2003) MADS-box protein complexes control carpel and ovule development in Arabidopsis. Plant Cell 15:2603–2611 es_ES
dc.description.references Fourquin C, Ferrándiz C (2012) Functional analyses of AGAMOUS family members in Nicotiana benthamiana clarify the evolution of early and late roles of C-function genes in eudicots. Plant J 71:990–1001 es_ES
dc.description.references Geuten K, Irish V (2010) Hidden variability of floral homeotic B genes in Solanaceae provides a molecular basis for the evolution of novel functions. Plant Cell 22:2562–2578 es_ES
dc.description.references Gimenez E, Dominguez E, Pineda B, Heredia A, Moreno V, Lozano R et al (2015) Transcriptional activity of the MADS box ARLEQUIN/TOMATO AGAMOUS-LIKE1 gene is required for cuticle development of tomato fruit. Plant Physiol 168(3):1036–1048 es_ES
dc.description.references Gimenez E, Pineda B, Capel J, Antón MT, Atarés A, Perez-Martin F, Garcia-Sogo B, Angosto T, Moreno V, Lozano R (2010) Functional analysis of the Arlequin mutant corroborates the essential role of the ARLEQUIN/TAGL1 gene during reproductive development of tomato. Plos One 5:e14427 es_ES
dc.description.references Gómez P, Jamilena M, Capel J, Zurita S, Angosto T, Lozano R (1999) Stamenless, a tomato mutant with homeotic conversions in petals and stamens. Planta 209:172–179 es_ES
dc.description.references Gómez-Mena G, de Folter S, Costa MM, Angenent GC, Sablowski R (2005) Transcriptional program controlled by the floral homeotic gene AGAMOUS during early organogenesis. Development 132:429–438 es_ES
dc.description.references Gramzow L, Theissen G (2010) A hitchhiker’s guide to the MADS world of plants. Genome Biol 11:214–224 es_ES
dc.description.references Heijmans K, Ament K, Rijpkema AS, Zethof J, Wolters-Arts M, Gerats T, Vandenbussche M (2012) Redefining C and D in the petunia ABC. Plant Cell 24:2305–2317 es_ES
dc.description.references Henschel K, Kofuji R, Hasebe M, Saedler H, Münster T, Theissen G (2002) Two ancient classes of MIKC-type MADS-box genes are present in the Moss Physcomitrella patens. Mol Biol Evol 19:801–814 es_ES
dc.description.references Hoffman NE, Ko K, Milkowski D, Pichersky E (1991) Isolation and characterization of tomato cDNA and genomic clones encoding the ubiquitin gene ubi3. Plant Mo1 Biol 17:1189–1201 es_ES
dc.description.references Ishida BK, Jenkins SM, Say B (1998) Induction of AGAMOUS gene expression plays a key role in ripening of tomato sepals in vitro. Plant Mol Biol 36:733–739 es_ES
dc.description.references Itkin M, Seybold H, Breitel D, Rogachev I, Meir S, Aharoni A (2009) TOMATO AGAMOUS-LIKE 1 is a component of the fruit ripening regulatory network. Plant J 60:1081–1095 es_ES
dc.description.references Ito T, Wellmer F, Yu H, Das P, Ito N, Alves-Ferreira M, Riechmann JL, Meyerowitz EM (2004) The homeotic protein AGAMOUS controls microsporogenesis by regulation of SPOROCYTELESS. Nature 430:356–360 es_ES
dc.description.references Joubes J, Phan TH, Just D, Rothan C, Bergounioux C, Raymond P et al (1999) Molecular and biochemical characterization of the involvement of cyclin-dependent kinase a during the early development of tomato fruit. Plant Physiol 121:857–869 es_ES
dc.description.references Joubes J, Walsh D, Raymond P, Chevalier C (2000) Molecular characterization of the expression of distinct classes of cyclins during the early development of tomato fruit. Planta 211:430–439 es_ES
dc.description.references Kapoor M, Tsuda S, Tanaka Y, Mayama T, Okuyama Y, Tsuchimoto S, Takatsuji H (2002) Role of petunia pMADS3 in determination of floral organ and meristem identity, as reveal by its loss of function. Plant J 32:115–127 es_ES
dc.description.references Klee HJ, Giovannoni JJ (2011) Genetics and control of tomato fruit ripening and quality attributes. Annu Rev Genet 45:41–59 es_ES
dc.description.references Kofuji R, Sumikawa N, Yamasaki M, Kondo K, Ueda K, Ito M, Hasebe M (2003) Evolution and divergence of the MADS-box gene family based on genome-wide expression analyses. Mol Biol Evol 20:1963–1977 es_ES
dc.description.references Kramer EM, Jaramillo MA, Di Stilio VS (2004) Patterns of gene duplication and functional evolution during the diversification of the AGAMOUS subfamily of MADS box genes in angiosperms. Genetics 166:1011–1023 es_ES
dc.description.references Kramer EM, Dorit RL, Irish VF (1998) Molecular evolution of petal and stamen development, gene duplication and divergence within the APETALA3 and PISTILLATA MADS-box gene lineages. Genetics 149:765–783 es_ES
dc.description.references Leseberg CH, Eissler CL, Wang X, Johns MA, Duvall MR, Mao L (2008) Interaction study of MADS-domain proteins in tomato. J Exp Bot 59:2253–2265 es_ES
dc.description.references Liljegren SJ, Ditta GS, Eshed Y, Savidge B, Bowman JL, Yanofsky MF (2000) SHATTERPROOF MADS-box genes control seed dispersal in Arabidopsis. Nature 404:766–770 es_ES
dc.description.references Lozano R, Angosto T, Gomez P, Payán C, Capel J, Huijser P, Salinas J, Martínez-Zapater JM (1998) Tomato flower abnormalities induced by low temperatures are associated with changes of expression of MADS-box genes. Plant Physiol 117:91–100 es_ES
dc.description.references Mandel MA, Gustafson-Brown C, Savidge B, Yanofsky MF (1992) Molecular characterization of the Arabidopsis floral homeotic gene APETALA1. Nature 360:273–277 es_ES
dc.description.references Mazzucato A, Olimpieri I, Siligato F, Picarella ME, Soressi GP (2008) Characterization of genes controlling stamen identity and development in a parthenocarpic tomato mutant indicates a role for the DEFICIENS ortholog in the control of fruit set. Physiol Plant 132:526–537 es_ES
dc.description.references Meissner R, Jacobson Y, Melame S, Levyatuv S, Shalev G, Ashri A, Elkind Y, Levy A (1997) A new model system for tomato genetics. Plant J 12:1465–1472 es_ES
dc.description.references Mellway RD, Lund ST (2013) Interaction analysis of grapevine MIKCc-type MADS transcription factors and heterologous expression of putative véraison regulators in tomato. J Plant Physiol 170:1424–1433 es_ES
dc.description.references Ng M, Yanofsky MF (2000) Three ways to learn the ABCs. Curr Opin Plant Biol 3:47–52 es_ES
dc.description.references Pan IL, McQuinn R, Giovannoni JJ, Irish VF (2010) Functional diversification of AGAMOUS lineage genes in regulating tomato flower and fruit development. J Exp Bot 61:1795–1806 es_ES
dc.description.references Pina C, Pinto F, Feijó JA, Becker JD (2005) Gene family analysis of the Arabidopsis pollen transcriptome reveals biological implications for cell growth, division control, and gene expression regulation. Plant Physiol 138:744–756 es_ES
dc.description.references Pinyopich A, Ditta GS, Savidge B, Liljegren SJ, Baumann E, Wisman E, Yanofsky MF (2003) Assessing the redundancy of MADS-box genes during carpel and ovule development. Nature 424:85–88 es_ES
dc.description.references Pnueli L, Abu-Abeid M, Zamir D, Nacken W, Schwarz-Sommer Z, Lifschitz E (1991) The MADS box gene family in tomato: temporal expression during floral development, conserved secondary structures and homology with homeotic genes from Antirrhinum and Arabidopsis. Plant J 1:255–266 es_ES
dc.description.references Pnueli L, Hareven D, Rounsley SD, Yanofsky MF, Lifschitz E (1994) Isolation of the tomato AGAMOUS gene TAG1 and analysis of its homeotic role in transgenic plants. Plant Cell 6:163–173 es_ES
dc.description.references Quinet M, Bataille G, Dobrev PI, Capel C, Gómez P, Capel J, Lutts S, Motyka V, Angosto T, Lozano R (2014) Transcriptional and hormonal regulation of petal and stamen development by STAMENLESS, the tomato (Solanum lycopersicum L.) orthologue to the B-class APETALA3 gene. J Exp Bot 65:2243–2256 es_ES
dc.description.references Seymour GB, Ostergaard L, Chapman NH, Knapp S, Martin C (2013) Fruit development and ripening. Annu Rev Plant Biol 64:1–23 es_ES
dc.description.references Tadiello A, Pavanello A, Zanin D, Caporali E, Colombo L, Rotino GL, Trainotti L, Casadoro G (2009) A PLENA-like gene of peach is involved in carpel formation and subsequent transformation into a fleshy fruit. J Exp Bot 60:651–661 es_ES
dc.description.references Tani E, Polidoros AN, Tsaftaris AS (2007) Characterization and expression analysis of FRUITFULL- and SHATTERPROOF-like genes from peach (Prunus persica) and their role in split-pit formation. Tree Physiol 27:649–659 es_ES
dc.description.references Theissen G, Becker A, Di Rosa A, Kanno A, Kim JT, Münster T, Winter K-U, Saedler H (2000) A short history of MADS-box genes in plants. Plant Mol Biol 42:115–149 es_ES
dc.description.references Verelst W, Saedler H, Münster T (2007a) MIKC* MADS-protein complexes bind motifs enriched in the proximal region of late pollen-specific Arabidopsis promoters. Plant Physiol 143:447–460 es_ES
dc.description.references Verelst W, Twell D, de Folter S, Immink R, Saedler H, Munster T (2007b) MADS-complexes regulate transcriptome dynamics during pollen maturation. Genome Biol 8:R249 es_ES
dc.description.references Vrebalov J, Pan IL, Arroyo AJM, McQuinn R, Chung M, Poole M, Rose J, Seymour G, Grandillo S, Giovannoni J, Irish VF (2009) Fleshy fruit expansion and ripening are regulated by the tomato SHATTERPROOF gene TAGL1. Plant Cell 21:3041–3062 es_ES
dc.description.references Vrebalov J, Ruezinsky D, Padmanabhan V, White R, Medrano D, Drake R, Schuch W, Giovannoni J (2002) A MADS-box gene necessary for fruit ripening at the tomato ripening-inhibitor (rin) locus. Science 296:343–346 es_ES
dc.description.references Yanofsky MF, Ma H, Bowman JL, Drews GN, Feldmann KA, Meyerowitz EM (1990) The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors. Nature 346:35–39 es_ES


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