TOMATO AGAMOUS-LIKE 1 is a component of the fruit ripening regulatory network

Plant Journal

Volumn 60, Issue 6, 2009, Pages 1081-1095

  Itkin, Maxim ^a   Seybold, Heike ^a,b   Breitel, Dario ^a   Rogachev, Ilana ^a   Meir, Sagit ^a   Aharoni, Asaph ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Ethylene; Fruit; Regulation; Ripening; Tomato; Transcriptome

Indexed keywords

CAROTENOID; ETHYLENE; ETHYLENE DERIVATIVE; LYCOPENE; MADS DOMAIN PROTEIN; PLANT RNA; VEGETABLE PROTEIN;

ARTICLE; BIOLOGY; BIOSYNTHESIS; DNA MICROARRAY; FRUIT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PIGMENTATION; TOMATO; TRANSGENIC PLANT;

CAROTENOIDS; COMPUTATIONAL BIOLOGY; ETHYLENES; FRUIT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENE SILENCING; LYCOPERSICON ESCULENTUM; MADS DOMAIN PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PIGMENTATION; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; RNA, PLANT;

LYCOPERSICON ESCULENTUM;

EID: 71649092407     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2009.04064.x     Document Type: Article

References (86)

1. Adams-Phillips, L., Barry, C. Giovannoni, J. (2004) Signal transduction systems regulating fruit ripening. Trends Plant Sci., 9, 331 338.
2. Alba, R., Payton, P., Fei, Z., McQuinn, R., Debbie, P., Martin, G.B., Tanksley, S.D. Giovannoni, J.J. (2005) Transcriptome and selected metabolite analyses reveal multiple points of ethylene control during tomato fruit development. Plant Cell, 17, 2954 2965.
3. Balanza, V., Navarrete, M., Trigueros, M. Ferrandiz, C. (2006) Patterning the female side of Arabidopsis: the importance of hormones. J. Exp. Bot., 57, 3457 3469.
4. Bargel, H. Neinhuis, C. (2004) Altered tomato (Lycopersicon esculentum Mill.) fruit cuticle biomechanics of a pleiotropic non ripening mutant. J. Plant Growth Regul. 23, 61 75.
5. Barry, C.S. Giovannoni, J.J. (2006) Ripening in the tomato Green-ripe mutant is inhibited by ectopic expression of a protein that disrupts ethylene signaling. Proc. Natl Acad. Sci. USA, 103, 7923 7928.
6. Barry, C.S., Llop-Tous, M.I. Grierson, D. (2000) The regulation of 1-aminocyclopropane-1-carboxylic acid synthase gene expression during the transition from system-1 to system-2 ethylene synthesis in tomato. Plant Physiol., 123, 979 986.
7. Bartley, G.E. Ishida, B.K. (2003) Developmental gene regulation during tomato fruit ripening and in-vitro sepal morphogenesis. BMC Plant Biol., 3, 4.
8. Bartley, G.E. Ishida, B.K. (2007) Ethylene-sensitive and insensitive regulation of transcription factor expression during in vitro tomato sepal ripening. J. Exp. Bot., 58, 2043 2051.
9. Bartley, G.E., Viitanen, P.V., Bacot, K.O. Scolnik, P.A. (1992) A tomato gene expressed during fruit ripening encodes an enzyme of the carotenoid biosynthesis pathway. J. Biol. Chem., 267, 5036 5039.
10. 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.
11. Becker, A., Kaufmann, K., Freialdenhoven, A., Vincent, C., Li, M.A., Saedler, H. Theissen, G. (2002) A novel MADS-box gene subfamily with a sister-group relationship to class B floral homeotic genes. Mol. Genet. Genomics, 266, 942 950.
12. Benjamini, Y. Hochberg, Y. (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B, 57, 289 300.
13. dg mutation of tomato: alterations in the fruit metabolome. New Phytol., 166, 427 438.
14. Bleecker, A.B. Kende, H. (2000) Ethylene: a gaseous signal molecule in plants. Annu. Rev. Cell Dev. Biol., 16, 1 18.
15. Bouzayen, M., Cooper, W., Barry, C., Zegzouti, H., Hamilton, A.J. Grierson, D. (1993) EFE multigene family in tomato plants: expression and characterization. In Cellular and Molecular Aspects of the Plant Hormone Ethylene (Pech, J.C., Latché, A. Balagué, C., eds). Dordrecht, The Netherlands: Kluwer Academic Publishers, pp. 76 81.
16. Busi, M.V., Bustamante, C., D'Angelo, C., Hidalgo-Cuevas, M., Boggio, S.B., Valle, E.M. Zabaleta, E. (2003) MADS-box genes expressed during tomato seed and fruit development. Plant Mol. Biol., 52, 801 815.
17. Carrari, F. Fernie, A.R. (2006) Metabolic regulation underlying tomato fruit development. J. Exp. Bot., 57, 1883 1897.
18. Carrington, C.M.S., Vendrell, M. Dominguez-Puigjaner, E. (2002) Characterisation of an endo-(1,4)-mannanase (LeMAN4) expressed in ripening tomato fruit. Plant Sci., 163, 599 606.
19. Chen, X., Riechmann, J.L., Jia, D. Meyerowitz, E. (2000) Minimal regions in the Arabidopsis PISTILLATA promoter responsive to the APETALA3PISTILLATA feedback control do not contain a CArG box. Sex. Plant Reprod., 13, 85 94.
20. Chen, G., Alexander, L. Grierson, D. (2004) Constitutive expression of EIL-like transcription factor partially restores ripening in the ethylene-insensitive Nr tomato mutant. J. Exp. Bot., 55, 1491 1497.
21. C-type MADS box genes in grapevine. Plant Physiol., 149, 354 369.
22. van Engelen, F.A., Molthoff, J.W., Conner, A.J., Nap, J.P., Pereira, A. Stiekema, W.J. (1995) pBINPLUS: an improved plant transformation vector based on pBIN19. Transgenic Res., 4, 288 290.
23. Exposito-Rodriguez, M., Borges, A.A., Borges-Perez, A. Perez, J.A. (2008) Selection of internal control genes for quantitative real-time RT-PCR studies during tomato development process. BMC Plant Biol., 8, 131.
24. Fallik, E., Polevaya, Y., Tuvia-Alkalai, S., Shalom, Y. Zuckermann, H. (2003) A 24 h anoxia treatment reduces decay development while maintaining tomato fruit quality. Postharvest Biol. Technol., 29, 233 236.
25. Fei, Z., Tang, X., Alba, R.M., White, J.A., Ronning, C.M., Martin, G.B., Tanksley, S.D. Giovannoni, J.J. (2004) Comprehensive EST analysis of tomato and comparative genomics of fruit ripening. Plant J., 40, 47 59.
26. Ferrandiz, C., Pelaz, S. Yanofsky, M.F. (1999) Control of carpel and fruit development in Arabidopsis. Annu. Rev. Biochem., 68, 321 354.
27. Ferrandiz, C., Liljegren, S.J. Yanofsky, M.F. (2000) Negative regulation of the SHATTERPROOF genes by FRUITFULL during Arabidopsis fruit development. Science, 289, 436 438.
28. de Folter, S. Angenent, G.C. (2006) trans meets cis in MADS science. Trends Plant Sci., 11, 224 231.
29. Fraser, P.D., Pinto, M.E., Holloway, D.E. Bramley, P.M. (2000) Application of high-performance liquid chromatography with photodiode array detection to the metabolic profiling of plant isoprenoids. Plant J., 24, 551 558.
30. Giovannoni, J., Tanksley, S., Vrebalov, J. Noensie, E. (2004) NOR gene compositions and methods for use thereof. US Patent Number 6 762 347, issued 13 July 2004.
31. Gomez-Mena, C., de Folter, S., Costa, M.M., Angenent, G.C. Sablowski, R. (2005) Transcriptional program controlled by the floral homeotic gene AGAMOUS during early organogenesis. Development, 132, 429 438.
32. Hamilton, A.J., Lycett, G.W. Grierson, D. (1990) Antisense gene that inhibits synthesis of the hormone ethylene in transgenic plants. Nature, 346, 284 287.
33. He, C. Saedler, H. (2005) Heterotopic expression of MPF2 is the key to the evolution of the Chinese lantern of Physalis, a morphological novelty in Solanaceae. Proc. Natl Acad. Sci. USA, 102, 5779 5784.
34. Hellens, R.P., Allan, A.C., Friel, E.N., Bolitho, K., Grafton, K., Templeton, M.D., Karunairetnam, S., Gleave, A.P. Laing, W.A. (2005) Transient expression vectors for functional genomics, quantification of promoter activity and RNA silencing in plants. Plant Methods, 1, 13.
35. Herner, R. Sink, K. (1973) Ethylene production and respiratory behavior of the rin tomato mutant. Plant Physiol., 52, 38 42.
36. Hileman, L.C., Sundstrom, J.F., Litt, A., Chen, M., Shumba, T. Irish, V.F. (2006) Molecular and phylogenetic analyses of the MADS-box gene family in tomato. Mol. Biol. Evol., 23, 2245 2258.
37. Hiratsu, K., Matsui, K., Koyama, T. Ohme-Takagi, M. (2003) Dominant repression of target genes by chimeric repressors that include the EAR motif, a repression domain, in Arabidopsis. Plant J., 34, 733 739.
38. Irizarry, R.A., Bolstad, B.M., Collin, F., Cope, L.M., Hobbs, B. Speed, T.P. (2003) Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res., 31, e15.
39. Ishida, B.K., Jenkins, S.M. 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.
40. Ito, Y., Kitagawa, M., Ihashi, N., Yabe, K., Kimbara, J., Yasuda, J., Ito, H., Inakuma, T., Hiroi, S. Kasumi, T. (2008) DNA-binding specificity, transcriptional activation potential, and the rin mutation effect for the tomato fruit-ripening regulator RIN. Plant J., 55, 212 223.
41. Jack, T., Fox, G.L. Meyerowitz, E.M. (1994) Arabidopsis homeotic gene APETALA3 ectopic expression: transcriptional and posttranscriptional regulation determine floral organ identity. Cell, 76, 703 716.
42. Kerr, E. (1981) Linkage studies of green ripe and never ripe. Rep. Tomato Genet. Coop. Rep., 31, 7.
43. Kerr, E. (1982) Never ripe-2 (Nr-2), a slow ripening mutant resembling Nr and Gr. Rep. Tomato Genet. Coop., 32, 33.
44. Lanahan, M.B., Yen, H.C., Giovannoni, J.J. Klee, H.J. (1994) The never ripe mutation blocks ethylene perception in tomato. Plant Cell, 6, 521 530.
45. Leide, J., Hildebrandt, U., Reussing, K., Riederer, M. Vogg, G. (2007) The developmental pattern of tomato fruit wax accumulation and its impact on cuticular transpiration barrier properties: effects of a deficiency in a-ketoacyl-coenzyme A synthase (LeCER6). Plant Physiol., 144, 1667 1679.
46. Leseberg, C.H., Eissler, C.L., Wang, X., Johns, M.A., Duvall, M.R. Mao, L. (2008) Interaction study of MADS-domain proteins in tomato. J. Exp. Bot., 59, 2253 2265.
47. Li, Y., Zhu, B., Xu, W., Zhu, H., Chen, A., Xie, Y., Shao, Y. Luo, Y. (2007) LeERF1 positively modulated ethylene triple response on etiolated seedling, plant development and fruit ripening and softening in tomato. Plant Cell Rep., 26, 1999 2008.
48. Liljegren, S.J., Ditta, G.S., Eshed, Y., Savidge, B., Bowman, J.L. Yanofsky, M.F. (2000) SHATTERPROOF MADS-box genes control seed dispersal in Arabidopsis. Nature, 404, 766 770.
49. Lin, Z., Hong, Y., Yin, M., Li, C., Zhang, K. Grierson, D. (2008) A tomato HD-Zip homeobox protein, LeHB-1, plays an important role in floral organogenesis and ripening. Plant J., 55, 301 310.
50. Lincoln, J.E., Campbell, A.D., Oetiker, J., Rottmann, W.H., Oeller, P.W., Shen, N.F. Theologis, A. (1993) Le-ACS4, a fruit ripening and wound-induced 1-aminocyclopropane-1-carboxylate synthase gene of tomato (Lycopersicon esculentum). Expression in Escherichia coli, structural characterization, expression characteristics, and phylogenetic analysis. J. Biol. Chem., 268, 19422 19430.
51. Liu, Y., Schiff, M. Dinesh-Kumar, S.P. (2002) Virus-induced gene silencing in tomato. Plant J., 31, 777 786.
52. Manning, K., Tor, M., Poole, M., Hong, Y., Thompson, A.J., King, G.J., Giovannoni, J.J. Seymour, G.B. (2006) A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nat. Genet., 38, 948 952.
53. Mao, L., Begum, D., Chuang, H.W., Budiman, M.A., Szymkowiak, E.J., Irish, E.E. Wing, R.A. (2000) JOINTLESS is a MADS-box gene controlling tomato flower abscission zone development. Nature, 406, 910 913.
54. Marin-Rodriguez, M.C., Orchard, J. Seymour, G.B. (2002) Pectate lyases, cell wall degradation and fruit softening. J. Exp. Bot., 53, 2115 2119.
55. Marsh, J.T., Sullivan, S., Hartwell, J. Nimmo, H.G. (2003) Structure and expression of phosphoenolpyruvate carboxylase kinase genes in Solanaceae. A novel gene exhibits alternative splicing. Plant Physiol., 133, 2021 2028.
56. Matsui, K., Tanaka, H. Ohme-Takagi, M. (2004) Suppression of the biosynthesis of proanthocyanidin in Arabidopsis by a chimeric PAP1 repressor. Plant Biotechnol. J., 2, 487 493.
57. McMurchie, E.J., McGlasson, W.B. Eaks, I.L. (1972) Treatment of fruit with propylene gives information about the biogenesis of ethylene. Nature, 237, 235 236.
58. Meissner, R., Jacobson, Y., Melmed, S., Levyatuv, S., Shalev, G., Ashri, A., Elkind, Y. Levy, A. (1997) A new model system for tomato genetics. Plant J., 12, 1465 1472.
59. Meissner, R., Chague, V., Zhu, Q., Emmanuel, E., Elkind, Y. Levy, A.A. (2000) A high throughput system for transposon tagging and promoter trapping in tomato. Plant J., 22, 265 274.
60. Mintz-Oron, S., Mandel, T., Rogachev, I. et al. (2008) Gene expression and metabolism in tomato fruit surface tissues. Plant Physiol., 147, 823 851.
61. Nakatsuka, A., Murachi, S., Okunishi, H., Shiomi, S., Nakano, R., Kubo, Y. Inaba, A. (1998) Differential expression and internal feedback regulation of 1-aminocyclopropane-1-carboxylate synthase, 1-aminocyclopropane-1-carboxylate oxidase, and ethylene receptor genes in tomato fruit during development and ripening. Plant Physiol., 118, 1295 1305.
62. Olson, D.C., White, J.A., Edelman, L., Harkins, R.N. Kende, H. (1991) Differential expression of two genes for 1-aminocyclopropane-1-carboxylate synthase in tomato fruits. Proc. Natl Acad. Sci. USA, 88, 5340 5344.
63. Picton, S., Gray, J.E., Payton, S., Barton, S.L., Lowe, A. Grierson, D. (1993) A histidine decarboxylase-like mRNA is involved in tomato fruit ripening. Plant Mol. Biol., 23, 627 631.
64. Pnueli, L., Hareven, D., Rounsley, S.D., Yanofsky, M.F. Lifschitz, E. (1994) Isolation of the tomato AGAMOUS gene TAG1 and analysis of its homeotic role in transgenic plants. Plant Cell, 6, 163 173.
65. Ruuska, S.A. Ohlrogge, J.B. (2001) Protocol for small-scale RNA isolation and transcriptional profiling of developing Arabidopsis seeds. BioTechniques, 31, 752 758.
66. Saladie, M., Matas, A.J., Isaacson, T. et al. (2007) A reevaluation of the key factors that influence tomato fruit softening and integrity. Plant Physiol., 144, 1012 1028.
67. 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.
68. Schwarz-Sommer, Z., Hue, I., Huijser, P., Flor, P.J., Hansen, R., Tetens, F., Lonnig, W.E., Saedler, H. Sommer, H. (1992) Characterization of the Antirrhinum floral homeotic MADS-box gene deficiens: evidence for DNA binding and autoregulation of its persistent expression throughout flower development. EMBO J., 11, 251 263.
69. Seymour, G., Poole, M., Manning, K. King, G.J. (2008) Genetics and epigenetics of fruit development and ripening. Curr. Opin. Plant Biol., 11, 58 63.
70. Slater, A., Maunders, M.J., Edwards, K., Schuch, W. Grierson, D. (1985) Isolation and characterization of cDNA clones for tomato polygalacturonase and other ripening-related proteins. Plant Mol. Biol., 5, 137 147.
71. Smith, D.L. Gross, K.C. (2000) A family of at least seven-galactosidase genes is expressed during tomato fruit development. Plant Physiol., 123, 1173 1183.
72. Smith, D.L., Starrett, D.A. Gross, K.C. (1998) A gene coding for tomato fruit-galactosidase II is expressed during fruit ripening. Cloning, characterization, and expression pattern. Plant Physiol., 117, 417 423.
73. Srivastava, A. Handa, A.K. (2005) Hormonal regulation of fruit development: a molecular perspective. J. Plant Growth Regul., 24, 67 82.
74. Tadiello, A., Pavanello, A., Zanin, D., Caporali, E., Colombo, L., Rotino, G.L., 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.
75. Takase, T., Yasuhara, M., Geekiyanage, S., Ogura, Y. Kiyosue, T. (2007) Overexpression of the chimeric gene of the floral regulator CONSTANS and the EAR motif repressor causes late flowering in Arabidopsis. Plant Cell Rep., 26, 815 821.
76. Tani, E., Polidoros, A.N. Tsaftaris, A.S. (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.
77. Thompson, A.J., Tor, M., Barry, C.S., Vrebalov, J., Orfila, C., Jarvis, M.C., Giovannoni, J.J., Grierson, D. Seymour, G.B. (1999) Molecular and genetic characterization of a novel pleiotropic tomato-ripening mutant. Plant Physiol., 120, 383 390.
78. Tigchelaar, E.C., McGlasson, W.B. Buescher, R.W. (1978) Genetic regulation of tomato fruit ripening. Hortic. Sci., 13, 508 513.
79. Trobner, W., Ramirez, L., Motte, P., Hue, I., Huijser, P., Lonnig, W.E., Saedler, H., Sommer, H. Schwarz-Sommer, Z. (1992) GLOBOSA: a homeotic gene which interacts with DEFICIENS in the control of Antirrhinum floral organogenesis. EMBO J., 11, 4693 4704.
80. Verwoerd, T.C., Dekker, B.M. Hoekema, A. (1989) A small-scale procedure for the rapid isolation of plant RNAs. Nucleic Acids Res., 17, 2362.
81. Voinnet, O., Rivas, S., Mestre, P. Baulcombe, D. (2003) An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J., 33, 949 956.
82. 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.
83. Wilkinson, J.Q., Lanahan, M.B., Yen, H.C., Giovannoni, J.J. Klee, H.J. (1995) An ethylene-inducible component of signal transduction encoded by never-ripe. Science, 270, 1807 1809.
84. Yang, S.F. Hoffman, N.E. (1984) Ethylene biosynthesis and its regulation in higher plants. Annu. Rev. Plant Physiol., 35, 155 189.
85. Yokotani, N., Nakano, R., Imanishi, S., Nagata, M., Inaba, A. Kubo, Y. (2009) Ripening-associated ethylene biosynthesis in tomato fruit is autocatalytically and developmentally regulated. J. Exp. Bot., 60, 3433 3442.
86. Zarembinski, T.I. Theologis, A. (1994) Ethylene biosynthesis and action: a case of conservation. Plant Mol. Biol., 26, 1579 1597.