Skip to main content
Log in

Phototropin 2 is involved in blue light-induced anthocyanin accumulation in Fragaria x ananassa fruits

  • Regular Paper
  • Published:
Journal of Plant Research Aims and scope Submit manuscript

Abstract

Anthocyanins are widespread, essential secondary metabolites in higher plants during color development in certain flowers and fruits. In strawberries, anthocyanins are also key contributors to fruit antioxidant capacity and nutritional value. However, the effects of different light qualities on anthocyanin accumulation in strawberry (Fragaria x ananassa, cv. Sachinoka) fruits remain elusive. In the present study, we showed the most efficient increase in anthocyanin content occurred by blue light irradiation. Light sensing at the molecular level was investigated by isolation of two phototropin (FaPHOT1 and FaPHOT2), two cryptochrome (FaCRY1 and FaCRY2), and two phytochrome (FaPHYA and FaPHYB) homologs. Expression analysis revealed only FaPHOT2 transcripts markedly increased depending on fruit developmental stage, and a corresponding increase in anthocyanin content was detected. FaPHOT2 knockdown resulted in decreased anthocyanin content; however, overexpression increased anthocyanin content. These findings suggested blue light induced anthocyanin accumulation, and FaPHOT2 may play a role in sensing blue light, and mediating anthocyanin biosynthesis in strawberry fruits. This is the first report to find a relationship between visible light sensing, and color development in strawberry fruits.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

Cry:

Cryptochrome

Phot:

Phototropin

Phy:

Phytochrome

LOV:

Light, oxygen or voltage

PAL:

Phenylalanine ammonia-lyase

CHS:

Chalcone synthase

CHI:

Chalcone isomerase

F3H:

Flavanone 3-hydroxylase

DFR:

Dihydroflavonol-4-reductase

ANS:

Anthocyanidin synthase

FGT:

Flavonoid glycosyltransferase

References

  • 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 x ananassa). Arch Biochem Biophys 465:61–71. doi:10.1016/j.abb.2007.04.040

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Briggs WR, Christie JM (2002) Phototropins 1 and 2: versatile plant blue-light receptors. Trends Plant 7:204–210. doi:10.1016/S1360-1385(02)02245-8

    Article  CAS  Google Scholar 

  • Christie JM (2007) Phototropin blue-light receptors. Annu Rev Plant Biol 58:21–45. doi:10.1146/annurev.arplant.58.032806.103951

    Article  PubMed  CAS  Google Scholar 

  • Christie JM, Arvai AS, Baxter KJ, Heilmann M, Pratt AJ, O’Hara A, Kelly SM, Hothorn M, Smith BO, Hitomi K, Jenkins GI, Getzoff ED (2012) Plant UVR8 photoreceptor senses UV-B by tryptophan-mediated disruption of cross-dimer salt bridges. Science 335:1492–1496. doi:10.1126/science.1218091

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Feng S, Wang Y, Yang S, Xu Y, Chen X (2010) Anthocyanin biosynthesis in pears is regulated by a R2R3-MYB transcription factor PyMYB10. Planta 232:245–255. doi:10.1007/s00425-010-1170-5

    Article  PubMed  CAS  Google Scholar 

  • Ferreyra ML, Rius S, Emiliani J, Pourcel L, Feller A, Morohashi K, Casati P, Grotewold E (2010) Cloning and characterization of a UV-B-inducible maize flavonol synthase. Plant J 62:77–91. doi:10.1111/j.1365-313X.2010.04133.x

    Article  CAS  Google Scholar 

  • Frohnmeyer H, Bowler C, Schäfer E (1997) Evidence for some signal transduction elements involved in UV-light-dependent responses in parsley protoplast. J Exp Bot 48:739–750. doi:10.1093/jxb/48.3.739

    Article  CAS  Google Scholar 

  • Fuglevand G, Jackson JA, Jenkins GI (1996) UV-B, UV-A, and blue light signal transduction pathways interact synergistically to regulate chalcone synthase gene expression in Arabidopsis. Plant Cell 8:2347–2357. doi:10.1105/tpc.8.12.2347

    PubMed  CAS  Google Scholar 

  • Giampieri F, Tulipani S, Alvarez-Suarez JM, Quiles JL, Mezzetti B, Battino M (2012) The strawberry: composition, nutritional quality, and impact on human health. Nutrition 28:9–19. doi:10.1016/j.nut.2011.08.009

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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.080708.100754

    Article  PubMed  CAS  Google Scholar 

  • Hoffmann T, Kalinowski G, Schwab W (2006) RNAi-induced silencing of gene expression in strawberry fruit (Fragaria x ananassa) by agroinfiltration: a rapid assay for gene function analysis. Plant J 48:818–826. doi:10.1111/j.1365-313X.2006.02913.x

    Article  PubMed  CAS  Google Scholar 

  • Jain M, Sharma P, Tyagi SB, Tyagi AK, Khurana JP (2007) Light regulation and differential tissue-specific expression of phototropin homologues from rice (Oryza sativa ssp. indica). Plant Sci 172:164–171. doi:10.1016/j.plantsci.2006.08.003

    Article  CAS  Google Scholar 

  • Jang IC, Henriques R, Seo HS, Nagatani A, Chua NH (2010) Arabidopsis PHYTOCHROME INTERACTING FACTOR Proteins Promote Phytochrome B Polyubiquitination by COP1 E3 Ligase in the Nucleus. Plant Cell 22:2370–2383. doi:10.1105/tpc.109.072520

    Article  PubMed  CAS  Google Scholar 

  • Jarillo JA, Gabrys H, Capel J, Alonso JM, Ecker JR, Cashmore AR (2001) Phototropin-related NPL1 controls chloroplast relocation induced by blue light. Nature 410:952–954. doi:10.1038/35073622

    Article  PubMed  CAS  Google Scholar 

  • Jeong RD, Chandra-Shekara AC, Barman SR, Navarre D, Klessig DF, Kachroo A, Kachroo P (2010) Cryptochrome 2 and phototropin 2 regulate resistance protein-mediated viral defense by negatively regulating an E3 ubiquitin ligase. Proc Natl Acad Sci USA 107:13538–13543. doi:10.1073/pnas.1004529107

    Article  PubMed  CAS  Google Scholar 

  • Jiao Y, Yang H, Ma L, Sun N, Yu H, Liu T, Gao Y, Gu H, Chen Z, Wada M, Gerstein M, Zhao H, Qu LJ, Deng XW (2003) A genome-wide analysis of blue-light regulation of Arabidopsis transcription factor gene expression during seedling development. Plant Physiol 133:1480–1493. doi:10.1104/pp.103.029439

    Article  PubMed  CAS  Google Scholar 

  • Jiao Y, Lau OS, Deng XW (2007) Light-regulated transcriptional networks in higher plants. Nat Rev Genet 8:217–230. doi:10.1038/nrg2049

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Kataoka I, Sugiyama A, Beppu K (2003) Role of ultraviolet radiation in accumulation of anthocyanin in berries of ‘Gros Colman’ grapes (Vitis vinifera L.). J Jpn Soc Hortic Sci 72:1–6

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Kubasek WL, Shirley BW, McKillop A, Goodman HM, Briggs W, Ausubel FM (1992) Regulation of Flavonoid Biosynthetic Genes in Germinating Arabidopsis Seedlings. Plant Cell 4:1229–1236. doi:10.1105/tpc.4.10.1229

    PubMed  CAS  Google Scholar 

  • Łabuz J, Sztatelman O, Banaś AK, Gabryś H (2012) The expression of phototropins in Arabidopsis leaves: developmental and light regulation. J Exp Bot 63:1763–1771. doi:10.1093/jxb/ers061

    Article  PubMed  Google Scholar 

  • Li QH, Yang HQ (2007) Cryptochrome signaling in plants. Photochem Photobiol 83:94–101. doi:10.1562/2006-02-28-IR-826

    Article  PubMed  CAS  Google Scholar 

  • Li YY, Mao K, Zhao C, Zhao XY, Zhang HL, Shu HR, Hao YJ (2012) MdCOP1 ubiquitin E3 ligases interact with MdMYB1 to regulate light-induced anthocyanin biosynthesis and red fruit coloration in apple. Plant Physiol 160:1011–1022. doi:10.1104/pp.112.199703

    Article  PubMed  CAS  Google Scholar 

  • Liu H, Liu B, Zhao C, Pepper M, Lin C (2011) The action mechanisms of plant cryptochromes. Trends Plant Sci 16:684–691. doi:10.1016/j.tplants.2011.09.002

    Article  PubMed  CAS  Google Scholar 

  • Ma L, Li J, Qu L, Hager J, Chen Z, Zhao H, Deng XW (2001) Light control of Arabidopsis development entails coordinated regulation of genome expression and cellular pathways. Plant Cell 13:2589–2607. doi:10.1105/tpc.010229

    PubMed  CAS  Google Scholar 

  • Mao J, Zhang YC, Sang Y, Li QH, Yang HQ (2005) From The Cover: A role for Arabidopsis cryptochromes and COP1 in the regulation of stomatal opening. Proc Natl Acad Sci USA 102:12270–12275. doi:10.1073pnas.0501011102

    Article  PubMed  CAS  Google Scholar 

  • Mazza G, Miniati E (1993) Anthocyanins in Fruits Vegetables and Grains. CRC Press, Boca Raton, pp 149–199

    Google Scholar 

  • Meyers KJ, Watkins CB, Pritts MP, Liu RH (2003) Antioxidant and antiproliferative activities of strawberries. J Agric Food Chem 51:6887–6892. doi:10.1021/jf034506n

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Möglich A, Yang X, Ayers RA, Moffat K (2010) Structure and function of plant photoreceptors. Annu Rev Plant Biol 61:21–47. doi:10.1146/annurev-arplant-042809-112259

    Article  PubMed  Google Scholar 

  • Niu SS, Xu CJ, Zhang WS, Zhang B, Li X, Lin-Wang K, Ferguson IB, Allan AC, Chen KS (2010) Coordinated regulation of anthocyanin biosynthesis in Chinese bayberry (Myrica rubra) fruit by a R2R3 MYB transcription factor. Planta 231:887–899. doi:10.1007/s00425-009-1095-z

    Article  PubMed  CAS  Google Scholar 

  • Piazza P, Procissi A, Jenkins GI, Tonelli C (2002) Members of the c1/pl1 regulatory gene family mediate the response of maize aleurone and mesocotyl to different light qualities and cytokinins. Plant Physiol 128:1077–1086. doi:10.1104/pp.010799

    Article  PubMed  CAS  Google Scholar 

  • Rizzini L, Favory JJ, Cloix C, Faggionato D, O’Hara A, Kaiserli E, Baumeister R, Schäfer E, Nagy F, Jenkins GI, Ulm R (2011) Perception of UV-B by the Arabidopsis UVR8 protein. Science 332:103–106. doi:10.1126/science.1200660

    Article  PubMed  CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Sharrock RA, Clack T (2002) Patterns of expression and normalized levels of the five Arabidopsis phytochromes. Plant Physiol 130:442–456. doi:10.1104/pp.005389

    Article  PubMed  CAS  Google Scholar 

  • Shulaev V, Sargent DJ, Crowhurst RN, Mockler TC, Folkerts O, Delcher AL, Jaiswal P, Mockaitis K, Liston A, Mane SP, Burns P, Davis TM, Slovin JP, Bassil N, Hellens RP, Evans C, Harkins T, Kodira C, Desany B, Crasta OR, Jensen RV, Allan AC, Michael TP, Setubal JC, Celton JM, Rees DJ, Williams KP, Holt SH, Ruiz Rojas JJ, Chatterjee M, Liu B, Silva H, Meisel L, Adato A, Filichkin SA, Troggio M, Viola R, Ashman TL, Wang H, Dharmawardhana P, Elser J, Raja R, Priest HD, Bryant DW Jr, Fox SE, Givan SA, Wilhelm LJ, Naithani S, Christoffels A, Salama DY, Carter J, Lopez Girona E, Zdepski A, Wang W, Kerstetter RA, Schwab W, Korban SS, Davik J, Monfort A, Denoyes-Rothan B, Arus P, Mittler R, Flinn B, Aharoni A, Bennetzen JL, Salzberg SL, Dickerman AW, Velasco R, Borodovsky M, Veilleux RE, Folta KM (2011) The genome of woodland strawberry (Fragaria vesca). Nat Genet 43:109–116. doi:10.1038/ng.740

    Article  PubMed  CAS  Google Scholar 

  • 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 142:1216–12132. doi:10.1104/pp.106.088104

    Article  PubMed  CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680. doi:10.1093/nar/22.22.4673

    Article  PubMed  CAS  Google Scholar 

  • Ubi BE, Honda C, Bessho H, Kondo S, Wada M, Kobayashi S, Moriguchi T (2006) Expression analysis of anthocyanin biosynthetic genes in apple skin: effect of UV-B and temperature. Plant Sci 170:571–578. doi:10.1016/j.plantsci.2005.10.009

    Article  CAS  Google Scholar 

  • Vogt T (2010) Phenylpropanoid biosynthesis. Mol Plant 3:2–20. doi:10.1093/mp/ssp106

    Article  PubMed  CAS  Google Scholar 

  • Wade HK, Bibikova TN, Valentine WJ, Jenkins GI (2001) Interactions within a network of phytochrome, cryptochrome and UV-B phototransduction pathways regulate chalcone synthase gene expression in Arabidopsis leaf tissue. Plant J 25:675–685. doi:10.1046/j.1365-313x.2001.01001.x

    Article  PubMed  CAS  Google Scholar 

  • Weller JL, Perrotta G, Schreuder ME, van Tuinen A, Koornneef M, Giuliano G, Kendrick RE (2001) Genetic dissection of blue-light sensing in tomato using mutants deficient in cryptochrome 1 and phytochromes A, B1 and B2. Plant J 25:427–440. doi:10.1046/j.1365-313x.2001.00978.x

    Article  PubMed  CAS  Google Scholar 

  • Winkel-Shirley B (2001) Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol 126:485–493. doi:10.1104/pp.126.2.485

    Article  PubMed  CAS  Google Scholar 

  • Wu D, Hu Q, Yan Z, Chen W, Yan C, Huang X, Zhang J, Yang P, Deng H, Wang J, Deng X, Shi Y (2012) Structural basis of ultraviolet-B perception by UVR8. Nature 484:214–219. doi:10.1038/nature10931

    Article  PubMed  Google Scholar 

  • Zhang Y, Seeram NP, Lee R, Feng L, Heber D (2008) Isolation and identification of strawberry phenolics with antioxidant and human cancer cell antiproliferative properties. J Agric Food Chem 56:670–675. doi:10.1021/jf071989c

    Article  PubMed  CAS  Google Scholar 

  • Zhou B, Li Y, Xu Z, Yan H, Homma S, Kawabata S (2007) Ultraviolet A-specific induction of anthocyanin biosynthesis in the swollen hypocotyls of turnip (Brassica rapa). J Exp Bot 58:1771–1781. doi:10.1093/jxb/erm036

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Koichi Hayashi for donating strawberry fruit samples. We also thank Toshifumi Miki and Keisuke Hirota (Tokushima Agricultural Research Center, Japan) for invaluable advice and donations of strawberry fruit samples. Ourgenic Co., Ltd. supported this work (Tokushima, Japan). This work was also financially supported by the LED-Life project of the University of Tokushima, Japan.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Akira Takahashi.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PPTX 1449 kb)

Supplementary material 2 (DOCX 110 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kadomura-Ishikawa, Y., Miyawaki, K., Noji, S. et al. Phototropin 2 is involved in blue light-induced anthocyanin accumulation in Fragaria x ananassa fruits. J Plant Res 126, 847–857 (2013). https://doi.org/10.1007/s10265-013-0582-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-013-0582-2

Keywords

Navigation