Expression and functional analysis of a novel MYB gene, MdMYB110a_JP, responsible for red flesh, not skin color in apple fruit

Planta

Volumn 238, Issue 1, 2013, Pages 65-76

  Umemura, Hitomi ^a   Otagaki, Shungo ^a   Wada, Masato ^b   Kondo, Satoru ^c   Matsumoto, Shogo ^a  

^a NAGOYA UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE OF FRUIT TREE SCIENCE   (Japan)

^c CHIBA UNIVERSITY   (Japan)

Author keywords

Anthocyanin; Malus; MdMYB; Red fleshed apple

Indexed keywords

ANTHOCYANIN; MICROSATELLITE DNA; TRANSCRIPTION FACTOR;

AMINO ACID SEQUENCE; ARTICLE; BIOSYNTHESIS; CHROMOSOME MAP; FRUIT; GENE EXPRESSION REGULATION; GENETICS; MALUS; METABOLISM; MOLECULAR GENETICS; ONCOGENE MYB; PIGMENTATION; TRANSGENIC PLANT;

AMINO ACID SEQUENCE; ANTHOCYANINS; CHROMOSOME MAPPING; FRUIT; GENE EXPRESSION REGULATION, PLANT; GENES, MYB; MALUS; MICROSATELLITE REPEATS; MOLECULAR SEQUENCE DATA; PIGMENTATION; PLANTS, GENETICALLY MODIFIED; TRANSCRIPTION FACTORS;

MALUS; MALUS X DOMESTICA;

EID: 84879499763     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-013-1875-3     Document Type: Article

References (38)

1. Allan AC, Hellens RP, Laing WA (2008) MYB transcription factors that colour our fruit. Trends Plant Sci 13: 99-102.
2. Ban Y, Honda C, Hatsuyama Y, Igarashi M, Bessho H, Moriguchi T (2007) Isolation and functional analysis of a MYB transcription factor gene that is a key regulator for the development of red coloration in apple skin. Plant Cell Physiol 48: 958-970.
3. Broothaerts W, Janssens GA, Proost P, Broekaert WF (1995) cDNA cloning and molecular analysis of two self-incompatibility alleles from apple. Plant Mol Biol 27: 499-511.
4. Butelli E, Titta L, Giorgio M, Mock H-P, Matros A, Peterek S, Schijlen EGWM, Hall RD, Bovy AG, Luo J, Martin C (2008) Enrichment of tomato fruit with health-promoting anthocyanins by expression of select transcription factors. Nat Biotechnol 26: 1301-1308.
5. Celton JM, Tustin DS, Chagné D, Gardiner SE (2009) Construction of a dense genetic linkage map for apple rootstocks using SSRs developed from Malus ESTs and Pyrus genomic sequences. Tree Genet Genomes 5: 93-107.
6. Chagné D, Carlisle CM, Blond C, Volz RK, Whitworth CJ, Oraguzie NC, Crowhurst RN, Allan AC, R. V. Espley RV, Hellens RP, Gardiner SE (2007) Mapping a candidate gene (MdMYB10) for red flesh and foliage colour apple. BMC Genomics 8: 212.
7. Chagné D, Lin-Wang K, Espley RV, Volz RK, How NM, Rouse S, Brendolise C, Carlisle CM, Kumar S, De Silva N, Micheletti D, McGhie T, Crowhurst RN, Storey RD, Velasco R, Hellens RP, Gardiner SE, Allan AC (2013) An ancient duplication of apple MYB transcription factors is responsible for novel red fruit-flesh phenotypes. Plant Physiol 161: 225-239.
8. Chang S, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Rep 11: 113-116.
9. Eberhardt MV, Lee CY, Liu RH (2000) Antioxidant activity of fresh apples. Nature 405: 903-904.
10. Espley RV, Hellens RP, Putterill J, Stevenson DE, Kutty-Amma S, Allan AC (2007) Red colouration in apple fruit is due to the activity of the MYB transcription factor, MdMYB10. Plant J 49: 414-427.
11. Espley RV, Brendolise C, Chagné D, Kutty-Amma S, Green S, Volz R, Putterill J, Schouten HJ, Gardiner SE, Hellens RP, Allan AC (2009) Multiple repeats of a promoter segment causes transcription factor autoregulation in red apples. Plant Cell 21: 168-183.
12. Feller A, Machemer K, Braun EL, Grotewold E (2011) Evolutionary and comparative analysis of MYB and bHLH plant transcription factors. Plant J 66: 94-116.
13. Grotewold E (2004) The challenges of moving chemicals within and out of cells: insights into the transport of plant natural products. Planta 219: 906-909.
14. Honda C, Kotoda N, Wada M, Kondo S, Kobayashi S, Soejima J, Zhang Z, Tsuda T, Moriguchi T (2002) Anthocyanin biosynthetic genes are coordinately expressed during red coloration in apple skin. Plant Physiol Biochem 40: 955-962.
15. Janssens GA, Goderis IJ, Broekaert WF, Broothaerts W (1995) A molecular method for S-allele identification in apple based on allele-specific PCR. Theor Appl Genet 91: 691-698.
16. Kim SH, Lee JR, Hong ST, Yoo YK, An G, Kim SR (2003) Molecular cloning and analysis of anthocyanin biosynthesis genes preferentially expressed in apple skin. Plant Sci 165: 403-413.
17. Lin-Wang K, Bolitho K, Grafton K, Kortsee A, Karunairetnam S, McGhie TK, Espley RV, Hellens RP, Allan AC (2010) An R2R3 MYB transcription factor associated with regulation of the anthocyanin biosynthetic pathway in Rosaceae. BMC Plant Biol 10: 50.
18. Lin-Wang K, Micheletti D, Palmer J, Volz R, Lozano L, Espley R, Hellens RP, Chagné D, Rowan DD, Troggio M, Iglesias I, Allan AC (2011) High temperature reduces apple fruit colour via modulation of the anthocyanin regulatory complex. Plant Cell Environ 34: 1176-1190.
19. Lister CE, Lancaster JE (1996) Developmental changes in enzymes of flavonoid biosynthesis in the skins of red and green apple cultivars. J Sci Food Agric 71: 313-320.
20. Maliepaard C, Alston FH, van Arkel G, Brown LM, Chevreau E, Dunemann F, Evans KM, Gardiner S, Guilford P, van Heusden AW, Janse J, Laurens F, Lynn JR, Manganaris AG, den Nijs APM, Periam N, Rikkerink E, Roche P, Ryder C, Sansavini S, Schmidt H, Tartarini S, Verhaegh JJ, Vrielink-van Ginkel M, King GJ (1998) Aligning male and female linkage maps of apple (Maluspumila Mill.) using multi-allelic markers. Theor Apple Genet 97: 60-73.
21. Matsumoto S, Kitahara K, Komori S, Soejima J (1999) A new S-allele in apple, 'Sg', and its similarity to the 'Sf' allele from 'Fuji'. HortScience 34: 708-710.
22. Nishitani C, Terakami S, Sawamura Y, Takada N, Yamamoto T (2009) Development of novel EST-SSR markers derived from Japanese pear (Pyruspyrifolia). Breed Sci 59: 391-400.
23. Petroni K, Tonelli C (2011) Recent advances on the regulation of anthocyanin synthesis in reproductive organs. Plant Sci 181: 219-229.
24. Sassa H, Kakui H, Minamikawa M (2010) Pollen-expressed F-box gene family and mechanism of S-RNase-based gametophytic self-incompatibility (GSI) in Rosaceae. Sex Plant Reprod 23: 39-43.
25. 3-RNase allele in 'Pink Pearl'. HortScience 45: 534-537.
26. Sekido K, Yamada K, Shiratake K, Fukui H, Matsumoto S (2010b) MdMYB alleles responsible for apple skin and flesh color. Curr Top Plant Biol 11: 17-21.
27. Silfverberg-Dilworth E, Matasci CL, van de Weg WE, van Kaauwen MPW, Walser M, Kodde LP, Soglio V, Gianfranceschi L, Durel CE, Costa F, Yamamoto T, Koller B, Gessler C, Patocchi A (2006) Microsatellite markers spanning the apple (Malus × domestica Borkh.) genome. Tree Genet Genomes 2: 202-224.
28. Takos AM, Jaffé FW, Jacob SR, Bogs J, Robinson SP, Walker AR (2006) Light-induced expression of a MYB gene regulates anthocyanin biosynthesis in red apples. Plant Physiol 142: 1216-1232.
29. Tanaka Y, Sasaki N, Ohmiya A (2008) Biosynthesis of plant pigments: anthocyanins, betalains and carotenoids. Plant J 54: 733-749.
30. Thomas MR, Matsumoto S, Cain P, Scott NS (1993) Repetitive DNA of grapevine: classes present and sequences suitable for cultivar identification. Theor Appl Genet 86: 173-180.
31. Toufektsian M-C, de Lorgeril M, Nagy N, Salen P, Donati MB, Giordano L, Mock H-P, Peterek S, Matros A, Petroni K, Pilu R, Rotilio D, Tonelli C, de Leiris J, Boucher F, Martin C (2008) Chronic dietary intake of plant-derived anthocyanins protects the rat heart against ischemia-reperfusion injury. J Nutr 138: 747-752.
32. Tsao R, Yang R, Young JC, Zhu H (2003) Polyphenolic profiles in eight apple cultivars using High-Performance Liquid Chromatography (HPLC). J Agric Food Chem 51: 6347-6353.
33. Umemura H, Shiratake K, Maejima T, Komatsu H, Matsumoto S (2011) Practical breeding of red-fleshed apple: cultivar combination for efficient red-fleshed progeny production. HortScience 46: 1098-1101.
34. van Nocker S, Berry G, Najdowski J, Michelutti R, Luffman M, Forsline P, Alsmairat N, Beaudry R, Nair MG, Ordidge M (2012) Genetic diversity of red-fleshed apple (Malus). Euphytica 185: 281-293.
35. Wada M, Ureshino A, Tanaka N, Komori S, Takahashi S, Kudo K, Bessho H (2009) Anatomical analysis by two approaches ensures the promoter activities of apple AFL genes. J Soc Hort Sci 78: 32-39.
36. Wang B, He J, Duan C, Yu X, Zhu L, Xie Z, Zhang C, Xu W, Wang S (2012) Root restriction affects anthocyanin accumulation and composition in berry skin of 'Kyoho' grape (Vitis vinifera L. × Vitis labrusca L.) during ripening. Scientia Hort 137: 20-28.
37. Wolfe K, Wu X, Liu RH (2003) Antioxidant activity of apple peels. J Agric Food Chem 51: 609-614.
38. Xu Y, Feng S, Jiao Q, Liu C, Zhang W, Chen W, Chen X (2012) Comparison of MdMYB1 sequences and expression of anthocyanin biosynthetic and regulatory genes between Malusdomestica Borkh. Cultivar 'Ralls' and its blushed sport. Euphytica 185: 157-170.