Advertisement

Planta

, Volume 241, Issue 4, pp 953–965 | Cite as

Light and abscisic acid independently regulated FaMYB10 in Fragaria × ananassa fruit

  • Yasuko Kadomura-IshikawaEmail author
  • Katsuyuki Miyawaki
  • Akira Takahashi
  • Toshiya Masuda
  • Sumihare Noji
Original Article

Abstract

Main conclusion

Light and ABA independently regulated anthocyanin biosynthesis via activation of FaMYB10 expression. FaMYB10 accelerated anthocyanin synthesis of pelargonidin 3-glucoside and cyanidin 3-glucoside during strawberry fruit ripening.

Light is an integral factor in fruit ripening. Ripening in non-climacteric fruit is also effected by the plant hormone abscisic acid (ABA). However, how light and/or ABA regulate fruit ripening processes, such as strawberry color development remains elusive. Results of the present study showed light and ABA regulated strawberry fruit coloration via activation of FaMYB10 expression, an R2R3 MYB transcription factor. Light exposure increased FaMYB10 transcript levels, flavonoid pathway genes, and anthocyanin content. Exogenous ABA promoted FaMYB10 expression, and anthocyanin content, accompanied by increased ABA-responsive transcript levels and flavonoid pathway genes. ABA biosynthesis inhibitor treatment, and RNAi-mediated down-regulation of the ABA biosynthetic gene (9-cis epoxycarotenoid dioxygenase: FaNCED1), and ABA receptor (magnesium chelatase H subunit: FaCHLH/ABAR) showed inverse ABA effects. Furthermore, additive effects were observed in anthocyanin accumulation under combined light and ABA, indicating independent light and ABA signaling pathways. FaMYB10 down-regulation by Agrobacterium-mediated RNA interference (RNAi) in strawberry fruits showed decreased pelargonidin 3-glucoside and cyanidin 3-glucoside levels, accompanied by consistent flavonoid pathway gene expression levels. FaMYB10 over-expression showed opposite FaMYB10 RNAi phenotypes, particularly cyanidin 3-glucoside synthesis by FaMYB10, which was correlated with FaF3′H transcript levels. These data provided evidence that light and ABA promoted FaMYB10 expression, resulting in anthocyanin accumulation via acceleration of flavonoid pathway gene expression. Finally, our results suggested FaMYB10 serves a role as a signal transduction mediator from light and ABA perception to anthocyanin synthesis in strawberry fruit.

Keywords

Abscisic acid (ABA) Anthocyanins Flavonoid pathway Light MYB transcription factor Strawberry fruit 

Abbreviations

ABA

Abscisic acid

CHS

Chalcone synthase

CHI

Chalcone isomerase

CHLH/ABAR

Magnesium chelatase H subunit

F3′H

Flavonoid 3′-hydroxylase

F3H

Flavanone 3-hydroxylase

DFR

Dihydroflavonol-4-reductase

ANS

Anthocyanidin synthase

FGT

Flavonoid glycosyltransferase

TF

Transcription factors

NCED

9-cis epoxycarotenoid dioxygenase

Notes

Acknowledgments

We thank Koichi Hayashi for cultivating and donating strawberry fruit samples. We also thank Toshifumi Miki and Keisuke Hirota (Tokushima Agricultural Research Center, Japan) for invaluable advice, and additional strawberry fruit samples. Ourgenic Co. Ltd (Tokushima, Japan) supported this research. LED-Life project of the University of Tokushima, Japan, also provided financial support for this work.

Supplementary material

425_2014_2228_MOESM1_ESM.pdf (76 kb)
Supplementary material 1 (PDF 76 kb)
425_2014_2228_MOESM2_ESM.pdf (265 kb)
Supplementary material 2 (PDF 264 kb)
425_2014_2228_MOESM3_ESM.doc (62 kb)
Supplementary material 3 (DOC 61 kb)

References

  1. Aharoni A, De Vos CH, Wein M, Sun Z, Greco R, Kroon A, Mol JN, O’Connell AP (2001) The strawberry FaMYB1 transcription factor suppresses anthocyanin and flavonol accumulation in transgenic tobacco. Plant J 28:319–332. doi: 10.1046/j.1365-313X.2001.01154.x CrossRefPubMedGoogle Scholar
  2. Ahmad M, Lin C, Cashmore AR (1995) Mutations throughout an Arabidopsis blue-light photoreceptor impair blue-light-responsive anthocyanin accumulation and inhibition of hypocotyl elongation. Plant J 8:653–658. doi: 10.1046/j.1365-313X.1995.08050653.x CrossRefPubMedGoogle Scholar
  3. Alexander L, Grierson D (2002) Ethylene biosynthesis and action in tomato: a model for climacteric fruit ripening. J Exp Bot 53:2039–2055. doi: 10.1093/jxb/erf072 CrossRefPubMedGoogle Scholar
  4. Almeida JR, D’Amico E, Preuss A, Carbone F, de Vos CH, Deiml B, Mourgues F, Perrotta G, Fischer TC, Bovy AG, Martens S, Rosati C (2007) Characterization of major enzymes and genes involved in flavonoid and proanthocyanidin biosynthesis during fruit development in strawberry (Fragaria xananassa). Arch Biochem Biophys 465:61–71. doi: 10.1016/j.abb.2007.04.040 CrossRefPubMedGoogle Scholar
  5. Anttonen MJ, Hoppula KI, Nestby R, Verheul MJ, Karjalainen RO (2006) Influence of fertilization, mulch color, early forcing, fruit order, planting date, shading, growing environment, and genotype on the contents of selected phenolics in strawberry (Fragaria × ananassa Duch.) fruits. J Agric Food Chem 54:2614–2620. doi: 10.1021/jf052947w CrossRefPubMedGoogle Scholar
  6. Azuma A, Yakushiji H, Koshita Y, Kobayashi S (2012) Flavonoid biosynthesis-related genes in grape skin are differentially regulated by temperature and light conditions. Planta 236:1067–1080. doi: 10.1007/s00425-012-1650-x CrossRefPubMedGoogle Scholar
  7. Baudry A, Heim MA, Dubreucq B, Caboche M, Weisshaar B, Lepiniec L (2004) TT2, TT8, and TTG1 synergistically specify the expression of BANYULS and proanthocyanidin biosynthesis in Arabidopsis thaliana. Plant J 39:366–380. doi: 10.1111/j.1365-313X.2004.02138.x CrossRefPubMedGoogle Scholar
  8. 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. doi: 10.1105/tpc.12.12.2383 CrossRefPubMedCentralPubMedGoogle Scholar
  9. Carbone F, Preuss A, De Vos RC, D’Amico E, Perrotta G, Bovy AG, Martens S, Rosati C (2009) Developmental, genetic and environmental factors affect the expression of flavonoid genes, enzymes and metabolites in strawberry fruits. Plant Cell Environ 32:1117–1131. doi: 10.1111/j.1365-3040.2009.01994.x CrossRefPubMedGoogle Scholar
  10. Chai YM, Jia HF, Li CL, Dong QH, Shen YY (2011) FaPYR1 is involved in strawberry fruit ripening. J Exp Bot 62:5079–5089. doi: 10.1093/jxb/err207 CrossRefPubMedGoogle Scholar
  11. Chatterjee M, Sharma P, Khurana JP (2006) Cryptochrome 1 from Brassica napus is up-regulated by blue light and controls hypocotyl/stem growth and anthocyanin accumulation. Plant Physiol 141:61–74. doi: 10.1104/pp.105.076323 CrossRefPubMedCentralPubMedGoogle Scholar
  12. Chernys JT, Zeevaart JAD (2007) Characterization of the 9-cis-epoxycarotenoid dioxygenase gene family and the regulation of abscisic acid biosynthesis in avocado. Plant Physiol 124:343–353. doi: 10.1104/pp.124.1.343 CrossRefGoogle Scholar
  13. Cominelli E, Gusmaroli G, Allegra D, Galbiati M, Wade HK, Jenkins GI, Tonelli C (2008) Expression analysis of anthocyanin regulatory genes in response to different light qualities in Arabidopsis thaliana. J Plant Physiol 165:886–894. doi: 10.1016/j.jplph.2007.06.010 CrossRefPubMedGoogle Scholar
  14. Daminato M, Guzzo F, Casadoro G (2013) A SHATTERPROOF-like gene controls ripening in non-climacteric strawberries, and auxin and abscisic acid antagonistically affect its expression. J Exp Bot 64:3775–3786. doi: 10.1093/jxb/ert214 CrossRefPubMedCentralPubMedGoogle Scholar
  15. Davies C, Boss PK, Robinson SP (1997) Treatment of grape berries, a nonclimacteric fruit with a synthetic auxin, retards ripening and alters the expression of developmentally regulated genes. Plant Physiol 115:1155–1161. doi: 10.1104/pp.115.3.1155 PubMedCentralPubMedGoogle Scholar
  16. Deikman J (1997) Molecular mechanisms of ethylene regulation of gene transcription. Physiol Plant 100:561–566. doi: 10.1111/j.1399-3054.1997.tb03061.x CrossRefGoogle Scholar
  17. Dubos C, Le Gourrierec J, Baudry A, Huep G, Lanet E, Debeaujon I, Routaboul JM, Alboresi A, Weisshaar B, Lepiniec L (2008) MYBL2 is a new regulator of flavonoid biosynthesis in Arabidopsis thaliana. Plant J 55:940–953. doi: 10.1111/j.1365-313X.2008.03564.x CrossRefPubMedGoogle Scholar
  18. Dussi MC, Sugar D, Wrolstad RE (1995) Characterizing and quantifying anthocyanins in red pears and the effect of light quality on fruit color. J Am Soc Hortic Sci 120:785–789Google Scholar
  19. Fait A, Hanhineva K, Beleggia R, Dai N, Rogachev I, Nikiforova VJ, Fernie AR, Aharoni A (2008) Reconfiguration of the achene and receptacle metabolic networks during strawberry fruit development. Plant Physiol 148:730–750. doi: 10.1104/pp.108.120691 CrossRefPubMedCentralPubMedGoogle Scholar
  20. Finkelstein RR, Gampala SS, Rock CD (2002) Abscisic acid signaling in seeds and seedlings. Plant Cell 14:S15–S45. doi: 10.1105/tpc.010441 PubMedCentralPubMedGoogle Scholar
  21. Gapper NE, McQuinn RP, Giovannoni JJ (2013) Molecular and genetic regulation of fruit ripening. Plant Mol Biol 82:575–591. doi: 10.1007/s11103-013-0050-3 CrossRefPubMedGoogle Scholar
  22. Giliberto L, Perrotta G, Pallara P, Weller JL, Fraser PD, Bramley PM, Fiore A, Tavazza M, Giuliano G (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. doi: 10.1104/pp.104.051987 CrossRefPubMedCentralPubMedGoogle Scholar
  23. Giovannoni JJ (2004) Genetic regulation of fruit development and ripening. Plant Cell 16:S170–S180. doi: 10.1105/tpc.019158 CrossRefPubMedCentralPubMedGoogle Scholar
  24. He J, Giusti MM (2010) Anthocyanins: natural colorants with health-promoting properties. Annu Rev Food Sci Technol 1:163–187. doi: 10.1146/annurev.food.080708 CrossRefPubMedGoogle Scholar
  25. Hirayama T, Shinozaki K (2007) Perception and transduction of abscisic acid signals: keys to the function of the versatile plant hormone ABA. Trends Plant Sci 12:343–351. doi: 10.1016/j.tplants.2007.06.013 CrossRefPubMedGoogle Scholar
  26. Hoffmann T, Kalinowski G, Schwab W (2006) RNAi-induced silencing of gene expression in strawberry fruit (Fragaria × ananassa) by agroinfiltration: a rapid assay for gene function analysis. Plant J 48:818–826. doi: 10.1111/j.1365-313X.2006.02913.x CrossRefPubMedGoogle Scholar
  27. Jia HJ, Araki A, Okamoto G (2005) Influence of fruit bagging on aroma volatiles and skin coloration of “Hakuho” peach (Prunus persica Batsch). Postharvest Biol Technol 35:61–68. doi: 10.1016/j.postharvbio.2004.06.004 CrossRefGoogle Scholar
  28. Jia HF, Chai YM, Li CL, Lu D, Luo JJ, Qin L, Shen YY (2011) Abscisic acid plays an important role in the regulation of strawberry fruit ripening. Plant Physiol 157:188–199. doi: 10.1104/pp.111.177311 CrossRefPubMedCentralPubMedGoogle Scholar
  29. Jia H, Wang Y, Sun M, Li B, Han Y, Zhao Y, Li X, Ding N, Li C, Ji W, Jia W (2013a) Sucrose functions as a signal involved in the regulation of strawberry fruit development and ripening. New Phytol 198:453–465. doi: 10.1111/nph.12176 CrossRefPubMedGoogle Scholar
  30. Jia HF, Lu D, Sun JH, Li CL, Xing Y, Qin L, Shen YY (2013b) Type 2C protein phosphatase ABI1 is a negative regulator of strawberry fruit ripening. J Exp Bot 64:1677–1687. doi: 10.1093/jxb/ert028 CrossRefPubMedCentralPubMedGoogle Scholar
  31. Jiang Y, Joyce DC (2003) ABA effects on ethylene production, PAL activity, anthocyanin and phenolic contents of strawberry fruit. Plant Growth Regul 39:171–174. doi: 10.1023/A:1022539901044 CrossRefGoogle Scholar
  32. Jin H, Cominelli E, Bailey P, Parr A, Mehrtens F, Jones J, Tonelli C, Weisshaar B, Martin C (2000) Transcriptional repression by AtMYB4 controls production of UV-protecting sunscreens in Arabidopsis. EMBO J 19:6150–6161. doi: 10.1093/emboj/19.22.6150 CrossRefPubMedCentralPubMedGoogle Scholar
  33. Josuttis M, Dietrich H, Treutter D, Will F, Linnemannstöns L, Krüger E (2010) Solar UVB response of bioactives in strawberry (Fragaria × ananassa Duch. L.): a comparison of protected and open-field cultivation. J Agric Food Chem 58:12692–12702. doi: 10.1021/jf102937e CrossRefPubMedGoogle Scholar
  34. Kadomura-Ishikawa Y, Miyawaki K, Noji S, Takahashi A (2013) Phototropin 2 is involved in blue light-induced anthocyanin accumulation in Fragaria × ananassa fruits. J Plant Res 126:847–857. doi: 10.1007/s10265-013-0582-2 CrossRefPubMedGoogle Scholar
  35. Kami C, Lorrain S, Hornitschek P, Fankhauser C (2010) Light-regulated plant growth and development. Curr Top Dev Biol 91:29–66. doi: 10.1016/S0070-2153(10)91002-8 CrossRefPubMedGoogle Scholar
  36. Kano Y, Asahira T (1981) Roles of cytokinin and abscisic acid in the maturing of strawberry fruits. J Jpn Soc Hortic Sci 50:31–36CrossRefGoogle Scholar
  37. Karppinen K, Hirvelä E, Nevala T, Sipari N, Suokas M, Jaakola L (2013) Changes in the abscisic acid levels and related gene expression during fruit development and ripening in bilberry (Vaccinium myrtillus L.). Phytochemistry 95:127–134. doi: 10.1016/j.phytochem.2013.06.023 CrossRefPubMedGoogle Scholar
  38. Kataoka I, Beppu K (2004) UV irradiance increases development of red skin color and anthocyanins in “Hakuho” peach. HortScience 39:1234–1237Google Scholar
  39. 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. doi: 10.1016/S0168-9452(03)00201-2 CrossRefGoogle Scholar
  40. Klee HJ, Giovannoni JJ (2011) Genetics and control of tomato fruit ripening and quality attributes. Annu Rev Genet 45:41–59. doi: 10.1146/annurev-genet-110410-132507 CrossRefPubMedGoogle Scholar
  41. Kobashi K, Gemma H, Iwahori S (1999) Sugar accumulation in peach fruit as affected by abscisic acid (ABA) treatment in relation to some sugar metabolizing enzymes. J Jpn Soc Hortic Sci 68:465–470CrossRefGoogle Scholar
  42. 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. doi: 10.1016/j.tplants.2005.03.002 CrossRefPubMedGoogle Scholar
  43. Kortstee AJ, Khan SA, Helderman C, Trindade LM, Wu Y, Visser RG, Brendolise C, Allan A, Schouten HJ, Jacobsen E (2011) Anthocyanin production as a potential visual selection marker during plant transformation. Transgenic Res 20:1253–1264. doi: 10.1007/s11248-011-9490-1 CrossRefPubMedCentralPubMedGoogle Scholar
  44. Li C, Jia H, Chai Y, Shen Y (2011) Abscisic acid perception and signaling transduction in strawberry: a model for non-climacteric fruit ripening. Plant Signal Behav 6:1950–1953. doi: 10.4161/psb.6.12.18024 CrossRefPubMedCentralPubMedGoogle Scholar
  45. Li YY, Mao K, Zhao C, Zhao XY, Zhang RF, Zhang HL, Shu HR, Hao YJ (2013) Molecular cloning and functional analysis of a blue light receptor gene MdCRY2 from apple (Malus domestica). Plant Cell Rep 32:555–566. doi: 10.1007/s00299-013-1387-4 CrossRefPubMedGoogle Scholar
  46. Lin-Wang K, Bolitho K, Grafton K, Kortstee 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 21(10):50. doi: 10.1186/1471-2229-10-50 CrossRefGoogle Scholar
  47. Lopes-da-Silva F, Escribano-Bailòn MT, Pérez Alonso JJ, Rivas-Gonzalo JC, Santos-Buelga C (2007) Anthocyanin pigments in strawberry. LWT Food Sci Technol 40:374–382. doi: 10.1016/j.lwt.2005.09.018 CrossRefGoogle Scholar
  48. Matsui K, Umemura Y, Ohme-Takagi M (2008) AtMYBL2, a protein with a single MYB domain, acts as a negative regulator of anthocyanin biosynthesis in Arabidopsis. Plant J 55:954–967. doi: 10.1111/j.1365-313X.2008.03565.x CrossRefPubMedGoogle Scholar
  49. Medina-Puche L, Cumplido-Laso G, Amil-Ruiz F, Hoffmann T, Ring L, Rodríguez-Franco A, Caballero JL, Schwab W, Muñoz-Blanco J, Blanco-Portales R (2014) MYB10 plays a major role in the regulation of flavonoid/phenylpropanoid metabolism during ripening of Fragaria × ananassa fruits. J Exp Bot 65:401–417. doi: 10.1093/jxb/ert377 CrossRefPubMedGoogle Scholar
  50. Miyawaki K, Fukuoka S, Kadomura Y, Hamaoka H, Mito T, Ohuchi H, Schwab W, Noji S (2012) Establishment of a novel system to elucidate the mechanisms underlying light-induced ripening of strawberry fruit with an Agrobacterium-mediated RNAi technique. Plant Biotechnol 29:271–277. doi: 10.5511/plantbiotechnology.12.0406a CrossRefGoogle Scholar
  51. Nakashima K, Yamaguchi-Shinozaki K (2013) ABA signaling in stress-response and seed development. Plant Cell Rep 32:959–970. doi: 10.1007/s00299-013-1418-1 CrossRefPubMedGoogle Scholar
  52. Pan QH, Li MJ, Peng CC, Zhang N, Zou X, Zou KQ, Wang XL, Yu XC, Wang XF, Zhang DP (2005) Abscisic acid activates acid invertases in developing grape berry. Physiol Plant 125:157–170. doi: 10.1111/j.1399-3054.2005.00552.x CrossRefGoogle Scholar
  53. Qin X, Zeevaart JA (1999) The 9-cis-epoxycarotenoid cleavage reaction is the key regulatory step of abscisic acid biosynthesis in water-stressed bean. Proc Natl Acad Sci USA 96:15354–15361. doi: 10.1016/j.jplph.2009.01.013 CrossRefPubMedCentralPubMedGoogle Scholar
  54. Rodrigo MJ, Marcos JF, Alférez F, Mallent MD, Zacarías L (2003) Characterization of Pinalate, a novel Citrus sinensis mutant with a fruit specific alteration that results in yellow pigmentation and decreased ABA content. J Exp Bot 54:727–738. doi: 10.1093/jxb/erg083 CrossRefPubMedGoogle Scholar
  55. Rodrigo MJ, Alquezar B, Zacarı´as L (2006) Cloning and characterization of two 9-cis-epoxycarotenoid dioxygenase genes, differentially regulated during fruit maturation and under stress conditions, from orange (Citrus sinensis L. Osbeck). J Exp Bot 57:633–643. doi: 10.1093/jxb/erj048 CrossRefPubMedGoogle Scholar
  56. Rook F, Hadingham SA, Li Y, Bevan MW (2006) Sugar and ABA response pathways and the control of gene expression. Plant Cell Environ 29:426–434. doi: 10.1111/j.1365-3040.2005.01477.x CrossRefPubMedGoogle Scholar
  57. Salvatierra A, Pimentel P, Moya-Leon MA, Caligari PD, Herrera R (2010) Comparison of transcriptional profiles of flavonoid genes and anthocyanin contents during fruit development of two botanical forms of Fragaria chiloensis ssp. chiloensis. Phytochemistry 71:1839–1847. doi: 10.1016/j.phytochem.2010.08.005 CrossRefPubMedGoogle Scholar
  58. Symons GM, Chua YJ, Ross JJ, Quittenden LJ, Davies NW, Reid JB (2012) Hormonal changes during non-climacteric ripening in strawberry. J Exp Bot 63:4741–4750. doi: 10.1093/jxb/ers147 CrossRefPubMedCentralPubMedGoogle Scholar
  59. Tamagnone L, Merida A, Parr A, Mackay S, Culianez-Macia FA, Roberts K, Martin C (1998) The AmMYB308 and AmMYB330 transcription factors from Antirrhinum regulate phenylpropanoid and lignin biosynthesis in transgenic tobacco. Plant Cell 10:135–154. doi: 10.1105/tpc.10.2.135 CrossRefPubMedCentralPubMedGoogle Scholar
  60. Uleberg E, Rohloff J, Jaakola L, Trôst K, Junttila O, Häggman H, Martinussen I (2012) Effects of temperature and photoperiod on yield and chemical composition of northern and southern clones of bilberry (Vaccinium myrtillus L.). J Agric Food Chem 60:10406–10414. doi: 10.1021/jf302924m CrossRefPubMedGoogle Scholar
  61. Wei YZ, Hu FC, Hu GB, Li XJ, Huang XM, Wang HC (2011) Differential expression of anthocyanin biosynthetic genes in relation to anthocyanin accumulation in the pericarp of Litchi chinensis Sonn. PLoS ONE 6:e19455. doi: 10.1371/journal.pone.0019455 CrossRefPubMedCentralPubMedGoogle Scholar
  62. Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803. doi: 10.1146/annurev.arplant.57.032905.105444 CrossRefPubMedGoogle Scholar
  63. Yoshida Y, Koyama N, Tamura H (2002) Color and anthocyanin composition of strawberry fruit: changes during fruit development and differences among cultivars, with special reference to the occurrence of pelargonidin 3-malnoylglucoside. J Japan Soc Hort Sci 71:355–361CrossRefGoogle Scholar
  64. Zhang M, Leng P, Zhang G, Li X (2009a) Cloning and functional analysis of 9-cis-epoxycarotenoid dioxygenase (NCED) genes encoding a key enzyme during abscisic acid biosynthesis from peach and grape fruits. J Plant Physiol 166:1241–1252. doi: 10.1016/j.jplph.2009.01.013 CrossRefPubMedGoogle Scholar
  65. Zhang M, Yuan B, Leng P (2009b) The role of ABA in triggering ethylene biosynthesis and ripening of tomato fruit. J Exp Bot 60:1579–1588. doi: 10.1093/jxb/erp026 CrossRefPubMedCentralPubMedGoogle Scholar
  66. Zhou Y, Singh BR (2004) Effect of light on anthocyanin levels in submerged, harvested cranberry fruit. J Biomed Biotechnol 2004:259–263. doi: 10.1155/S1110724304403027 CrossRefPubMedCentralPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Yasuko Kadomura-Ishikawa
    • 1
    • 2
    Email author
  • Katsuyuki Miyawaki
    • 2
  • Akira Takahashi
    • 1
  • Toshiya Masuda
    • 3
  • Sumihare Noji
    • 2
  1. 1.Department of Nutrition, Faculty of MedicineThe University of TokushimaTokushimaJapan
  2. 2.Department of Life System, Institute of Technology and ScienceThe University of TokushimaTokushimaJapan
  3. 3.Department of Integrated Arts and SciencesThe University of TokushimaTokushimaJapan

Personalised recommendations