Skip to main content
SpringerLink
Log in

The blue light signal transduction pathway is involved in anthocyanin accumulation in ‘Red Zaosu’ pear

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

A conserved blue light sensing and transduction pathway contributes to blue light-induced anthocyanin accumulation in the peel of red pear.

Abstract

Peel color is an economically important characteristic that influences the appearance quality of red pear, whose red color is due to anthocyanin accumulation. The process of coloration in the fruit peel is strongly influenced by light. However, how light quality influences color development remains unclear. In this study, we analyzed the effects of different light qualities on color development in the red pear ‘Red Zaosu’, a mutant of the hybrid cultivar ‘Zaosu’ of Pyrus pyrifolia and P. communis. The results showed that blue light increased anthocyanin accumulation after 72 h of light treatment, while red light had almost no effect. The expression of anthocyanin biosynthesis-related genes showed a similar trend to the anthocyanin accumulation. To clarify the mechanism of blue-light induced coloration, PpCRYs, PpCOP1 and PpHY5 genes were cloned. Gene expression analysis showed that their transcript abundance did not correlate with the expression of anthocyanin-related genes or anthocyanin content, but the yeast two-hybrid system revealed conserved physical interactions among these proteins. In addition, PpHY5 directly bound to the promoters of the anthocyanin biosynthesis genes PpCHS, PpDFR, PpANS and PpMYB10, and activated the transcription of PpCHS in a Nicotiana benthamiana-based dual-luciferase assay. In summary, our results preliminarily revealed that the conserved blue light signal transduction module CRY–COP1–HY5 contributed to the anthocyanin biosynthesis induced by blue light in red pear. However, our results did not provide evidence for why red light had no effect on anthocyanin accumulation, which needs further study.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

Abbreviations

ANS:

Anthocyanidin synthase

CHS:

Chalcone synthase

CHI:

Chalcone isomerase

COP1:

CONSTITUTIVE PHOTOMORPHOGENIC 1

CRY:

Cryptochrome

DFR:

Dihydroflavonol 4-reductase

F3H:

Flavanone 3 β-hydroxylase

HY5:

ELONGATED HYPOCOTYL 5

UFGT:

UDP-glucose: flavonoid-3-O-glucosyltransferase

References

  • An J, Qu F, Yao J, Wang X, You C, Wang X, Hao Y (2017) The bZIP transcription factor MdHY5 regulates anthocyanin accumulation and nitrate assimilation in apple. Hortic Res 4:17023

    Article  PubMed  PubMed Central  Google Scholar 

  • Ang L, Chattopadhyay S, Wei N, Oyama T, Okada K, Batschauer A, Deng XW (1998) Molecular interaction between COP1 and HY5 defines a regulatory switch for light control of Arabidopsis development. Mol Cell 1(2):213–222

    Article  PubMed  CAS  Google Scholar 

  • Anglia UOE (2008) Effects of anthocyanin on skin health and markers of cardiovascular disease risk. ClinicalTrials.gov Identifier:NCT00574574

  • Arakawa O, Hori Y, Ogata R (1985) Relative effectiveness and interaction of ultraviolet-B, red and blue light in anthocyanin synthesis of apple fruit. Physiol Plant 64(3):323–327

    Article  CAS  Google Scholar 

  • Bai S, Saito T, Honda M, Hatsuyama Y, Ito A, Moriguchi T (2014) An apple B-box protein, MdCOL11, is involved in UV-B- and temperature-induced anthocyanin biosynthesis. Planta 240(5):1051–1062

    Article  PubMed  CAS  Google Scholar 

  • Bai S, Sun Y, Qian M, Yang F, Ni J, Tao R, Lin L, Shu Q, Dong Z, Teng Y (2017) Transcriptome analysis of bagging-treated red Chinese sand pear peels reveals light-responsive pathway functions in anthocyanin accumulation. Sci Rep 7(1):63

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bulgakov VP, Avramenko TV, Tsitsiashvili GS (2016) Critical analysis of protein signaling networks involved in the regulation of plant secondary metabolism: focus on anthocyanins. Crit Rev Biotech 37:6

    Google Scholar 

  • Chaves I, Pokorny R, Byrdin M, Hoang N, Ritz T, Brettel K, Essen LO, Horst GTJVD, Batschauer A, Ahmad M (2010) The cryptochromes: blue light photoreceptors in plants and animals. Annu Rev Plant Biol 62(1):335–364

    Article  CAS  Google Scholar 

  • Cheng J, Wei L, Wu J (2015) Effect of light quality selective plastic films on anthocyanin biosynthesis in Vitis vinifera L. cv. Yatomi Rosa. J Agr Sci Tech-Iran 17(1):157–166

    Google Scholar 

  • Cluis CP, Mouchel CF, Hardtke CS (2004) The Arabidopsis transcription factor HY5 integrates light and hormone signaling pathways. Plant J 38(2):332–347

    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(8):886–894

    Article  PubMed  CAS  Google Scholar 

  • Cutuli B, Lemanski C, Fourquet A, Lafontan BD, Giard S, Lancrenon S, Meunier A, Pioud-Martigny R, Campana F, Marsiglia H (2010) Environmental significance of anthocyanins in plant stress responses. Photochem Photobiol 70(1):1–9

    Google Scholar 

  • Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L (2010) MYB transcription factors in Arabidopsis. Trends Plant Sci 15(10):573–581

    Article  PubMed  CAS  Google Scholar 

  • Dussi MC, Sugar D, Wrolstad RE (1995) Characterizing and quantifying anthocyanins in red pears and the effect of light quality on fruit color. Amer Soc Horti Sci 120(5):785–789

    CAS  Google Scholar 

  • Eckardt NA (2007) Light regulation of plant development: HY5 genomic binding sites. Plant Cell 19(3):727–729

    Article  PubMed Central  CAS  Google Scholar 

  • Feller A, Machemer K, Braun EL, Grotewold E (2011) Evolutionary and comparative analysis of MYB and bHLH plant transcription factors. Plant J 66(1):94–116

    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(1):245–255

    Article  PubMed  CAS  Google Scholar 

  • Folta KM, Pontin MA, Karlinneumann G, Bottini R, Spalding EP (2003) Genomic and physiological studies of early cryptochrome 1 action demonstrate roles for auxin and gibberellin in the control of hypocotyl growth by blue light. Plant J 36(2):203–214

    Article  PubMed  CAS  Google Scholar 

  • Fox AR, Soto GC, Jones AM, Casal JJ, Muschietti JP, Mazzella MA (2012) cry1 and GPA1 signaling genetically interact in hook opening and anthocyanin synthesis in Arabidopsis. Plant Mol Biol 80(3):315–324

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gangappa SN, Botto JF (2016) The multifaceted roles of HY5 in plant growth and development. Mol Plant 9(10):1353–1365

    Article  PubMed  CAS  Google Scholar 

  • Huang C, Yu B, Teng Y, Su J, Shu Q, Cheng Z, Zeng L (2009) Effects of fruit bagging on coloring and related physiology, and qualities of red Chinese sand pears during fruit maturation. Sci Hortic-Amsterdam 121:149–158

    Article  Google Scholar 

  • Jaakola L (2013) New insights into the regulation of anthocyanin biosynthesis in fruits. Trends Plant Sci 18(9):477–483

    Article  PubMed  CAS  Google Scholar 

  • Jiang M, Ren L, Lian H, Liu Y, Chen H (2016) Novel insight into the mechanism underlying light-controlled anthocyanin accumulation in eggplant (Solanum melongena L.). Plant Sci 249:46–58

    Article  PubMed  CAS  Google Scholar 

  • Koes R, Verweij W, Quattrocchio F (2005) Flavonoids: a colorful model for the regulation and evolution of biochemical pathways. Trends Plant Sci 10(5):236–242

    Article  PubMed  CAS  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23(21):2947–2948

    Article  PubMed  CAS  Google Scholar 

  • Lau OS, Deng X (2012) The photomorphogenic repressors COP1 and DET1: 20 years later. Trends Plant Sci 17(10):584–593

    Article  PubMed  CAS  Google Scholar 

  • Leng P, Itamura H, Yamamura H, Deng X (2000) Anthocyanin accumulation in apple and peach shoots during cold acclimation. Sci Hortic-Amsterdam 83(1):43–50

    Article  CAS  Google Scholar 

  • Li Y, Han L, Ma R, Xu X, Zhao C, Wang Z, Chen F, Hu X (2012a) Effect of energy density and citric acid concentration on anthocyanins yield and solution temperature of grape peel in microwave-assisted extraction process. J Food Eng 109(2):274–280

    Article  CAS  Google Scholar 

  • Li Y, Mao K, Zhao C, Zhao X, Zhang H, Shu H, Hao Y (2012b) MdCOP1 ubiquitin E3 ligases interact with MdMYB1 to regulate light-induced anthocyanin biosynthesis and red fruit coloration in apple. Plant Physiol 160(2):1011–1022

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li Y, Mao K, Zhao C, Zhao X, Zhang R, Zhang H, Shu H, Hao Y (2013) Molecular cloning and functional analysis of a blue light receptor gene MdCRY2 from apple (Malus domestica). Plant Cell Rep 32(4):555–566

    Article  PubMed  CAS  Google Scholar 

  • Liu B, Zuo Z, Liu H, Liu X, Lin C (2011a) Arabidopsis cryptochrome 1 interacts with SPA1 to suppress COP1 activity in response to blue light. Gene Dev 25(10):1029–1034

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liu H, Liu B, Zhao C, Pepper M, Lin C (2011b) The action mechanisms of plant cryptochromes. Trends Plant Sci 16(12):684–691

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liu Z, Zhang Y, Wang J, Li P, Zhao C, Chen Y, Bi Y (2015) Phytochrome-interacting factors PIF4 and PIF5 negatively regulate anthocyanin biosynthesis under red light in Arabidopsis seedlings. Plant Sci 238:64–72

    Article  PubMed  CAS  Google Scholar 

  • Maier A, Schrader A, Kokkelink L, Falke C, Welter B, Iniesto E, Rubio V, Uhrig JF, Hülskamp M, Hoecker U (2013) Light and the E3 ubiquitin ligase COP1/SPA control the protein stability of the MYB transcription factors PAP1 and PAP2 involved in anthocyanin accumulation in Arabidopsis. Plant J 74(4):638–651

    Article  PubMed  CAS  Google Scholar 

  • Miao L, Zhang Y, Yang X, Xiao J, Zhang H, Zhang Z, Wang Y, Jiang G (2016) Colored light-quality selective plastic films affect anthocyanin content, enzyme activities, and the expression of flavonoid genes in strawberry (Fragaria × ananassa) fruit. Food Chem 207:93–100

    Article  PubMed  CAS  Google Scholar 

  • Niu Q, Li J, Cai D, Qian M, Jia H, Bai S, Hussain S, Liu G, Teng Y, Zheng X (2016) Dormancy-associated MADS-box genes and microRNAs jointly control dormancy transition in pear (Pyrus pyrifolia white pear group) flower bud. J Exp Bot 67(1):239–257

    Article  PubMed  CAS  Google Scholar 

  • Quattrocchio F, Wing J, Van DWK, Souer E, De VN, Mol J, Koes R (1999) Molecular analysis of the anthocyanin2 gene of petunia and its role in the evolution of flower color. Plant Cell 11(8):1433–1444

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rizzini L, Favory JJ, Cloix C, Faggionato D, O’Hara A, Kaiserli E, Baumeister R, Schäfer E, Nagy F, Jenkins GI (2011) Perception of UV-B by the Arabidopsis UVR8 protein. Science 332(6025):103–106

    Article  PubMed  CAS  Google Scholar 

  • Rombauts S, Déhais P, Van MM, Rouzé P (1999) PlantCARE, a plant cis-acting regulatory element database. Nucleic Acids Res 27(1):295–296

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Saijo Y, Zhu D, Li J, Rubio V, Zhou Z, Shen Y, Hoecker U, Wang H, Deng X (2008) Arabidopsis COP1/SPA1 complex and phytochrome A signaling intermediates associate with distinct phosphorylated forms of phytochrome A in balancing signal propagation and attenuation. Mol Cell 31(4):607–613

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Seo H, Yang J, Ishikawa M, Bolle C, Ballesteros ML, Chua N (2003) LAF1 ubiquitination by COP1 controls photomorphogenesis and is stimulated by SPA1. Nature 423(6943):995–999

    Article  PubMed  CAS  Google Scholar 

  • Sheerin DJ, Hiltbrunner A (2017) Molecular mechanisms and ecological function of far-red light signalling. Plant Cell Environ 40(11):2509–2529

    Article  PubMed  CAS  Google Scholar 

  • Shin J, Park E, Choi G (2007) PIF3 regulates anthocyanin biosynthesis in an HY5-dependent manner with both factors directly binding anthocyanin biosynthetic gene promoters in Arabidopsis. Plant J 49(6):981–994

    Article  PubMed  CAS  Google Scholar 

  • Shin DH, Choi M, Kim K, Bang G, Cho M, Choi SB, Choi G, Park YI (2013) HY5 regulates anthocyanin biosynthesis by inducing the transcriptional activation of the MYB75/PAP1 transcription factor in Arabidopsis. FEBS Lett 587(10):1543–1547

    Article  PubMed  CAS  Google Scholar 

  • Steyn WJ, Wand SJE, Holcroft DM, Jaobs G (2005) Red colour development and loss in pears. Acta Hortic 671:79–85

    Article  CAS  Google Scholar 

  • Stracke R, Favory JJ, Gruber H, Bartelniewoehner L, Bartels S, Binkert M, Funk M, Weisshaar B, Ulm R (2010) The Arabidopsis bZIP transcription factor HY5 regulates expression of the PFG1/MYB12 gene in response to light and ultraviolet-B radiation. Plant, Cell Environ 33(1):88–103

    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(3):1216–1232

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S, Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2014) MEGA5: molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731–2739

    Article  CAS  Google Scholar 

  • Vandenbussche F, Habricot Y, Condiff AS, Maldiney R, Steaeten DV, Ahmad M (2007) HY5 is a point of convergence between cryptochrome and cytokinin signalling pathways in Arabidopsis thaliana. Plant J 49:428–441

    Article  PubMed  CAS  Google Scholar 

  • Veeriah S, Kautenburger T, Habermann N, Sauer J, Dietrich H, Will F, Poolzobel BL (2006) Apple flavonoids inhibit growth of HT29 human colon cancer cells and modulate expression of genes involved in the biotransformation of xenobiotics. Mol Carcinogen 45(3):164–174

    Article  CAS  Google Scholar 

  • Wang L, Zhang X, Xu J, Zhang G, Ge H (2009) Effect of light quality on the anthocyanin, phenolic and flavonoid compounds of strawberry fruits. J Agric Univ Hebei 32(2):54–57

    CAS  Google Scholar 

  • Wu G, Spalding EP (2007) Separate functions for nuclear and cytoplasmic cryptochrome 1 during photomorphogenesis of Arabidopsis seedlings. Proc Natl Acad Sci USA 104(47):18813–18818

    Article  PubMed  PubMed Central  Google Scholar 

  • Wu J, Wang Z, Shi Z, Zhang S, Ming R, Zhu S, Khan MA, Tao S, Korban SS, Wang H, Chen NJ, Nishio T, Xu X, Cong L, Qi K, Huang X, Wang Y, Zhao X, Wu J, Deng C, Gou C, Zhou W, Yin H, Qin G, Sha Y, Tao Y, Chen H, Yang Y, Song Y, Zhan D, Wang J, Li L, Dai M, Gu C, Wang Y, Shi D, Wang X, Zhang H, Zeng L, Zheng D, Wang C, Chen M, Wang G, Xie L, Sovero V, Sha S, Huang W, Zhang S, Zhang M, Sun J, Xu L, Li Y, Liu X, Li Q, Shen J, Wang J, Paull RE, Bennetzen JL, Wang J, Zhang S (2012) The genome of pear (Pyrus bretschneideri Rehd.). Genome Res 23(2):396–408

    Article  PubMed  CAS  Google Scholar 

  • Xie X, Li S, Zhang R, Zhao J, Chen Y, Zhao Q, Yao Y, You C, Zhang X, Hao Y (2012) The bHLH transcription factor MdbHLH3 promotes anthocyanin accumulation and fruit colouration in response to low temperature in apples. Plant Cell Environ 35(11):1884–1897

    Article  PubMed  CAS  Google Scholar 

  • Xu W, Dubos C, Lepiniec L (2015a) Transcriptional control of flavonoid biosynthesis by MYB–bHLH–WDR complexes. Trends Plant Sci 20(3):176–185

    Article  PubMed  CAS  Google Scholar 

  • Xu X, Paik I, Zhu L, Huq E (2015b) Illuminating progress in phytochrome-mediated light signaling pathways. Trends Plant Sci 20(10):641–650

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto YY, Matsui M, Ang LH, Deng X (1998) Role of a COP1 interactive protein in mediating light-regulated gene expression in Arabidopsis. Plant Cell 10(7):1083–1094

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang D, Yu B, Bai J, Qian M, Shu Q, Su J, Teng Y (2012) Effects of high temperatures on UV-B/visible irradiation induced postharvest anthocyanin accumulation in ‘Yunhongli No. 1’ (Pyrus pyrifolia Nakai) pears. Sci Hortic-Amsterdam 134:53–59

    Article  CAS  Google Scholar 

  • Zuo Z, Liu H, Liu B, Liu X, Lin C (2011) Blue light-dependent interaction of CRY2 with SPA1 regulates COP1 activity and floral initiation in Arabidopsis. Curr Biol 21(10):841–847

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (Grant nos., 31471852 and 31772272) and the Earmarked Fund for China Agriculture Research System (CARS-28).

Author information

Author notes

  1. Ruiyan Tao and Songling Bai contributed equally to this work.

Authors and Affiliations

  1. Department of Horticulture, Zhejiang University, Hangzhou, 310058, Zhejiang, People’s Republic of China

    Ruiyan Tao, Songling Bai, Junbei Ni, Qinsong Yang, Yuan Zhao & Yuanwen Teng

  2. Zhejiang Provincial Key Laboratory of Integrative Biology of Horticultural Plants, Hangzhou, 310058, Zhejiang, People’s Republic of China

    Ruiyan Tao, Songling Bai, Junbei Ni, Qinsong Yang, Yuan Zhao & Yuanwen Teng

  3. The Key Laboratory of Horticultural Plant Growth, Development and Quality Improvement, Ministry of Agriculture of China, Hangzhou, 310058, Zhejiang, People’s Republic of China

    Ruiyan Tao, Songling Bai, Junbei Ni, Qinsong Yang, Yuan Zhao & Yuanwen Teng

Authors
  1. Ruiyan Tao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Songling Bai
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Junbei Ni
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Qinsong Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yuan Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yuanwen Teng
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yuanwen Teng.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tao, R., Bai, S., Ni, J. et al. The blue light signal transduction pathway is involved in anthocyanin accumulation in ‘Red Zaosu’ pear. Planta 248, 37–48 (2018). https://doi.org/10.1007/s00425-018-2877-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-018-2877-y

Keywords

Search

Navigation