Skip to main content
SpringerLink
Log in

Photoperiod and shading regulate coloration and anthocyanin accumulation in the leaves of malus crabapples

  • Original Paper
  • Published:
Plant Cell, Tissue and Organ Culture (PCTOC) Aims and scope Submit manuscript

Abstract

In many ornamental plants, anthocyanin accumulation in leaves is a critical determinant of foliage coloration. However, the mechanism by which photoperiod and shading affect coloration and anthocyanin accumulation in the leaves of woody plants is less clear. By examining the leaves and calli of crabapple (Malus spp.) cultivars with different leaf color characteristics, we analyzed the foliage coloration, flavonoid contents, and expression levels of anthocyanin biosynthetic genes and the McMYB10 transcription factor under different photoperiods and shading treatments. The red color parameters, flavonoid contents, and expression levels of some anthocyanin-related genes in both the leaf and callus were generally higher under sun-exposure or long-day treatments compared to shading or short-day treatments. These data indicate that red color formation in cultivars with leaves that are naturally red requires a suitable photoperiod and light intensity; high light intensity or long-day conditions activate anthocyanin biosynthesis-related genes, leading to anthocyanin accumulation. Our results also indicate that the regulation of anthocyanin biosynthetic metabolism in response to light conditions differs between red-leafed and green-leafed cultivars. Taken together, our data reveal that photoperiod and light intensity are important in the regulation of pigmentation and anthocyanin accumulation in crabapple leaves and calli. Moreover, we provide a useful approach for studying and inducing the production of flavonoids by crabapple callus culture under certain photoperiods.

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
Fig. 7

Similar content being viewed by others

Abbreviations

PAL:

Phenylalanine ammonia lyase

CHS:

Chalcone synthase

CHI:

Chalcone isomerase

F3H:

Flavanone 3β-hydroxylase

F3′H:

Flavonoid 3′-monooxygenase

DFR:

Dihydroflavonol 4-reductase

ANS:

Anthocyanidin synthase

UFGT:

Uridine diphosphate (UDP)-glucoseflavonoid 3-O-glycosyltransferase

FLS:

Flavonol synthase

References

  • AbouZid S (2014) Yield improvement strategies for the production of secondary metabolites in plant tissue culture: silymarin from Silybum marianum tissue culture. Nat Prod Res 20:1–9. doi:10.1080/14786419.2014.927465

    Google Scholar 

  • Albert NW, Lewis DH, Zhang H, Irving LJ, Jameson PE et al (2009) Light-induced vegetative anthocyanin pigmentation in Petunia. J Exp Bot 60:2191–2202

    Article  PubMed Central  CAS  PubMed  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

    Article  CAS  PubMed  Google Scholar 

  • Ban Y, Honda C, Hatsuyama Y, Igarashi M, Bessho H et al (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

    Article  CAS  PubMed  Google Scholar 

  • Beckwith AG, Zhang Y, Seeram NP, Cameron AC, Nair MG (2004) Relationship of light quantity and anthocyanin production in Pennisetum setaceum Cvs. Rubrum and Red riding hood. J Agric Food Chem 52:456–461

    Article  CAS  PubMed  Google Scholar 

  • Bourgaud F, Gravot A, Milesi S, Gontier E (2001) Production of plant secondary metabolites: a historical perspective. Plant Sci 161:839–851

    Article  CAS  Google Scholar 

  • Carvalho IS, Cavaco T, Carvalho LM, Duque P (2010) Effect of photoperiod on flavonoid pathway activity in sweet potato (Ipomoea batatas (L.) Lam.) leaves. Food Chem 118:384–390

    Article  CAS  Google Scholar 

  • Chalker-Scott L, Scott JD (2004) Elevated ultraviolet-B radiation induces cross-protection to cold in leaves of rhododendron under field conditions. Photochem Photobiol 79:199–204

    Article  CAS  PubMed  Google Scholar 

  • Chattopadhyay S, Ang LH, Puente P, Deng XW, Wei N (1998) Arabidopsis bZIP protein HY5 directly interacts with light-responsive promoters in mediating light control of gene expression. Plant Cell 10:673–683

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dixon RA, Paiva NL (1995) Stress-induced phenylpropanoid metabolism. Plant Cell 7:1085–1097

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dong YH, Beuning L, Davies K, Mitra D, Morris B et al (1998) Expression of pigmentation genes and photo-regulation of anthocyanin biosynthesis in developing Royal Gala apple flowers. Funct Plant Biol 25:245–252

    CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Espley RV, Hellens RP, Putterill J, Stevenson DE, Kutty-Amma S et al (2007) Red coloration in apple fruit is due to the activity of the MYB transcription factor, MdMYB10. Plant J 49:414–427

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Grotewold E (2006) The genetics and biochemistry of floral pigments. Annu Rev Plant Biol 57:761–780

    Article  CAS  PubMed  Google Scholar 

  • Hong GJ, Hu WL, Li JX, Chen XY, Wang LJ (2009) Increased accumulation of artemisinin and anthocyanins in Artemisia annua expressing the Arabidopsis blue light receptor CRY1. Plant Mol Biol Rep 27:334–341

    Article  CAS  Google Scholar 

  • Huang C, Yu B, Teng Y, Su J, Shu Q et al (2009) Effects of fruit bagging on coloring and related physiology, and qualities of red Chinese sand pears during fruit maturation. Sci Hort 121:149–158

    Article  Google Scholar 

  • Ikeuchi M, Sugimoto K, Iwase A (2013) Plant callus: mechanisms of induction and repression. Plant Cell 25:3159–3173

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jaakola L, Hohtola A (2010) Effect of latitude on flavonoid biosynthesis in plants. Plant Cell Environ 33:1239–1247

    CAS  PubMed  Google Scholar 

  • Jiang R, Tian J, Song T, Zhang J, Yao Y (2014) The malus crabapple transcription factor McMYB10 regulates anthocyanin biosynthesis during petal coloration. Sci Hort 166:42–49

    Article  CAS  Google Scholar 

  • Ju Z, Liu C, Yuan Y, Wang Y, Liu G (1999) Coloration potential, anthocyanin accumulation, and enzyme activity in fruit of commercial apple cultivars and their F1 progeny. Sci Hort 79:39–50

    Article  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 10:236–242

    Article  CAS  PubMed  Google Scholar 

  • Li S (2014) Transcriptional control of flavonoid biosynthesis: fine-tuning of the MYB-bHLH-WD40 (MBW) complex. Plant Signal Behav. doi:10.4161/psb.27522

    Google Scholar 

  • Li J, Ou-Lee TM, Raba R, Amundson RG, Last RL (1993) Arabidopsis flavonoid mutants are hypersensitive to UV-B irradiation. Plant Cell 5:171–179

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Li YY, Mao K, Zhao C, Zhao XY, Zhang HL et al (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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Liu XF, Yin XR, Allan AC, Lin-Wang K, Shi YN et al (2013) The role of MrbHLH1 and MrMYB1 in regulating anthocyanin biosynthetic genes in tobacco and Chinese bayberry (Myrica rubra) during anthocyanin biosynthesis. Plant Cell Tissue Organ Cult 115:285–298

    Article  CAS  Google Scholar 

  • Maier A, Schrader A, Kokkelink L, Falke C, Welter B et al (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 74:638–651

    Article  CAS  PubMed  Google Scholar 

  • Matus JT, Loyola R, Vega A, Peña-Neira A, Bordeu E et al (2009) Post-veraison sunlight exposure induces MYB-mediated transcriptional regulation of anthocyanin and flavonol synthesis in berry skins of Vitis vinifera. J Exp Bot 60:853–867

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Medina-Puche L, Cumplido-Laso G, Amil-Ruiz F, Hoffmann T, Ring L et al (2014) MYB10 plays a major role in the regulation of flavonoid/phenylpropanoid metabolism during ripening of Fragaria x ananassa fruits. J Exp Bot 65:401–417

    Article  CAS  PubMed  Google Scholar 

  • Middleton EM, Teramura AH (1993) The role of flavonol glycosides and carotenoids in protecting soybean from ultraviolet-B damage. Plant Physiol 103:741–752

    PubMed Central  CAS  PubMed  Google Scholar 

  • Nguyen P, Cin VD (2009) The role of light on foliage colour development in coleus (Solenostemon scutellarioides (L.) Codd). Plant Physiol Biochem 47:934–945

    Article  CAS  PubMed  Google Scholar 

  • Overbeck V, Schmitz-Eiberger MA, Blanke MM (2013) Reflective mulch enhances ripening and health compounds in apple fruit. J Sci Food Agric 93:2575–2579

    Article  CAS  PubMed  Google Scholar 

  • Reyes LF, Miller JC, Cisneros-Zevallos L (2004) Environmental conditions influence the content and yield of anthocyanins and total phenolics in purple- and red-flesh potatoes during tuber development. Am J Pot Res 81:187–193

    Article  CAS  Google Scholar 

  • Rowan DD, Cao M, Lin-Wang K, Cooney JM, Jensen DJ et al (2009) Environmental regulation of leaf colour in red 35S:PAP1 Arabidopsis thaliana. New Phytol 182:102–115

    Article  CAS  PubMed  Google Scholar 

  • Sassi M, Lu Y, Zhang Y, Wang J, Dhonukshe P et al (2012) COP1 mediates the coordination of root and shoot growth by light through modulation of PIN1- and PIN2-dependent auxin transport in Arabidopsis. Development 139:3402–3412

    Article  CAS  PubMed  Google Scholar 

  • Schäfer E, Nagy F (2006) Historical overwiew. In: Nagy F, Schäfer E (eds) Photomorphogenesis in plants and bacteria. Springer, Dordrecht, pp 1–12

    Chapter  Google Scholar 

  • Seeram NP, Cichewicz RH, Chandra A, Nair MG (2003) Cyclooxygenase inhibitory and antioxidant compounds from crabapple fruits. J Agric Food Chem 51:1948–1951

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Simoes C, Brasil Bizarri CH, da Silva Cordeiro L, Carvalho de Castro T, Machado Coutada LC et al (2009) Anthocyanin production in callus cultures of cleome rosea: modulation by culture conditions and characterization of pigments by means of HPLC-DAD/ESIMS. Plant Physiol Bochem 47:895–903

    Article  CAS  Google Scholar 

  • Takos AM, Jaffé FW, Jacob SR, Bogs J, Robinson SP et al (2006) Light-induced expression of a MYB gene regulates anthocyanin biosynthesis in red apples. Plant Physiol 142:1216–1232

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tanaka Y, Ohmiya A (2008) Seeing is believing: engineering anthocyanin and carotenoid biosynthetic pathways. Curr Opin Biotechnol 19:190–197

    Article  CAS  PubMed  Google Scholar 

  • Tattini M, Landi M, Brunetti C, Giordano C, Remorini D et al (2014) Epidermal coumaroyl anthocyanins protect sweet basil against excess light stress: multiple consequences of light attenuation. Physiol Plant. doi:10.1111/ppl.12201

    PubMed  Google Scholar 

  • Taylor AO (1965) Some effects of photoperiod on the biosynthesis of Phenylpropane derivatives in Xanthium. Plant Physiol 40:273–280

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wang Y, Gao L, Shan Y, Liu Y, Tian Y et al (2012) Influence of shade on flavonoid biosynthesis in tea (Camellia sinensis (L.) O Kuntze). Sci Hort 141:7–16

    Article  CAS  Google Scholar 

  • Wei X, Zhao R, Sun YH, Cong JP, Meng FG et al (2009) The leaf extract of Siberian crabapple (Malus baccata (Linn.) Borkh) contains potential fatty acid synthase inhibitors. J Enzyme Inhib Med Chem 24:234–240

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Xu F, Cao S, Shi L, Chen W, Su X et al (2014a) Blue light irradiation affects anthocyanin content and enzyme activities involved in postharvest strawberry fruit. J Agric Food Chem 62:4778–4783

    Article  CAS  PubMed  Google Scholar 

  • Xu Q, Yin XR, Zeng JK, Ge H, Song M et al (2014b) Activator- and repressor-type MYB transcription factors are involved in chilling injury induced flesh lignification in loquat via their interactions with the phenylpropanoid pathway. J Exp Bot 65:4349–4359

    Article  PubMed Central  PubMed  Google Scholar 

  • Yi C, Deng XW (2005) COP1 - from plant photomorphogenesis to mammalian tumorigenesis. Trends Cell Biol 15:618–625

    Article  CAS  PubMed  Google Scholar 

  • Yompakdee C, Thunyaharn S, Phaechamud T (2012) Bactericidal activity of methanol extracts of crabapple mangrove tree (Sonneratia caseolaris Linn.) against Multi-drug resistant pathogens. Indian J Pharm Sci 74:230–236

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhang Y, Zhang J, Song T, Li J, Tian J et al (2014) Low medium pH value enhances anthocyanin accumulation in malus crabapple leaves. PLoS One 9:e97904. doi:10.1371/journal.pone.0097904

    Article  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

We thank the Fruit Tree Key Laboratory at the Beijing University of Agriculture (BUA) for providing basic laboratory equipments. We are grateful to all of the technicians at the BUA Crabapple Germplasm Resource Garden. Financial support was provided by the National Natural Science Foundation of China (Nos. 31071785 and 31200213), the Funding Project for Academic Human Resources Development in Institutions of Higher Learning under the Jurisdiction of Beijing Municipality (PHR20110515), and the Scientific Research Foundation for Selected Overseas Chinese Scholars, Beijing Human Resources and Social Security Bureau.

Conflict of interest

We declare no conflicts of interest.

Author information

Author notes

    Authors and Affiliations

    1. Plant Science and Technology College, Beijing University of Agriculture, Beijing, 102206, China

      Yanfen Lu, Meiling Zhang, Xiaona Meng, Huihua Wan, Jie Zhang, Ji Tian, Suxiao Hao, Kaina Jin & Yuncong Yao

    2. Beijing Key Laboratory of New Technology in Agriculture Application, Beijing University of Agriculture, Beijing, 102206, China

      Yanfen Lu, Meiling Zhang, Xiaona Meng, Huihua Wan, Jie Zhang, Ji Tian, Suxiao Hao, Kaina Jin & Yuncong Yao

    Authors
    1. Yanfen Lu
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Meiling Zhang
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Xiaona Meng
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Huihua Wan
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. Jie Zhang
      View author publications

      You can also search for this author in PubMed Google Scholar

    6. Ji Tian
      View author publications

      You can also search for this author in PubMed Google Scholar

    7. Suxiao Hao
      View author publications

      You can also search for this author in PubMed Google Scholar

    8. Kaina Jin
      View author publications

      You can also search for this author in PubMed Google Scholar

    9. Yuncong Yao
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding author

    Correspondence to Yuncong Yao.

    Additional information

    Yanfen Lu, Meiling Zhang and Xiaona Meng have contributed equally to this work.

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Lu, Y., Zhang, M., Meng, X. et al. Photoperiod and shading regulate coloration and anthocyanin accumulation in the leaves of malus crabapples. Plant Cell Tiss Organ Cult 121, 619–632 (2015). https://doi.org/10.1007/s11240-015-0733-3

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s11240-015-0733-3

    Keywords

    Search

    Navigation