Fruit-surface flavonoid accumulation in tomato is controlled by a SLMYB12-regulated transcriptional network

PLoS Genetics

Volumn 5, Issue 12, 2009, Pages

  Adato, Avital ^a   Mandel, Tali ^a   Mintz Oron, Shira ^a   Venger, Ilya ^a   Levy, Dorit ^a   Yativ, Merav ^a   Domínguez, Eva ^b   Wang, Zhonghua ^c   De Vos, Ric C H ^d   Jetter, Reinhard ^c   Schreiber, Lukas ^e   Heredia, Antonio ^b   Rogachev, Ilana ^a   Aharoni, Asaph ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b UNIVERSITY OF MÁLAGA   (Spain)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^d CENTRE FOR BIOSYSTEMS GENOMICS   (Netherlands)

^e UNIVERSITY OF BONN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

FLAVANOID; FLAVONOID;

ARTICLE; CHROMOSOME 1; FRUIT DEVELOPMENT; GENE CONTROL; GENE EXPRESSION; GENE IDENTIFICATION; GENE MAPPING; GENE MUTATION; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; NONHUMAN; PHENOTYPE; PLANT GENE; REGULATOR GENE; SIMYB12 GENE; TOMATO; FRUIT; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; MUTATION; PLANT CHROMOSOME;

LYCOPERSICON ESCULENTUM;

CHROMOSOMES, PLANT; FLAVONOIDS; FRUIT; GENE EXPRESSION REGULATION, PLANT; GENE REGULATORY NETWORKS; GENES, PLANT; LYCOPERSICON ESCULENTUM; MUTATION;

EID: 74249116441     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1000777     Document Type: Article

References (58)

1. Samuels L, Jetter R, Kunst L (2005) First steps in understanding the export of lipids to the plant cuticle. Plant Biosystems 139: 65-68.
2. Muir SR, Collins GJ, Robinson S, Hughes S, Bovy A, et al. (2001) Overexpression of petunia chalcone isomerase in tomato results in fruit containing increased levels of flavonols. Nature Biotechnology 19: 470-474.
3. Luque P, Bruque S, Heredia A (1995) Water permeability of isolated cuticular membranes: a structural analysis. Arch Biochem Biophys 317: 417-422.
4. Bovy A, de Vos R, Kemper M, Schijlen E, Almenar Pertejo M, et al. (2002) High-flavonol tomatoes resulting from the heterologous expression of the maize transcription factor genes LC and C1. Plant Cell 14: 2509-2526.
5. Willits MG, Kramer CM, Prata RT, De Luca V, Potter BG, et al. (2005) Utilization of the genetic resources of wild species to create a nontransgenic high flavonoid tomato. J Agric Food Chem 53: 1231-1236.
6. Verhoeyen ME, Bovy A, Collins G, Muir S, Robinson S, et al. (2002) Increasing antioxidant levels in tomatoes through modification of the flavonoid biosynthetic pathway. J Exp Bot 53: 2099-2106.
7. Schijlen E, de Vos CHR, Martens S, Jonker HH, Rosin FM, et al. (2007) RNA interference silencing of Chalcone synthase, the first step in the flavonoid biosynthesis pathway, leads to parthenocarpic tomato fruits. Plant Physiology 144: 1520-1530.
8. Iijima Y, Nakamura Y, Ogata Y, Tanaka K, Sakurai N, et al. (2008) Metabolite annotations based on the integration of mass spectral information. Plant J 54: 949-962.
9. Mintz-Oron S, Mandel T, Rogachev I, Feldberg L, Lotan O, et al. (2008) Gene expression and metabolism in tomato fruit surface tissues. Plant Physiology 147: 823-851.
10. Moco S, Bino RJ, Vorst O, Verhoeven HA, de Groot J, et al. (2006) A liquid chromatography-mass spectrometry-based metabolome database for tomato. Plant Physiology 141: 1205-1218.
11. Moco S, Capanoglu E, Tikunov Y, Bino RJ, Boyacioglu D, et al. (2007) Tissue specialization at the metabolite level is perceived during the development of tomato fruit. Journal of Experimental Botany 58: 4131-4146.
12. Slimestad R, Fossen T, Verheul MJ (2008) The flavonoids of tomatoes. Journal of Agricultural and Food Chemistry 56: 2436-2441.
13. Koes R, Verweij W, Quattrocchio F (2005) Flavonoids: a colorful model for the regulation and evolution of biochemical pathways. Trends Plant Sci 10: 236-242.
14. Ramsay NA, Glover BJ (2005) MYB-bHLH-WD40 protein complex and the evolution of cellular diversity. Trends Plant Sci 10: 63-70.
15. Lepiniec L, Debeaujon I, Routaboul JM, Baudry A, Pourcel L, et al. (2006) Genetics and biochemistry of seed flavonoids. Annu Rev Plant Biol 57: 405-430.
16. Dooner HK, Robbins TP, Jorgensen RA (1991) Genetic and developmental control of anthocyanin biosynthesis. Annu Rev Genet 25: 173-199.
17. Galis I, Simek P, Narisawa T, Sasaki M, Horiguchi T, et al. (2006) A novel R2R3 MYB transcription factor NtMYBJS1 is a methyl jasmonate-dependent regulator of phenylpropanoid-conjugate biosynthesis in tobacco. Plant J 46: 573-592.
18. Mehrtens F, Kranz H, Bednarek P, Weisshaar B (2005) The Arabidopsis transcription factor MYB12 is a flavonol-specific regulator of phenylpropanoid biosynthesis. Plant Physiology 138: 1083-1096.
19. Deluc L, Barrieu F, Marchive C, Lauvergeat V, Decendit A, et al. (2006) Characterization of a grapevine R2R3-MYB transcription factor that regulates the phenylpropanoid pathway. Plant Physiol 140: 499-511.
20. Stracke R, Ishihara H, Huep G, Barsch A, Mehrtens F, et al. (2007) Differential regulation of closely related R2R3-MYB transcription factors controls flavonol accumulation in different parts of the Arabidopsis thaliana seedling. Plant J 50: 660-677.
21. Bogs J, Jaffe FW, Takos AM, Walker AR, Robinson SP (2007) The grapevine transcription factor VvMYBPA1 regulates proanthocyanidin synthesis during fruit development. Plant Physiol 143: 1347-1361.
22. Borevitz JO, Xia Y, Blount J, Dixon RA, Lamb C (2000) Activation tagging identifies a conserved MYB regulator of phenylpropanoid biosynthesis. Plant Cell 12: 2383-2394.
23. Luo J, Butelli E, Hill L, Parr A, Niggeweg R, et al. (2008) AtMYB12 regulates caffeoyl quinic acid and flavonol synthesis in tomato: expression in fruit results in very high levels of both types of polyphenol. Plant J 56: 316-326.
24. Butelli E, Titta L, Giorgio M, Mock HP, Matros A, et al. (2008) Enrichment of tomato fruit with health-promoting anthocyanins by expression of select transcription factors. Nat Biotechnol 26: 1301-1308.
25. Quattrocchio F, Wing J, van der Woude K, Souer E, de Vetten N, et al. (1999) Molecular analysis of the anthocyanin2 gene of petunia and its role in the evolution of flower color. Plant Cell 11: 1433-1444.
26. Lin Q, Hamilton WD, Merryweather A (1996) Cloning and initial characterization of 14 myb-related cDNAs from tomato (Lycopersicon esculentum cv. Ailsa Craig). Plant Mol Biol 30: 1009-1020.
27. Lindstrom E (1925) Inheritance in tomatoes.
28. Rick C, Butler L (1956) Cytogenetics of the tomato. Advance Genetics 8: 267-382.
29. Duggar B, ed (1913) Lycopersicin, the red pigment of the tomato, and the effects of conditions upon its development: Washington Univ. Studies. pp 22-45.
30. Sapir M, Oren-Shamir M, Ovadia R, Reuveni M, Evenor D, et al. (2008) Molecular aspects of Anthocyanin fruit tomato in Relation to high pigment-I. Journal of Heredity 99: 292-303.
31. Fulton TM, Grandillo S, Beck-Bunn T, Fridman E, Frampton A, et al. (2000) Advanced backcross QTL analysis of a Lycopersicon esculentum x Lycopersicon parviflorum cross. Theoretical and Applied Genetics 100: 1025-1042.
32. Kutchan TM (2005) A role for intra- and intercellular translocation in natural product biosynthesis. Curr Opin Plant Biol 8: 292-300.
33. Saladie M, Matas AJ, Isaacson T, Jenks MA, Goodwin SM, et al. (2007) A reevaluation of the key factors that influence tomato fruit softening and integrity. Plant Physiology 144: 1012-1028.
34. Benitez JJ, Matas AJ, Heredia A (2004) Molecular characterization of the plant biopolyester cutin by AFM and spectroscopic techniques. J Struct Biol 147: 179-184.
35. 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 betaketoacyl-coenzyme A synthase (LeCER6). Plant Physiol 144: 1667-1679.
36. Fraser PD, Enfissi EM, Halket JM, Truesdale MR, Yu D, et al. (2007) Manipulation of phytoene levels in tomato fruit: effects on isoprenoids, plastids, and intermediary metabolism. Plant Cell 19: 3194-3211.
37. Giliberto L, Perrotta G, Pallara P, Weller JL, Fraser PD, et al. (2005) Manipulation of the blue light photoreceptor cryptochrome 2 in tomato affects vegetative development, flowering time, and fruit antioxidant content. Plant Physiol 137: 199-208.
38. Yen HC, Shelton BA, Howard LR, Lee S, Vrebalov J, et al. (1997) The tomato high-pigment (hp) locus maps to chromosome 2 and influences plastome copy number and fruit quality. Theoretical and Applied Genetics 95: 1069-1079.
39. Bino RJ, Ric de Vos CH, Lieberman M, Hall RD, Bovy A, et al. (2005) The light-hyperresponsive high pigment-2dg mutation of tomato: alterations in the fruit metabolome. New Phytol 166: 427-438.
40. Davuluri GR, van Tuinen A, Fraser PD, Manfredonia A, Newman R, et al. (2005) Fruit-specific RNAi-mediated suppression of DET1 enhances carotenoid and flavonoid content in tomatoes. Nat Biotechnol 23: 890-895.
41. Mahjoub A, Hernould M, Joubes J, Decendit A, Mars M, et al. (2009) Overexpression of a grapevine R2R3-MYB factor in tomato affects vegetative development, flower morphology and flavonoid and terpenoid metabolism. Plant Physiology and Biochemistry 47: 551-561.
42. Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58: 221-227.
43. Galpaz N, Wang Q, Menda N, Zamir D, Hirschberg J (2008) Abscisic acid deficiency in the tomato mutant high-pigment 3 leading to increased plastid number and higher fruit lycopene content. Plant J 53: 717-730.
44. Taylor IB, Burbidge A, Thompson AJ (2000) Control of abscisic acid synthesis. J Exp Bot 51: 1563-1574.
45. Zhao J, Zhang W, Zhao Y, Gong X, Guo L, et al. (2007) SAD2, an importin -like protein, is required for UV-B response in Arabidopsis by mediating MYB4 nuclear trafficking. Plant Cell 19: 3805-3818.
46. Malitsky S, Blum E, Less H, Venger I, Elbaz M, et al. (2008) The Transcript and Metabolite Networks Affected by the Two Clades of Arabidopsis Glucosinolate Biosynthesis Regulators. Plant Physiology 148: 2021-2049.
47. Zerback R, Dressler K, Hess D (1989) Flavonoid compounds from pollen and stigma of petunia hybrida - inducers of the vir region of the agrobacteriumtumefaciens ti plasmid. Plant Science 62: 83-91.
48. Sheahan JJ, Rechnitz GA (1992) Flavonoid-specific staining of Arabidopsis thaliana. Biotechniques 13: 880-883.
49. Vanengelen FA, Molthoff JW, Conner AJ, Nap JP, Pereira A, et al. (1995) Pbinplus - an improved plant transformation vector based on pbin19. Transgenic Research 4: 288-290.
50. Dan Y, Yan H, Munyikwa T, Dong J, Zhang Y, et al. (2006) MicroTom-a highthroughput model transformation system for functional genomics. Plant Cell Rep 25: 432-441.
51. Verwoerd TC, Dekker BM, Hoekema A (1989) A small-scale procedure for the rapid isolation of plant RNAs. Nucleic Acids Res 17: 2362.
52. Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, et al. (2003) Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res 31: e15.
53. Smith CA, Want EJ, O'Maille G, Abagyan R, Siuzdak G (2006) XCMS: processing mass spectrometry data for metabolite profiling using nonlinear peak alignment, matching, and identification. Anal Chem 78: 779-787.
54. Saeed AI, Sharov V, White J, Li J, Liang W, et al. (2003) TM4: A free, opensource system for microarray data management and analysis. Biotechniques 34: 374-+.
55. Fraser PD, Pinto ME, Holloway DE, Bramley PM (2000) Technical advance: application of high-performance liquid chromatography with photodiode array detection to the metabolic profiling of plant isoprenoids. Plant J 24: 551-558.
56. Hovav R, Chehanovsky N, Moy M, Jetter R, Schaffer AA (2007) The identification of a gene (Cwp1), silenced during Solanum evolution, which causes cuticle microfissuring and dehydration when expressed in tomato fruit. Plant J 52: 627-639.
57. Matas AJ, Lopez-Casado G, Cuartero J, Heredia A (2005) Relative humidity and temperature modify the mechanical properties of isolated tomato fruit cuticles. American Journal of Botany 92: 462-468.
58. Eshed Y, Zamir D (1995) An introgression line population of Lycopersicon pennellii in the cultivated tomato enables the identification and fine mapping of yield-associated QTL. Genetics 141: 1147-1162.