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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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Abstract

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.

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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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Bowman JL, Smyth DR, Meyerowitz EM (1989) Genes directing flower development in Arabidopsis. Plant Cell 1:37–52

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bowman JL, Smyth DR, Meyerowitzt EM (1991) Genetic interactions among floral homeotic genes of Arabidopsis. Development 112:1–20

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Carpenter R, Coen ES (1990) Floral homeotic mutations produced by transposon-mutagenesis in Antirrhinum majus. Genes Dev 4:1483–1493

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Coen E, Meyerowitz EM (1991) The war of the whorls: genetic interactions controlling flower development. Nature 353:31–37

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Gramzow L, Theissen G (2010) A hitchhiker’s guide to the MADS world of plants. Genome Biol 11:214–224

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Klee HJ, Giovannoni JJ (2011) Genetics and control of tomato fruit ripening and quality attributes. Annu Rev Genet 45:41–59

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mandel MA, Gustafson-Brown C, Savidge B, Yanofsky MF (1992) Molecular characterization of the Arabidopsis floral homeotic gene APETALA1. Nature 360:273–277

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Ng M, Yanofsky MF (2000) Three ways to learn the ABCs. Curr Opin Plant Biol 3:47–52

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seymour GB, Ostergaard L, Chapman NH, Knapp S, Martin C (2013) Fruit development and ripening. Annu Rev Plant Biol 64:1–23

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors also thank research facilities provided by the Campus de Excelencia Internacional CeiA3. We thank Dr. F. J. Yuste-Lisbona for critical reading of the manuscript.

Funding

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.).

Author contributions

E. G. conducted the experiments, assisted in data interpretation and drafted the manuscript. L. C. collaborated in the experimental work. B. P. and V. M. generated transgenic plants and collaborated in genetic analyses. I. L. P. contributed to a critical review of the manuscript. T. A. assisted in data analysis and reviewed the manuscript. R. L. planned the research work, assisted in data interpretation, and edited the manuscript. All authors have read and approved the final manuscript.

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Authors and Affiliations

  1. Centro de Investigación en Biotecnología Agroalimentaria (BITAL), Universidad de Almería, 04120, Almería, Spain

    Estela Gimenez, Laura Castañeda, Trinidad Angosto & Rafael Lozano

  2. Instituto de Biología Molecular y Celular de Plantas (UPV-CSIC), Universidad Politécnica de Valencia, 46022, Valencia, Spain

    Benito Pineda & Vicente Moreno

  3. Department of Biology, Stonehill College, 320 Washington Street, Easton, MA, 02357, USA

    Irvin L. Pan

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  1. Estela Gimenez
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  2. Laura Castañeda
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  4. Irvin L. Pan
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  6. Trinidad Angosto
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  7. Rafael Lozano
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Correspondence to Rafael Lozano.

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Gimenez, E., Castañeda, L., Pineda, B. et al. TOMATO AGAMOUS1 and ARLEQUIN/TOMATO AGAMOUS-LIKE1 MADS-box genes have redundant and divergent functions required for tomato reproductive development. Plant Mol Biol 91, 513–531 (2016). https://doi.org/10.1007/s11103-016-0485-4

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