Genetic and physiological characterization of the arlequin insertional mutant reveals a key regulator of reproductive development in Tomato

Plant and Cell Physiology

Volumn 51, Issue 3, 2010, Pages 435-447

  Pineda, Benito ^a   Giménez Caminero, Estela ^b   García Sogo, Begoña ^a   Antón, Mara Teresa ^a   Atarés, Alejandro ^a   Capel, Juan ^b   Lozano, Rafael ^b   Angosto, Trinidad ^b   Moreno, Vicente ^a  

^a Ciudad Politécnica de la Innovación   (Spain)

^b UNIVERSITY OF ALMERÍA   (Spain)

Author keywords

Arlequin; Fruit ripening; Insertional mutant; Reproductive development; Solanum lycopersicum; Tomato

Indexed keywords

BACTERIAL DNA; PLANT DNA; T DNA; T-DNA;

ARTICLE; FLOWER; FRUIT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; INHERITANCE; MUTATION; PHENOTYPE; SCANNING ELECTRON MICROSCOPY; TOMATO;

DNA, BACTERIAL; DNA, PLANT; FLOWERS; FRUIT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; INHERITANCE PATTERNS; LYCOPERSICON ESCULENTUM; MICROSCOPY, ELECTRON, SCANNING; MUTAGENESIS, INSERTIONAL; MUTATION; PHENOTYPE;

LYCOPERSICON ESCULENTUM; SOLANUM;

EID: 77949393185     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcq009     Document Type: Article

References (67)

1. Adams-Phillips, L., Barry, C. and Giovannoni, J. (2004) Signal transduction systems regulating fruit ripening. Trends Plant Sci. 9: 331-338.
2. Alonso, J.M., Stepanova, A.N., Leisse, T.J., Kim, C.J., Chen, H.M., Shinn, P., et al. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657.
3. Alvarez-Buylla, E.R., Liljegren, S.J., Pelaz, S., Gold, S.E., Burgeff, C., Ditta, G.S., et al. (2000) MADS-box gene evolution beyond fl owers: expression in pollen, endosperm, guard cells, roots and trichomes. Plant J. 24: 457-466.
4. An, S.Y., Park, S., Jeong, D.H., Lee, D.Y., Kang, H.G., Yu, J.H., et al. (2003) Generation and analysis of end sequence database for T-DNA tagging lines in rice. Plant Physiol. 133: 2040-2047.
5. Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A., et al. (1995) Current Protocols in Molecular Biology. John Wiley and Sons, London.
6. Bishop, G.J., Harrison, K. and Jones, J.D.G. (1996) The tomato Dwarf gene isolated by heterologous transposon tagging encodes the first member of a new cytochrome P450 family. Plant Cell 8: 959-969.
7. Busi, M.V., Bustamante, C., D'Angelo, C., Hidalgo-Cuevas, M., Boggio, S.B., Valle, E.M., et al. (2003) MADS-box genes expressed during tomato seed and fruit development. Plant Mol. Biol. 5 2: 801-815.
8. Carrari, F., Asis, R. and Fernie, A.R. (2007) The metabolic shifts underlying tomato fruit development. Plant Biotechnol. 24: 45-55.
9. Chen, S.Y., Jin, W.Z., Wang, M.Y., Zhang, F., Zhou, J., Jia, O.J., et al. (2003) Distribution and characterization of over 1000 T-DNA tags in rice genome. Plant J. 36: 105-113.
10. Cong, B., Barrero, L.S. and Tanksley, S.D. (2008) Regulatory change in YABBY-like transcription factor led to evolution of extreme fruit size during tomato domestication. Nat. Genet. 40: 800-804.
11. De Bodt, S., Theissen, G. and Van de Peer, Y. (2006) Promoter analysis of MADS-box genes in eudicots through phylogenetic footprinting. Mol. Biol. Evol. 23: 1293-1303.
12. De Jong, M., Mariani, C. and Vriezen, W.H. (2009) The role of auxin and gibberellin in tomato fruit set. J. Exp. Bot. 60: 1523-1532.
13. De Martino, G., Pan, I., Emmanuel, E., Levy, A. and Irish, V.F. (2006) Functional analyses of two tomato APETALA3 genes demonstrate diversifi cation in their roles in regulating floral development. Plant Cell 18: 1833-1845.
14. Ellul, P., Garcia-Sogo, B., Pineda, B., Rios, G., Roig, L.A. and Moreno, V. (2003) The ploidy level of transgenic plants in Agrobacterium-mediated transformation of tomato cotyledons (Lycopersicon esculentum L.Mill.) is genotype and procedure dependent. Theor. Appl. Genet. 106: 231-238.
15. Emmanuel, E. and Levy, A.A. (2002) Tomato mutants as tools for functional genomics. Curr. Opin. Plant Biol. 5: 112-117.
16. Fei, Z.J., Tang, X., Alba, R.M., White, J.A., Ronning, C.M., Martin, G.B., et al. (2004) Comprehensive EST analysis of tomato and comparative genomics of fruit ripening. Plant J. 40: 47-59.
17. Galpaz, N., Ronen, G., Khalfa, Z., Zamir, D. and Hirschberg, J. (2006) A chromoplast-specifi c carotenoid biosynthesis pathway is revealed by cloning of the tomato white-flower locus. Plant Cell 18: 1947-1960.
18. Genard, M., Bertin, N., Borel, C., Bussieres, P., Gautier, H., Habib, R., et al. (2007) Towards a virtual fruit focusing on quality: modelling features and potential uses. J. Exp. Bot. 58: 917-928.
19. Gillaspy, G., Ben-David, H. and Gruissem, W. (1993) Fruits: a developmental perspective. Plant Cell. 5: 1439-1451.
20. Giovannoni, J. (2004) Genetic regulation of fruit development and ripening. Plant Cell 16: S170-S180.
21. Giovannoni, J. (2007) Fruit ripening mutants yield insights into ripening control. Curr. Opin. Plant Biol. 10: 283-289.
22. Hileman, L.C., Sundstrom, J.F., Litt, A., Chen, M.Q., Shumba, T. and Irish, V.F. (2006) Molecular and phylogenetic analyses of the MADS-box gene family in tomato. Mol. Biol. Evol. 23: 2245-2258.
23. Ho, L.C. (1996) The mechanism of assimilate partitioning and carbohydrate compartmentation in fruit in realtion to the quality and yield of tomato. J. Exp. Bot. 47: 1239-1243.
24. Hoffman, N.E., Ko, K., Milkowski, D. and Pichersky, E. (1991) Isolation and characterization of tomato cDNA and genomic clones encoding the ubiquitin gene ubi3. Plant Mol. Biol. 17: 1189-1201.
25. Irish, V.F. (2003) The evolution of fl oral homeotic gene function. Bioessays 25: 637-646.
26. Jack, T. (2004) Molecular and genetic mechanisms of floral control. Plant Cell 16: S1-S17.
27. Jeong, D.H., An, S.Y., Kang, H.G., Moon, S., Han, J.J., Park, S., et al. (2002) T-DNA insertional mutagenesis for activation tagging in rice. Plant Physiol. 130: 1636-1644.
28. Jones, D.A., Thomas, C.M., Hammondkosack, K.E., Balintkurti, P.J. and Jones, J.D.G. (1994) Isolation of the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging. Science 266: 789-793.
29. Keddie, J.S., Carroll, B., Jones, J.D.G. and Gruissem, W. (1996) The DCL gene of tomato is required for chloroplast development and palisade cell morphogenesis in leaves. EMBO J. 15: 4208-4217.
30. Klann, E.M., Chetelat, R.T. and Bennett, A.B. (1993) Expression of acid invertase gene controls sugar composition in tomato (Lycopersicon) fruit. Plant Physiol. 103: 863-870.
31. Kramer, E.M., Dorit, R.L. and Irish, V.F. (1998) Molecular evolution of genes controlling petal and stamen development: duplication and divergence within the APETALA3 and PISTILLATA MADS-box gene lineages. Genetics 149: 765-783.
32. Krysan, P.J., Young, J.C. and Sussman, M.R. (1999) T-DNA as an insertional mutagen in Arabidopsis. Plant Cell 11: 2283-2290.
33. Ku, H.M., Liu, J., Doganlar, S. and Tanksely, S.D. (2001) Exploitation of Arabidopsis-tomato synteny to construct a high-resolution map of the ovate-containing region in tomato chromosome 2. Genome 44: 470-475.
34. Lanfermeijer, F.C., Dijkhuis, J., Sturre, M.J.G., de Haan, P. and Hille, J. (2003) Cloning and characterization of the durable tomato mosaic virus resistance gene Tm-2(2) from Lycopersicon esculentum. Plant Mol. Biol. 52: 1037-1049.
35. Leseberg, C.H., Eissler, C.L., Wang, X., Johns, M.A., Duvall, M.R. and Mao, L. (2008) Interaction study of MADS-domain proteins in tomato. J. Exp. Bot. 59: 2253-2265.
36. Li, Y., Rosso, M.G., Strizhov, N., Viehoever, P. and Weisshaar, B. (2003) GABI-Kat SimpleSearch: a fl anking sequence tag (FST) database for the identifi cation of T-DNA insertion mutants in Arabidopsis thaliana. Bioinformatics 19: 1441-1442.
37. Liu, J.P., Van Eck, J., Cong, B. and Tanksley, S.D. (2002) A new class of regulatory genes underlying the cause of pear-shaped tomato fruit. Proc. Natl Acad. Sci. USA 99: 13302-13306.
38. Lozano, R., Giménez-Caminero, E., Cara, B., Capel, J. and Angosto, T. (2009) Genetic analysis of reproductive development in tomato. Int. J. Dev. Biol. 53: 1635-1648.
39. Manning, K., Tor, M., Poole, M., Hong, Y., Thompson, A.J., King, G.J., et al. (2006) A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nat. Genet. 38: 948-952.
40. Mao, L., Begum, D., Chuang, H.W., Budiman, M.A., Szymkowiak, E.J., Irish, E.E., et al. (2000) JOINTLESS is a MADS-box gene controlling tomato fl ower abscission zone development. Nature 406: 910-913.
41. Mathews, H., Clendennen, S.K., Caldwell, C.G., Liu, X.L., Connors, K., Matheis, N., et al. (2003) Activation tagging in tomato identifies a transcriptional regulator of anthocyanin biosynthesis, modifi cation, and transport. Plant Cell 15: 1689-1703.
42. Murashige, T. and Skoog, F. (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol. Plant. 15: 473-497.
43. Nagy, R., Karandashov, V., Chague, W., Kalinkevich, K., Tamasloukht, M., Xu, G.H., et al. (2005) The characterization of novel mycorrhiza-specifi c phosphate transporters from Lycopersicon esculentum and Solanum tuberosum uncovers functional redundancy in symbiotic phosphate transport in solanaceous species. Plant J. 4 2: 236-250.
44. Pinyopich, A., Ditta, G.S., Savidge, B., Liljegren, S.J., Baumann, E., Wisman, E., et al. (2003) Assessing the redundancy of MADS-box genes during carpel and ovule development. Nature 424: 85-88.
45. Pnueli, L., Hareven, A.D., Rounsley, S.D., Yanofsky, M.F. and Lifschitz, E. (1994) Isolation of the tomato AGAMOUS gene TAG1 and analysis of its homeotic role in transgenic plants. Plant Cell 6: 163-173.
46. Quinet, M., Dubois, C., Goffin, M.C., Chao, J., Dielen, V., Batoko, H., et al. (2006) Characterization of tomato (Solanum lycopersicum L.) mutants affected in their fl owering time and in the morphogenesis of their reproductive structure. J. Exp. Bot. 57: 1381-1390.
47. Ronen, G., Cohen, M., Zamir, D. and Hirschberg, J. (1999) Regulation of carotenoid biosynthesis during tomato fruit development: expression of the gene for lycopene epsilon-cyclase is down-regulated during ripening and is elevated in the mutant Delta. Plant J. 17: 341-351.
48. Samach, A. and Lotan, H. (2007) The transition to flowering in tomato. Plant Biotechnol. 24: 71-82.
49. Scholte, M., d'Erfurth, I., Rippa, S., Mondy, S., Cosson, V., Durand, P., et al. (2002) T-DNA tagging in the model legume Medicago truncatula allows effi cient gene discovery. Mol. Breed. 10: 203-215.
50. Sedgley, M. and Griffin, A.R. (1989) Sexual Reproduction of Tree Crops. Academic Press, London.
51. Sessions, A., Burke, E., Presting, G., Aux, G., McElver, J., Patton, D., et al. (2002) A high-throughput Arabidopsis reverse genetics system. Plant Cell. 14: 2985-2994.
52. Seymour, G. and Manning, K. (2007) Developmental regulation of ripening in fleshy fruits. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 146: S244.
53. Soto-Zamora, G., Yahia, E.M., Brecht, J.K. and Gardea, A. (2005) Effects of postharvest hot air treatments on the quality and antioxidant levels in tomato fruit. LWT 38: 657-663.
54. Tadiello, A., Pavanello, A., Zanin, D., Caporali, E., Colombo, L., Rotino, G.L., et al. (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.
55. Takken, F.L.W., Schipper, D., Nijkamp, H.J.J. and Hille, J. (1998) Identifi cation and Ds-tagged isolation of a new gene at the Cf-4 locus of tomato involved in disease resistance to Cladosporium fulvum race 5. Plant J. 14: 401-411.
56. Tanksley, S.D. (2004) The genetic, developmental, and molecular bases of fruit size and shape variation in tomato. Plant Cell 16: S181-S189.
57. Taylor, J.E. and Whitelaw, C.A. (2001) Signals in abscission. New Phytol. 151: 323-339.
58. Van Camp, W. (2005) Yield enhancement genes: seeds for growth. Curr. Opin. Biotechnol. 16: 147-153.
59. Van der Biezen, E.A., Brandwagt, B.F., Van Leeuwen, W., Nijkamp, H.J.J. and Hille, J. (1996) Identification and isolation of the FEEBLY gene from tomato by transposon tagging. Mol. Gen. Genet. 251: 267-280.
60. Varoquaux, F., Blanvillain, R., Delseny, M. and Gallois, P. (2000) Less is better: new approaches for seedless fruit production. TIBTECH 1 8: 233-242.
61. Vogg, G., Fischer, S., Leide, J., Emmanuel, E., Jetter, R., Levy, A.A., et al. (2004) Tomato fruit cuticular waxes and their effects on transpiration barrier properties: functional characterization of a mutant defi cient in a very-long-chain fatty acid β-ketoacyl-CoA synthase. J. Exp. Bot. 55: 1401-1410.
62. Vrebalov, J., Ruezinsky, D., Padmanabhan, V., White, R., Medrano, D., Drake, R., et al. (2002) A MADS-box gene necessary for fruit ripening at the tomato ripening-inhibitor (Rin) locus. Science 296: 343-346.
63. Vriezen, W.H., Feron, R., Maretto, F., Keijman, J. and Mariani, C. (2008) Changes in tomato ovary transcriptome demonstrate complex hormonal regulation of fruit set. New Phytol. 177: 60-76.
64. Wang, H., Schauer, N., Usadel, B., Frasse, P., Zouine, M., Hernould, M., et al. (2009) Regulatory features underlying pollination-dependent and-independent tomato fruit set revealed by transcript and primary metabolite profi ling. Plant Cell 21: 1428-1452.
65. Xiao, H., Jiang, N., Schaffner, E., Stockinger, E.J. and van der Knaap, E. (2008) A retrotransposon-mediated gene duplication underlies morphological variation of tomato fruit. Science 319: 1527-1530.
66. Yen, H.C., Lee, S.Y., Tanksley, S.D., Lanahan, M.B., Klee, H.J. and Giovannoni, J. (1995) The tomato Never-ripe locus regulates ethylene-inducible gene expression and is linked to a homolog of the Arabidopsis ETR1 gene. Plant Physiol. 107: 1343-1353.
67. Zhang, S., Gu, Y.Q., Singh, J., Coleman-Derr, D., Brar, D.S., Jiang, N., et al. (2007) New insights into Oryza genome evolution: high gene colinearity and differential retrotransposon amplifi cation. Plant Mol. Biol. 64: 589-600.