Skip to main content

Phenotypic and genetic characterization of the pistillate mutation in tomato

Abstract

Many floral phenotypes have been described in decades of tomato genetics, but for very few of them the underlying genes have been identified so far. Because the increasing availability of genome sequence data will facilitate forward genetics in tomato, novel descriptive and map information will help the attribution of genes to phenotypes. In this contribution, we present our work on pistillate (pi), a genotype that directly recalls mutations affecting class B MADS-box genes, but that has not been further characterized after the first description. Plants homozygous for the pi allele appear with Mendelian proportions and, compared to wild-type, show delayed flowering, a frequently modified sympodial segment, higher occurrence of compound inflorescences, and reversion of the floral meristem to vegetative identity. In pi mutant flowers, the most striking aberration is the homeotic transformation of stamens into carpels. Ultrastructural analysis also reveals more or less subtle sepaloid features in the three inner floral whorls, mainly based on the presence, distribution and amount of glandular and non glandular trichomes. In the ovary, a ‘flower within flower’ phenotype was seldom observed; in one instance such phenotype was coupled with the setting of a parthenocarpic fruit, that reiterated the differentiation of a new flower. Mapping experiments positioned PI on the distal end of the long arm of chromosome 3. This position was not compatible with any class B or E MADS box gene; differently, the PI genetic window contained the FALSIFLORA (FA) gene, the tomato orthologue of LEAFY (LFY). The pi defects in flowering time and inflorescence development are in agreement with a direct involvement of the floral meristem identity gene. The class B- and E-like phenotypes shown by pi mutant plants are likely an indirect consequence because FA, as LFY, is reported as a positive regulator of homeotic MADS-box genes. Because fa mutant plants do not form complete flowers, the pi mutation deserves a particular interest, producing four-whorled, although modified, flowers useful to study the functional linkage between flower induction and flower organ identity specification.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  • Allen KD, Sussex IM (1996) Falsiflora and anantha control early stages of floral meristem development in tomato (Lycopersicon esculentum Mill.). Planta 200:254–264

    Article  Google Scholar 

  • Ampomah-Dwamena C, Morris B, Sutherland P, Veit B, Yao J-L (2002) Down-regulation of TM29, a tomato SEPALLATA homolog, causes parthenocarpic fruit development and floral reversion. Plant Physiol 130:605–617

    PubMed  Article  CAS  Google Scholar 

  • Beraldi D, Picarella ME, Soressi GP, Mazzucato A (2004) Fine mapping of the parthenocarpic fruit (pat) mutation in tomato. Theor Appl Genet 108:209–216

    PubMed  Article  CAS  Google Scholar 

  • Blázquez M, Soowal L, Lee I, Weigel D (1997) LEAFY expression and flower initiation in Arabidopsis. Development 124:3835–3844

    PubMed  Google Scholar 

  • Bomblies K, Wang R-L, Ambrose BA, Schmidt RJ, Meeley RB, Doebley J (2003) Duplicate FLORICAULA/LEAFY homologs zfl1 and zfl2 control inflorescence architecture and flower patterning in maize. Development 130:2385–2395

    PubMed  Article  CAS  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

    PubMed  Article  CAS  Google Scholar 

  • Causse M, Duffe P, Gomez MC, Buret M, Damidaux R, Zamir D, Gur A, Chevalier C, Lemaire-Chamley M, Rothan C (2004) A genetic map of candidate genes and QTLs involved in tomato fruit size and composition. J Exp Bot 55:1671–1685

    PubMed  Article  CAS  Google Scholar 

  • Carpenter R, Copsey L, Vincent C, Doyle S, Magrath R, Coen E (1995) Control of flower development and phyllotaxy by meristem identity genes in Antirrhinum. Plant Cell 7:2001–2011

    PubMed  Article  CAS  Google Scholar 

  • Chandra Sekhar KN, Sawhney VK (1984) A scanning electron microscope study of the development and surface features of floral organs of tomato (Lycopersicon esculentum). Can J Bot 62:2403–2413

    Article  Google Scholar 

  • Chetelat RT (2005) Revised list of miscellaneous stocks. Tomato Genet Coop 55:48–69

    Google Scholar 

  • Coen ES, Romero JM, Doyle S, Elliott R, Murphy G, Carpenter R (1990) floricaula: a homeotic gene required for flower development in Antirrhinum majus. Cell 63:1311–1322

    PubMed  Article  CAS  Google Scholar 

  • Colombo L, Franken J, Koetje E, van Went J, Dons HJM, Angenent GC, van Tunen AJ (1995) The Petunia MADS box gene FBP11 determines ovule identity. Plant Cell 7:1859–1868

    PubMed  Article  CAS  Google Scholar 

  • de Martino G, Pan I, Emmanuel E, Levy A, Irish VF (2006) Functional analyses of two tomato APETALA3 genes demonstrate diversification in their roles in regulating floral development. Plant Cell 18:1833–1845

    PubMed  Article  Google Scholar 

  • Ditta G, Pinyopich A, Robles P, Pelaz S, Yanofsky MF (2004) The SEP4 gene of Arabidopsis thaliana functions in floral organ and meristem identity. Curr Biol 14:1935–1940

    PubMed  Article  CAS  Google Scholar 

  • Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15

    Google Scholar 

  • Eshed Y, Zamir D (1994) A genomic library of Lycopersicon pennellii in L. esculentum: a tool for fine mapping of genes. Euphytica 79:175–179

    Article  CAS  Google Scholar 

  • Ferrario S, Immink RGH, Shchennikova A, Busscher-Lange J, Angenent GC (2003) The MADS box gene FBP2 is required for SEPALLATA function in Petunia. Plant Cell 15:914–925

    PubMed  Article  CAS  Google Scholar 

  • Giovannoni J, Noensie E, Ruezinsky D, Lu X, Tracy S, Ganal M, Martin G, Pillen K, Albert K, Tankslev SD (1995) Molecular genetic analysis of the ripening-inhibitor and non-ripening loci of tomato: a first step in genetic map-based cloning of fruit ripening genes. Mol Gen Genet 248:195–206

    PubMed  Article  CAS  Google Scholar 

  • Giovannoni JJ (2007) Fruit ripening mutants yield insights into ripening control. Curr Opin Plant Biol 10:283–289

    PubMed  Article  CAS  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

    PubMed  Article  Google Scholar 

  • Grandillo S, Ku HM, Tanksley SD (1999) Identifying the loci responsible for natural variation in fruit size and shape in tomato. Theor Appl Genet 99:978–987

    Article  CAS  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

    PubMed  Article  CAS  Google Scholar 

  • Hofer J, Turner L, Hellens R, Ambrose M, Matthews P, Michael A, Ellis N (1997) UNIFOLIATA regulates leaf and flower morphogenesis in pea. Curr Biol 7:581–587

    PubMed  Article  CAS  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

  • Huala E, Sussex IM (1992) LEAFY interacts with floral homeotic genes to regulate Arabidopsis floral development. Plant Cell 4:901–913

    PubMed  Article  Google Scholar 

  • Kato K, Ohta K, Komata Y, Araki T, Kanahama K, Kanayama Y (2005) Morphological and molecular analyses of the tomato floral mutant leafy inflorescence, a new allele of falsiflora. Plant Sci 169:131–138

    Article  CAS  Google Scholar 

  • Lamb RS, Hill TA, Tan QKG, Irish VF (2002) Regulation of APETALA3 floral homeotic gene expression by meristem identity genes. Development 129:2079–2086

    PubMed  CAS  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

    PubMed  Article  CAS  Google Scholar 

  • Lifschitz E, Brodai L, Hareven D, Hurwitz C, Prihadash A, Pnueli L, Samach A, Zamir D (1993) Molecular mapping of flower development in tomato. In: Yoder J (ed) Molecular biology of tomato. Technomic Publishing Company Incorporated, Lancaster, pp 175–184

    Google Scholar 

  • Lifschitz E, Eviatar T, Rozman A, Shalit A, Goldshmidt A, Amsellem Z, Alvarez JP, Eshed Y (2006) The tomato FT ortholog triggers systemic signals that regulate growth and flowering and substitute for diverse environmental stimuli. Proc Natl Acad Sci USA 103:6398–6403

    PubMed  Article  CAS  Google Scholar 

  • Malcomber ST, Kellogg EA (2005) SEPALLATA gene diversification: brave new whorls. Trends Plant Sci 10:427–435

    PubMed  Article  CAS  Google Scholar 

  • Mazzucato A, Taddei AR, Soressi GP (1998) The parthenocarpic fruit (pat) mutant of tomato (Lycopersicon esculentum Mill.) sets seedless fruits and has aberrant anther and ovule development. Development 125:107–114

    PubMed  CAS  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

    PubMed  Article  CAS  Google Scholar 

  • Menda N, Semel Y, Peled D, Eshed Y, Zamir D (2004) In silico screening of a saturated mutation library of tomato. Plant J 38:861–872

    PubMed  Article  CAS  Google Scholar 

  • Molinero-Rosales N, Jamilena M, Zurita S, Gomez P, Capel J, Lozano R (1999) FALSIFLORA, the tomato orthologue of FLORICAULA and LEAFY, controls flowering time and floral meristem identity. Plant J 20:685–693

    PubMed  Article  CAS  Google Scholar 

  • Paran I, van der Knaap E (2007) Genetic and molecular regulation of fruit and plant domestication traits in tomato and pepper. J Exp Bot 58:3841–3852

    PubMed  Article  CAS  Google Scholar 

  • Parcy F, Nilsson O, Busch MA, Lee L, Weigel D (1998) A genetic framework for floral patterning. Nature 395:561–566

    PubMed  Article  CAS  Google Scholar 

  • Pelaz S, Gustafson-Brown C, Kohalmi SE, Crosby WL, Yanofsky MF (2001) APETALA1 and SEPALLATA3 interact to promote flower development. Plant J 26:385–394

    PubMed  Article  CAS  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

    PubMed  Article  CAS  Google Scholar 

  • Pnueli L, Hareven D, Broday L, Hurwitz C, Lifschitz E (1994a) The TM5 MADS box gene mediates organ differentiation in the three inner whorls of tomato flowers. Plant Cell 6:175–186

    PubMed  Article  CAS  Google Scholar 

  • Pnueli L, Hareven D, Rounsley SD, Yanofsky MF, Lifschitz E (1994b) Isolation of the tomato AGAMOUS gene TAG1 and analysis of its homeotic role in transgenic plants. Plant Cell 6:163–173

    PubMed  Article  CAS  Google Scholar 

  • Pnueli L, Carmel-Goren L, Hareven D, Gutfinger T, Alvarez J, Ganal M, Zamir D, Lifschitz E (1998) The SELF-PRUNING gene of tomato regulates vegetative to reproductive switching of sympodial meristems and is the ortholog of CEN and TFL1. Development 125:1979–1989

    PubMed  CAS  Google Scholar 

  • Quinet M, Dubois C, Goffin M-C, Chao J, Dielen V, Batoko H, Boutry M, Kinet J-M (2006) Characterization of tomato (Solanum lycopersicum L.) mutants affected in their flowering time and in the morphogenesis of their reproductive structure. J Exp Bot 57:1381–1390

    PubMed  Article  CAS  Google Scholar 

  • Rasmussen N, Green PB (1993) Organogenesis in flowers of the homeotic green pistillate mutant of tomato (Lycopersicon esculentum). Am J Bot 80:805–813

    Article  Google Scholar 

  • Rick CM (1993) pi-2—a novel pistillate mutant. Tomato Genet Coop Rep 43:40

    Google Scholar 

  • Rick CM, Robinson J (1951) Inherited defects of floral structure affecting fruitfulness in Lycopersicon esculentum. Am J Bot 38:639–652

    Article  Google Scholar 

  • Samach A, Lotan H (2007) The transition to flowering in tomato. Plant Biotechnol 24:71–82

    Google Scholar 

  • Sawhney VK (1992) Floral mutants in tomato: development, physiology and evolutionary implications. Can J Bot 70:701–707

    Google Scholar 

  • Schultz EA, Haughn GW (1991) LEAFY, a homeotic gene that regulates inflorescence development in Arabidopsis. Plant Cell 3:771–781

    PubMed  Article  Google Scholar 

  • Schultz EA, Haughn GW (1993) Genetic analysis of the floral initiation process (FLIP) in Arabidopsis. Development 119:745–765

    CAS  Google Scholar 

  • Simmons AT, Gurr GM, McGrath D, Nicol HI, Martin PM (2003) Trichomes of Lycopersicon spp. and their effect on Myzus persicae (Sulzer) (Hemiptera: Aphididae. Austr J Entomol 42:373–378

    Article  Google Scholar 

  • Souer E, van der Krol A, Kloos D, Spelt C, Bliek M, Mol J, Koes R (1998) Genetic control of branching pattern and floral identity during Petunia inflorescence development. Development 125:733–742

    PubMed  CAS  Google Scholar 

  • Theißen G (2001) Development of floral organ identity: stories from the MADS house. Curr Opin Plant Biol 4:75–85

    PubMed  Article  Google Scholar 

  • Van Ooijen JW, Voorrips RE (2001) JoinMap® 3.0 software for calculation of genetic linkage maps. Plant Research International, Wageningen

    Google Scholar 

  • Vandenbussche M, Zethof J, Souer E, Koes R, Tornielli GB, Pezzotti M, Ferrario S, Angenent GC, Gerats T (2003) Toward the analysis of the Petunia MADS box gene family by reverse and forward transposon insertion mutagenesis approaches: B, C, and D floral organ identity functions require SEPALLATA-Like MADS box genes in Petunia. Plant Cell 15:2680–2693

    PubMed  Article  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

    PubMed  Article  CAS  Google Scholar 

  • Wang H, Chen J, Wen J, Tadege M, Li G, Liu Y, Mysore KS, Ratet P, Chen R (2008) Control of compound leaf development by FLORICAULA/LEAFY ortholog SINGLE LEAFLET1 in Medicago truncatula. Plant Physiol 146:1759–1772

    PubMed  Article  CAS  Google Scholar 

  • Weigel D, Alvarez J, Smyth DR, Yanofsky MF, Meyerowitz EM (1992) LEAFY controls floral meristem identity in Arabidopsis. Cell 69:843–860

    PubMed  Article  CAS  Google Scholar 

  • Weigel D, Meyerowitz EM (1993) Activation of floral homeotic genes in Arabidopsis. Science 261:1723–1726

    PubMed  Article  CAS  Google Scholar 

  • Weigel D, Meyerowitz EM (1994) The ABCs of floral homeotic genes. Cell 78:203–209

    PubMed  Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors wish to thank the Tomato Genetic Resource Center, Davis (CA, USA) for providing the seed stocks, Dr. Maria Maddalena Altamura, Prof. Gian Piero Soressi and two anonymous reviewers for critical reading of the manuscript, Pietro Mosconi, Fabrizio Ruiu and Maurizio Enea Picarella for expert technical assistance, and Anna Rita Taddei for the help with the electron microscopy facilities. This research work was funded by the Italian Ministry for University and Research, project No. 2004071420, “Genetic dissection of the processes controlling male fertility: a basis for the development of male sterile plants”.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Andrea Mazzucato.

Additional information

Communicated by I. Paran.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Olimpieri, I., Mazzucato, A. Phenotypic and genetic characterization of the pistillate mutation in tomato. Theor Appl Genet 118, 151–163 (2008). https://doi.org/10.1007/s00122-008-0884-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-008-0884-2

Keywords

  • Floral Organ
  • Floral Meristem
  • Glandular Hair
  • Floral Organ Identity
  • Parthenocarpic Fruit