Retrotransposons control fruit-specific, cold-dependent accumulation of anthocyanins in blood oranges

Plant Cell

Volumn 24, Issue 3, 2012, Pages 1242-1255

  Butelli, Eugenio ^a   Licciardello, Concetta ^b   Zhang, Yang ^a   Liu, Jianjun ^c   Mackay, Steve ^a   Bailey, Paul ^a   Reforgiato Recupero, Giuseppe ^b   Martin, Cathie ^a  

^a JOHN INNES CENTRE   (United Kingdom)

^b ISTITUTO NAZIONALE DELLA NUTRIZIONE   (Italy)

^c CROP RESEARCH INSTITUTE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84860200867     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.111.095232     Document Type: Article

References (62)

1. Ancillo, G., Gadea, J., Forment, J., Guerri, J., and Navarro, L. (2007). Class prediction of closely related plant varieties using gene expression profiling. J. Exp. Bot. 58: 1927-1933.
2. Bailey, P.C., Dicks, J., Wang, T.L., and Martin, C. (2008). IT3F: A webbased tool for functional analysis of transcription factors in plants. Phytochemistry 69: 2417-2425.
3. Barrett, H.C., and Rhodes, A.M. (1976). A numerical taxonomic study of affinity relationships in cultivated Citrus and its close relatives. Syst. Bot. 1: 105-136.
4. Bernardi, J., Licciardello, C., Russo, M.P., Luisa Chiusano, M., Carletti, G., Recupero, G.R., and Marocco, A. (2010). Use of a custom array to study differentially expressed genes during blood orange (Citrus sinensis L. Osbeck) ripening. J. Plant Physiol. 167: 301-310.
5. Bonina, F.P., Leotta, C., Scalia, G., Puglia, C., Trombetta, D., Tringali, G., Roccazzello, A.M., Rapisarda, P., and Saija, A. (2002). Evaluation of oxidative stress in diabetic patients after supplementation with a standardised red orange extract. Diabetes Nutr. Metab. 15: 14-19.
6. Butelli, E., Titta, L., Giorgio, M., Mock, H.P., Matros, A., Peterek, S., Schijlen, E.G.W.M., Hall, R.D., Bovy, A.G., Luo, J., and Martin, C. (2008). Enrichment of tomato fruit with health-promoting anthocyanins by expression of select transcription factors. Nat. Biotechnol. 26: 1301-1308.
7. Chapot, H. (1963). Quelques oranges sanguines. Cah. Rech. Agron. (Rabat) 18: 61-87.
8. Cultrone, A., Controneo, P.S., and Reforgiato-Recupero, G. (2010). Cloning and molecular characterisation of R2R3-MYB and bHLHMYC transcription factors from Citrus sinensis. Tree Genet. Genomes 6: 101-112.
9. Crifó, T., Puglisi, I., Petrone, G., Recupero, G.R., and Lo Piero, A.R. (2011). Expression analysis in response to low temperature stress in blood oranges: implication of the flavonoid biosynthetic pathway. Gene 476: 1-9.
10. De Felice, B., Wilson, R.R., Argenziano, C., Kafantaris, I., and Conicella, C. (2009). A transcriptionally active copia-like retroelement in Citrus limon. Cell. Mol. Biol. Lett. 14: 289-304.
11. de Pascual-Teresa, S., Moreno, D.A., and García-Viguera, C. (2010). Flavanols and anthocyanins in cardiovascular health: A review of current evidence. Int. J. Mol. Sci. 11: 1679-1703.
12. Davies, K.M. (2007). Genetic modification of plant metabolism for human health benefits. Mutat. Res. 622: 122-137.
13. Espley, R.V., Hellens, R.P., Putterill, J., Stevenson, D.E., Kutty- Amma, S., and Allan, A.C. (2007). Red colouration in apple fruit is due to the activity of the MYB transcription factor, MdMYB10. Plant J. 49: 414-427.
14. Felsenstein, J. (2004). PHYLIP (Phylogeny Inference Package) Version 3.6. (Seattle, WA: University of Washington).
15. Ferrari, G.B. (1646). Hesperides Sive Malorum Aureorum Cultura et Usu. (Romae, sumptibus Hermanni Scheus).
16. Feschotte, C., Jiang, N., and Wessler, S.R. (2002). Plant transposable elements: where genetics meets genomics. Nat. Rev. Genet. 3: 329-341.
17. Fournier-Level, A., Lacombe, T., Le Cunff, L., Boursiquot, J.M., and This, P. (2010). Evolution of the VvMybA gene family, the major determinant of berry colour in cultivated grapevine (Vitis vinifera L.). Heredity (Edinb) 104: 351-362.
18. Geekiyanage, S., Takase, T., Ogura, Y., and Kiyosue, T. (2007). Anthocyanin production by over-expression of grape transcription factor gene VlmybA2 in transgenic tobacco and Arabidopsis. Plant Biotech. Rep. 1: 11-18.
19. Guarnieri, S., Riso, P., and Porrini, M. (2007). Orange juice vs vitamin C: Effect on hydrogen peroxide-induced DNA damage in mononuclear blood cells. Br. J. Nutr. 97: 639-643.
20. Heim, M.A., Jakoby, M., Werber, M., Martin, C., Weisshaar, B., and Bailey, P.C. (2003). The basic helix-loop-helix transcription factor family in plants: A genome-wide study of protein structure and functional diversity. Mol. Biol. Evol. 20: 735-747.
21. Hodgson, R.W. (1967). History, world distribution, botany and varieties. In The Citrus Industry, Vol. I, W. Reuther, H.J. Webber, and L.D. Batchelor, eds (Berkeley, CA: University of California), pp. 431-591.
22. Holmes, E.M. (1924). The origin of the Maltese blood orange. Pharm. J. Citrus 614-615.
23. Jayaprakasha, G.K., and Patl, B.S. (2007). In vitro evaluation of the antioxidant activities in fruit extracts from citron and blood orange. Food Chem. 101: 410-418.
24. Jefferson, R.A. (1987). Assaying chimeric genes in plants: The GUS gene fusion system. Plant Mol. Biol. Rep. 5: 387-405.
25. Kelebek, H., Canbas, A., and Selli, S. (2008). Determination of phenolic composition and antioxidant capacity of blood orange juices obtained from cvs Moro and Sanguinelli (Citrus sinensis (L) Osbeck) grown in Turkey. Food Chem. 107: 1710-1716.
26. Kim, J.M., Vanguri, S., Boeke, J.D., Gabriel, A., and Voytas, D.F. (1998). Transposable elements and genome organization: A comprehensive survey of retrotransposons revealed by the complete Saccharomyces cerevisiae genome sequence. Genome Res. 8: 464-478.
27. Kobayashi, S., Goto-Yamamoto, N., and Hirochika, H. (2004). Retrotransposon- induced mutations in grape skin color. Science 304: 982.
28. Latado, R.R., Tognato, P.C., Silva-Stenico, M.E., do Nascimento, L.M., and dos Santos, P.C. (2008). Anthocyanin accumulation and physical and chemical characteristics of blood orange fruits during cold storage. Rev. Bras. Frutic. 30: 604-610.
29. Li, X., Xie, R., Lu, Z., and Zhou, Z. (2010). The origin of cultivated Citrus as inferred from internal transcribed spacer and chloroplast DNA sequence and amplified fragment length polymorphism fingerprints. J. Am. Soc. Hortic. Sci. 135: 341-350.
30. Licciardello, C., Russo, M.P., Vale', G., and Recupero-Reforiato, G. (2008). Identification of differentially expressed genes in the flesh of blood and common oranges. Tree Genet. Genomes 4: 315-331.
31. Lin-Wang, K., Bolitho, K., Grafton, K., Kortstee, A., Karunairetnam, S., McGhie, T.K., Espley, R.V., Hellens, R.P., and Allan, A.C. (2010). An R2R3 MYB transcription factor associated with regulation of the anthocyanin biosynthetic pathway in Rosaceae. BMCPlant Biol. 10: 50.
32. Löytynoja, A., and Goldman, N. (2008). Phylogeny-aware gap placement prevents errors in sequence alignment and evolutionary analysis. Science 320: 1632-1635.
33. Mabberley, D.J. (1997). A classification of edible Citrus (Rutaceae). Telopea (Syd.) 7: 167-172.
34. McClintock, B. (1984). The significance of responses of the genome to challenge. Science 226: 792-801.
35. Moore, G.A. (2001). Oranges and lemons: Clues to the taxonomy of Citrus from molecular markers. Trends Genet. 17: 536-540.
36. Negrutiu, I., Shillito, R., Potrykus, I., Biasini, G., and Sala, F. (1987). Hybrid genes in the analysis of transformation conditions. I. Setting up a simple method for direct gene transfer into plant protoplasts. Plant Mol. Biol. 8: 363-373.
37. Nicolosi, E., Deng, Z.N., Gentile, A., La Malfa, S., Continella, G., and Tribulato, E. (2000). Citrus phylogeny and genetic origin of important species as investigated by molecular markers. Theor. Appl. Genet. 100: 1155-1166.
38. Paredes-López, O., Cervantes-Ceja, M.L., Vigna-Pérez, M., and Hernández-Pérez, T. (2010). Berries: Improving human health and healthy aging, and promoting quality life-a review. Plant Foods Hum. Nutr. 65: 299-308.
39. Parisod, C., Alix, K., Just, J., Petit, M., Sarilar, V., Mhiri, C., Ainouche, M., Chalhoub, B., and Grandbastien, M.A. (2010). Impact of transposable elements on the organization and function of allopolyploid genomes. New Phytol. 186: 37-45.
40. Pelsy, F. (2010). Molecular and cellular mechanisms of diversity within grapevine varieties. Heredity (Edinb.) 104: 331-340.
41. Prior, R.L., and Wu, X.L. (2006). Anthocyanins: Structural characteristics that result in unique metabolic patterns and biological activities. Free Radic. Res. 40: 1014-1028.
42. Proteggente, A.R., Saija, A., De Pasquale, A., and Rice-Evans, C.A. (2003). The compositional characterisation and antioxidant activity of fresh juices from sicilian sweet orange (Citrus sinensis L. Osbeck) varieties. Free Radic. Res. 37: 681-687.
43. Ramsay, N.A., and Glover, B.J. (2005). MYB-bHLH-WD40 protein complex and the evolution of cellular diversity. Trends Plant Sci. 10: 63-70.
44. Rapisarda, P., Fabroni, S., Peterek, S., Russo, G., and Mock, H.P. (2009). Juice of new citrus hybrids (Citrus clementina Hort. ex Tan. X C.sinensis L. Osbeck) as a source of natural antioxidants. Food Chem. 117: 212-218.
45. Rapisarda, P., Tomaino, A., Lo Cascio, R., Bonina, F., De Pasquale, A., and Saija, A. (1999). Antioxidant effectiveness as influenced by phenolic content of fresh orange juices. J. Agric. Food Chem. 47: 4718-4723.
46. Rico-Cabanas, L., and Martínez-Izquierdo, J.A. (2007). CIRE1, a novel transcriptionally active Ty1-copia retrotransposon from Citrus sinensis. Mol. Genet. Genomics 277: 365-377.
47. Riso, P., Visioli, F., Gardana, C., Grande, S., Brusamolino, A., Galvano, F., Galvano, G., and Porrini, M. (2005). Effects of blood orange juice intake on antioxidant bioavailability and on different markers related to oxidative stress. J. Agric. Food Chem. 53: 941-947.
48. Schwinn, K., Venail, J., Shang, Y.J., Mackay, S., Alm, V., Butelli, E., Oyama, R., Bailey, P., Davies, K., and Martin, C. (2006). A small family of MYB-regulatory genes controls floral pigmentation intensity and patterning in the genus Antirrhinum. Plant Cell 18: 831-851.
49. Scora, R.W. (1975). On the history and origin of Citrus. Bull. Torrey Bot. Club 102: 369-375.
50. Shapiro, J.A. (2005). Retrotransposons and regulatory suites. Bioessays 27: 122-125.
51. Spiegel-Roy, P. (1979). Chimeral nature of the shamouti orange. Euphytica 28: 361-365.
52. Stracke, R., Werber, M., and Weisshaar, B. (2001). The R2R3-MYB gene family in Arabidopsis thaliana. Curr. Opin. Plant Biol. 4: 447-456.
53. Takos, A.M., Jaffé, F.W., Jacob, S.R., Bogs, J., Robinson, S.P., and Walker, A.R. (2006). Light-induced expression of a MYB gene regulates anthocyanin biosynthesis in red apples. Plant Physiol. 142: 1216-1232.
54. Tao, N.G., Xu, J., Cheng, Y.J., Hong, L., Guo, W.W., Yi, H.L., and Deng, X.X. (2005). Isolation and characterization of Copia-like retrotransposons from 12 sweet orange (Citrus sinensis Osbeek) cultivars. J. Int. Biol. 47: 1507-1515.
55. Titta, L., et al. (2010). Blood orange juice inhibits fat accumulation in mice. Int J Obes (Lond) 34: 578-588.
56. Toufektsian, M.C., et al. (2008). Chronic dietary intake of plant-derived anthocyanins protects the rat heart against ischemia-reperfusion injury. J. Nutr. 138: 747-752.
57. Walker, A.R., Lee, E., Bogs, J., McDavid, D.A.J., Thomas, M.R., and Robinson, S.P. (2007). White grapes arose through the mutation of two similar and adjacent regulatory genes. Plant J. 49: 772-785.
58. Wessler, S.R. (1996). Turned on by stress. Plant retrotransposons. Curr. Biol. 6: 959-961.
59. Winkel-Shirley, B. (2001). Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol. 126: 485-493.
60. Yuan, F., Long, G., and Deng, Z. (2008). Jingxian blood orange: The only pigmented sweet orange cultivar originated in China. In Abstracts of the 11th International Citrus Congress, Proceedings of the International Society of Citriculture, Vol. 1. (Beijing: China Agriculture Press), pp 70-72. China.
61. Zarba, A.S., and Pulvirenti, G. (2006). The consumption of Sicilian red oranges: Implications for firms involved in commercialization. J. Business Chemistry 3: 22-41.
62. Zimmermann, I.M., Heim, M.A., Weisshaar, B., and Uhrig, J.F. (2004). Comprehensive identification of Arabidopsis thaliana MYB transcription factors interacting with R/B-like BHLH proteins. Plant J. 40: 22-34.