Skip to main content
SpringerLink
Log in

Variations on a theme in fruit development: the PLE lineage of MADS-box genes in tomato (TAGL1) and other species

  • Review
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

This article focuses on the role of TOMATO AGAMOUS-LIKE 1 (TAGL1) on a wide range of ripening functions in tomato. We also examine orthologs of this gene in related species that produce different fruit types and discuss some evolutionary implications.

TOMATO AGAMOUS-LIKE 1 (TAGL1) is a MADS-box transcription factor gene that belongs to the PLENA (PLE) lineage within the AGAMOUS (AG) clade. The most well-studied genes in this lineage are the SHATTERPROOF (SHP) genes in Arabidopsis, known to be involved in dehiscence zone formation during silique development. In tomato, TAGL1 has been shown to control several aspects of tomato fruit ripening. Most notably, carotenoid synthesis seems to be controlled by TAGL1, likely via the ethylene synthesis and signaling pathway and in combination with RIPENING INHIBITOR (RIN). In addition, TAGL1 regulates genes involved in cell cycle regulation, flavonoid and lignin biosynthesis, and cuticle development. We discuss many of the genes in these different pathways that are likely controlled by TAGL1, directly or indirectly. We also examine the relationship of TAGL1 with known and putative interaction partners. PLE lineage genes have also been examined in other species such as Antirrhinum, Petunia, and Nicotiana and provide an interesting example of conservation and diversification of function in species that produce very different types of fleshy and dry fruits. The control of lignification may be a common mechanism for this group of genes. Lastly, we discuss future work needed to elucidate the TAGL1 regulatory pathway in tomato and to help better understand the functional diversification of genes in this lineage in related species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Adapted from fruit anatomical depictions in Dinneny et al. (2005) and Pabon-Mora and Litt (2011)

Fig. 2

Modified from Pan et al. (2010)

Fig. 3

Similar content being viewed by others

References

  • Arnaud N, Lawrenson T, Ostergaard L, Sablowski R (2011) The same regulatory point mutation changed seed-dispersal structures in evolution and domestication. Curr Biol 21:1215–1219

    Article  CAS  PubMed  Google Scholar 

  • Bemer M, Karlova R, Ballester AR, Tikunov YM, Bovy AG, Wolters-Arts M, Rossetto Pde B, Angenent GC, de Maagd RA (2012) The tomato FRUITFULL homologs TDR4/FUL1 and MBP7/FUL2 regulate ethylene-independent aspects of fruit ripening. Plant Cell 24:4437–4451

    Article  CAS  PubMed  PubMed Central  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 

  • Bremer B, Eriksson O (1992) Evolution of fruit characters and dispersal modes in the tropical family Rubiaceae. Biol J Linn Soc 47:79–95

    Article  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 

  • Cheniclet C, Rong WY, Causse M, Frangne N, Bolling L, Carde JP, Renaudin JP (2005) Cell expansion and endoreduplication show a large genetic variability in pericarp and contribute strongly to tomato fruit growth. Plant Physiol 139:1984–1994

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dave YS, Patel ND, Rao KS (1981) Structural design of the developing fruit of Nicotiana tabacum. Phyton 21:63–71

    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 

  • Dinneny JR, Weigel D, Yanofsky MF (2005) A genetic framework for fruit patterning in Arabidopsis thaliana. Development 132:4687–4696

    Article  CAS  PubMed  Google Scholar 

  • Dreni L, Kater MM (2014) MADS reloaded: evolution of the AGAMOUS subfamily genes. New Phytol 201:717–732

    Article  CAS  PubMed  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 

  • Ferrándiz C, Fourquin C (2014) Role of the FUL-SHP network in the evolution of fruit morphology and function. J Exp Bot 65:4505–4513

    Article  PubMed  Google Scholar 

  • Ferrándiz C, Pelaz S, Yanofsky MF (1999) Control of carpel and fruit development in Arabidopsis. Annu Rev Biochem 68:321–354

    Article  PubMed  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 

  • Fourquin C, del Cerro C, Victoria FC, Vialette-Guiraud A, de Oliveira AC, Ferrándiz C (2013) A change in SHATTERPROOF protein lies at the origin of a fruit morphological novelty and a new strategy for seed dispersal in medicago genus. Plant Physiol 162:907–917

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujisawa M, Shima Y, Nakagawa H, Kitagawa M, Kimbara J, Nakano T, Kasumi T, Ito Y (2014) Transcriptional regulation of fruit ripening by tomato FRUITFULL homologs and associated MADS box proteins. Plant Cell 26:89–101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gillaspy G, Ben-David H, Gruissem W (1993) Fruits: a developmental perspective. Plant Cell 5:1439–1451

    Article  PubMed  PubMed Central  Google Scholar 

  • Gimenez E, Pineda B, Capel J, Anton MT, Atares 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 

  • Gimenez E, Dominguez E, Pineda B, Heredia A, Moreno V, Lozano R, Angosto T (2015) Transcriptional activity of the MADS Box ARLEQUIN/TOMATO AGAMOUS-LIKE1 gene is required for cuticle development of tomato fruit. Plant Physiol 168:1036–1048

    Article  PubMed  PubMed Central  Google Scholar 

  • Gimenez E, Castaneda L, Pineda B, Pan IL, Moreno 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 Mol Biol 91:513–531

    Article  CAS  PubMed  Google Scholar 

  • Gramzow L, Theissen G (2010) A hitchhiker’s guide to the MADS world of plants. Genome Biol 11:1–11

    Article  Google Scholar 

  • Gustafson-Brown C, Savidge B, Yanofsky MF (1994) Regulation of the arabidopsis floral homeotic gene APETALA1. Cell 76:131–143

    Article  CAS  PubMed  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 

  • Hileman LC, Sundstrom JF, Litt A, Chen M, Shumba T, Irish VF (2006) Molecular and phylogenetic analyses of the MADS-box gene family in tomato. Mol Biol Evol 23:2245–2258

    Article  CAS  PubMed  Google Scholar 

  • Honma T, Goto K (2001) Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature 409:525–529

    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 

  • 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 

  • Knapp S (2002) Tobacco to tomatoes: a phylogenetic perspective on fruit diversity in the Solanaceae. J Exp Bot 53:2001–2022

    Article  CAS  PubMed  Google Scholar 

  • Knapp S, Litt A (2013) Fruit-an angiosperm innovation. In: Seymour GB, Poole M, Giovannoni JJ, Tucker GA (eds) The molecular biology and biochemistry of fruit ripening. Wiley-Blackwell, New York, pp 28–42

    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 

  • 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 

  • Liljegren SJ, Roeder AH, Kempin SA, Gremski K, Ostergaard L, Guimil S, Reyes DK, Yanofsky MF (2004) Control of fruit patterning in Arabidopsis by INDEHISCENT. Cell 116:843–853

    Article  CAS  PubMed  Google Scholar 

  • Ma H, Yanofsky MF, Meyerowitz EM (1991) AGL1-AGL6, an Arabidopsis gene family with similarity to floral homeotic and transcription factor genes. Genes Dev 5:484–495

    Article  CAS  PubMed  Google Scholar 

  • Martel C, Vrebalov J, Tafelmeyer P, Giovannoni JJ (2011) The tomato MADS-box transcription factor RIPENING INHIBITOR interacts with promoters involved in numerous ripening processes in a COLORLESS NONRIPENING-dependent manner. Plant Physiol 157:1568–1579

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Olmstead RG, Bohs L, Migid HA, Santiago-Valentín E, Garcia VF, Collier SM (2008) A molecular phylogeny of the Solanaceae. Taxon 57:1159–1181

    Google Scholar 

  • Pabon-Mora N, Litt A (2011) Comparative anatomical and developmental analysis of dry and fleshy fruits of Solanaceae. Am J Bot 98:1415–1436

    Article  PubMed  Google Scholar 

  • Pabon-Mora N, Wong GK, Ambrose BA (2014) Evolution of fruit development genes in flowering plants. Front Plant Sci 5:300

    PubMed  PubMed Central  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 

  • Pineda B, Gimenez-Caminero E, Garcia-Sogo B, Anton MT, Atares A, Capel J, Lozano R, Angosto T, Moreno V (2010) Genetic and physiological characterization of the arlequin insertional mutant reveals a key regulator of reproductive development in tomato. Plant Cell Physiol 51:435–447

    Article  CAS  PubMed  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, 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 

  • Rajani S, Sundaresan V (2001) The Arabidopsis myc/bHLH gene ALCATRAZ enables cell separation in fruit dehiscence. Curr Biol 11:1914–1922

    Article  CAS  PubMed  Google Scholar 

  • Roeder AH, Ferrándiz C, Yanofsky MF (2003) The role of the REPLUMLESS homeodomain protein in patterning the Arabidopsis fruit. Curr Biol 13:1630–1635

    Article  CAS  PubMed  Google Scholar 

  • Sato T, Theologis A (1989) Cloning the mRNA encoding 1-aminocyclopropane-1-carboxylate synthase, the key enzyme for ethylene biosynthesis in plants. Proc Natl Acad Sci USA 86:6621–6625

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shima Y, Kitagawa M, Fujisawa M, Nakano T, Kato H, Kimbara J, Kasumi T, Ito Y (2013) Tomato FRUITFULL homologues act in fruit ripening via forming MADS-box transcription factor complexes with RIN. Plant Mol Biol 82:427–438

    Article  CAS  PubMed  Google Scholar 

  • Spence J, Vercher Y, Gates P, Harris N (1996) ‘Pod shatter’ in Arabidopsis thaliana, Brassica napus and B. juncea. J Microsc 181:195–203

    Article  Google Scholar 

  • Spujt RW (1994) A systematic treatment of fruit types. Mem NY Bot Gard 70:1–81

    Google Scholar 

  • Tanksley SD (2004) The genetic, developmental, and molecular bases of fruit size and shape variation in tomato. Plant Cell 16(Suppl):S181–S189

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tigchelaar EC, McGlasson WB, Buescher RW (1978) Genetic regulation of tomato fruit ripening. HortScience 13:508–513

    CAS  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 

  • Vrebalov J, Pan IL, Arroyo AJ, 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 

  • 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 

Download references

Author information

Authors and Affiliations

  1. Department of Botany and Plant Sciences, University of California, Riverside, CA, 92521, USA

    Danielle C. Garceau

  2. MassBiologics, Boston, MA, 02126, USA

    Megan K. Batson

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

    Irvin L. Pan

Authors
  1. Danielle C. Garceau
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Megan K. Batson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Irvin L. Pan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Irvin L. Pan.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Garceau, D.C., Batson, M.K. & Pan, I.L. Variations on a theme in fruit development: the PLE lineage of MADS-box genes in tomato (TAGL1) and other species. Planta 246, 313–321 (2017). https://doi.org/10.1007/s00425-017-2725-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-017-2725-5

Keywords

Search

Navigation