, Volume 56, Issue 1, pp 445–454 | Cite as

Anthocyanins function as a light attenuator to compensate for insufficient photoprotection mediated by nonphotochemical quenching in young leaves of Acmena acuminatissima in winter

  • H. Zhu
  • T.-J. Zhang
  • J. Zheng
  • X.-D. Huang
  • Z.-C. Yu
  • C.-L. Peng
  • W. S. Chow


Anthocyanins and nonphotochemical quenching (NPQ) are two important tools that provide photoprotection in plant leaves. In order to understand how plants use these tools for acclimation to changing seasonal conditions, we investigated pigments, antioxidative capacity, and photosynthesis in leaves of an evergreen tree (Acmena acuminatissima) in two contrasting seasons. Young leaves of A. acuminatissima appeared in distinct colors, being light green in summer and red in winter due to the presence of anthocyanins. In the winter young leaves, anthocyanins contributed less than 2% to the antioxidant pool. In the summer, young leaves had higher NPQ than that of mature leaves, but in the winter, they did not derive any NPQ-related advantage over mature leaves. These results suggest that the accumulation of anthocyanins in young leaves in the winter may compensate for the insufficient photoprotection afforded by NPQ and that anthocyanins function as a light attenuator to protect the photochemical apparatus against excess light.

Additional key words

chlorophyll fluorescence evergreen tree gas exchange photoprotection pigment season 



intercellular CO2 concentration








transpiration rate


electron transport rate


maximum photochemical efficiency of PSII


stomatal conductance


mature leaves


nonphotochemical quenching


net light-saturated photosynthetic rate


effective photochemical efficiency of PSII


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  1. Ainsworth E.A., Gillespie K.M.: Estimation of total phenolic content and other oxidation substrates in plant tissues using Folin–Ciocalteu reagent.–Nat. Protoc. 2: 875–877, 2007.CrossRefPubMedGoogle Scholar
  2. Albert N.W., Lewis D.H., Zhang H. et al.: Light-induced vegetative anthocyanin pigmentation in petunia.–J. Exp. Bot. 60: 2191–2202, 2009.CrossRefPubMedPubMedCentralGoogle Scholar
  3. Bilger W., Björkman O.: Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis.–Photosynth. Res. 25: 173–185, 19CrossRefPubMedGoogle Scholar
  4. Bradford M.M.: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.–Anal. Biochem. 72: 248–254, 1976.CrossRefPubMedGoogle Scholar
  5. Feild T.S., Lee D.W., Holbrook N.M.: Why leaves turn red in autumn. The role of anthocyanins in senescing leaves of redosier dogwood.–Plant Physiol. 127: 566–574, 2001.CrossRefPubMedPubMedCentralGoogle Scholar
  6. Genty B., Briantais J.M., Baker N.R.: The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence.–Biochim. Biophys. Acta 990: 87–92 1989.CrossRefGoogle Scholar
  7. Gould K.S., Kuhn D.N., Lee D.W. et al.: Why leaves are sometimes red.–Nature 378: 241–242, 1995.CrossRefGoogle Scholar
  8. Gould K.S., Markham K.R., Smith R.H. et al.: Functional role of anthocyanins in the leaves of Quintinia serrata A. Cunn.–J. Exp. Bot. 51: 1107–1115, 2000.CrossRefPubMedGoogle Scholar
  9. Guo Y.-H., Cao K.-F.: Effect of night chilling on photosynthesis of two coffee species grown under different irradiances.–J. Hortic. Sci. Biotech. 79: 713–716, 2004.CrossRefGoogle Scholar
  10. Hakala M., Tuominen I., Keränen M. et al.: Evidence for the role of the oxygen-evolving manganese complex in photoinhibition of photosystem II.–BBA-Bioenergetics 1706: 68–80, 2005.CrossRefPubMedGoogle Scholar
  11. Havaux M., Kloppstech K.: The protective functions of carotenoid and flavonoid pigments against excess visible radiation at chilling temperature investigated in Arabidopsis npq and tt mutants.–Planta 213: 953–966, 2001.CrossRefGoogle Scholar
  12. He J., Yang W., Qin L. et al. Photoinactivation of photosystem II in wild type and chlorophyll b-less barley leaves: Which mechanism dominates depends on experimental circumstances.–Photosynth. Res. 126: 399–407, 2015.CrossRefPubMedGoogle Scholar
  13. Heimler D., Vignolini P., Dini M.G. et al.: Rapid tests to assess the antioxidant activity of Phaseolus vulgaris L. Dry beans.–J. Agr. Food Chem. 53: 3053–3056, 2005.CrossRefGoogle Scholar
  14. Hendrickson L., Ball M.C., Osmond C.B. et al.: Assessment of photoprotection mechanisms of grapevines at low temperature.–Funct. Plant Biol. 30: 631–642 2003.CrossRefGoogle Scholar
  15. Hipskind J., Wood K., Nicholson R.L.: Localized stimulation of anthocyanin accumulation and delineation of pathogen ingress in maize genetically resistant Tobipolaris maydisrace O.–Physiol. Mol. Plant Pathol. 49: 247–256, 1996.CrossRefGoogle Scholar
  16. Hirotsu N., Makino A., Ushio A. et al.: Changes in the thermal dissipation and the electron flow in the water–water cycle in rice grown under conditions of physiologically low temperature.–Plant Cell Physiol. 45: 635–644, 2004.CrossRefPubMedGoogle Scholar
  17. Hu W., Song X., Shi K. et al.: Changes in electron transport, superoxide dismutase and ascorbate peroxidase isoenzymes in chloroplasts and mitochondria of cucumber leaves as influenced by chilling.–Photosynthetica 46: 581–588, 2008.CrossRefGoogle Scholar
  18. Hughes N.M., Neufeld H.S., Burkey K.O.: Functional role of anthocyanins in high-light winter leaves of the evergreen herb Galax urceolata.–New Phytol. 168: 575–587, 20CrossRefPubMedGoogle Scholar
  19. Hughes N.M., Morley C.B., Smith W.K.: Coordination of anthocyanin decline and photosynthetic maturation in juvenile leaves of three deciduous tree species.–New Phytol. 175: 675–685, 2007.CrossRefPubMedGoogle Scholar
  20. Hughes N.M., Smith W.K.: Attenuation of incident light in Galax urceolata (Diapensiaceae): Concerted influence of adaxial and abaxial anthocyanic layers on photoprotection.–Am. J. Bot. 94: 784–790, 2007.CrossRefPubMedGoogle Scholar
  21. Karageorgou P., Manetas Y.: The importance of being red when young: Anthocyanins and the protection of young leaves of Quercus coccifera from insect herbivory and excess light.–Tree Physiol. 26: 613–621, 2006.CrossRefPubMedGoogle Scholar
  22. Koćcielniak J., Biesaga-Koćcielniak J.: Photosynthesis and nonphotochemical excitation quenching components of chlorophyll excitation in maize and field bean during chilling at different photon flux density.–Photosynthetica 44: 174–180, 2006.CrossRefGoogle Scholar
  23. Krall J.P., Edwards G.E.: Relationship between photosystem II activity and CO2 fixation in leaves.–Physiol. Plantarum 86: 180–187, 1992.CrossRefGoogle Scholar
  24. Kratsch H.A., Wise R.R.: The ultrastructure of chilling stress.–Plant Cell Environ. 23: 337–350, 2000.CrossRefGoogle Scholar
  25. Kumar V., Sharma S.S.: Nutrient deficiency-dependent anthocyanin development in Spirodela polyrhiza L. Schleid.–Biol. Plantarum 42: 621–624, 1999.CrossRefGoogle Scholar
  26. Laine P.L., Bigot J., Ourry A. et al.: napus L.–New Phytol. 127: 675–683, 1994.CrossRefGoogle Scholar
  27. Lea U.S., Slimestad R., Smedvig P. et al: Nitrogen deficiency enhances expression of specific MYB and BHLH transcription factors and accumulation of end products in the flavonoid pathway.–Planta 225: 1245–1253, 2007.CrossRefPubMedGoogle Scholar
  28. Liakopoulos G., Nikolopoulos D., Klouvatou A. et al.: The photoprotective role of epidermal anthocyanins and surface pubescence in young leaves of grapevine (Vitis vinifera).–Ann. Bot.-London 98: 257–265, 2006.CrossRefGoogle Scholar
  29. Liu X., Ardo S., Bunning M. et al.: Total phenolic content and DPPH radical scavenging activity of lettuce (Lactuca sativa L.) grown in Colorado.–LWT-Food Sci. Technol. 40: 552–557, 2007.CrossRefGoogle Scholar
  30. Mai J., Herbette S., Vandame M. et al.: Effect of chilling on photosynthesis and antioxidant enzymes in Hevea brasiliensis Muell. Arg.–Trees 23: 863–874, 2009.CrossRefGoogle Scholar
  31. Mai J., Herbette S., Vandame M. et al.: Contrasting strategies to cope with chilling stress among clones of a tropical tree, Hevea brasiliensis.–Tree Physiol. 30: 1391–1402, 20CrossRefPubMedGoogle Scholar
  32. Müller P., Li X.-P., Niyogi K.K.: Non-photochemical quenching. A response to excess light energy.–Plant Physiol. 125: 1558–1566, 2001.CrossRefPubMedPubMedCentralGoogle Scholar
  33. Müller-Moulé P., Conklin P.L., Niyogi K.K.: Ascorbate deficiency can limit violaxanthin de-epoxidase activity in vivo.–Plant Physiol. 128: 970–977, 20CrossRefPubMedPubMedCentralGoogle Scholar
  34. Neill S.O., Gould K.S., Kilmartin P.A. et al.: Antioxidant activities of red versus green leaves in Elatostema rugosum.–Plant Cell Environ. 25: 539–547 20CrossRefGoogle Scholar
  35. Neill S.O., Gould K.S.: Anthocyanins in leaves: Light attenuators or antioxidants?–Funct. Plant Biol. 30: 865–873, 2003.CrossRefGoogle Scholar
  36. Niyogi K.K.: Photoprotection revisited: Genetic and molecular approaches.–Annu. Rev. Plant Phys. 50: 333–359, 1999.CrossRefGoogle Scholar
  37. Ohnishi N., Allakhverdiev S.I., Takahashi S. et al.: Two-step mechanism of photodamage to photosystem II: Step 1 occurs at the oxygen-evolving complex and step 2 occurs at the photochemical reaction center.–Biochemistry 44: 8494–8499, 2005.CrossRefPubMedGoogle Scholar
  38. Oxborough K., Baker N.R.: Resolving chlorophyll a fluorescence images of photosynthetic efficiency into photochemical and non-photochemical components–calculation of qP and Fv’/Fm’; without measuring Fo’.–Photosynth. Res. 54: 135–142 1997.CrossRefGoogle Scholar
  39. Peng S., Wang B.: Forest succession of Dinghushan, Guangdong, China.–Chin. J. Bot. 7: 75–80, 1994.Google Scholar
  40. Pietrini F., Iannelli M., Massacci A.: Anthocyanin accumulation in the illuminated surface of maize leaves enhances protection from photo-inhibitory risks at low temperature, without further limitation to photosynthesis.–Plant Cell Environ. 25: 1251–1259, 2002.CrossRefGoogle Scholar
  41. Saha M.R, Hasan S.M.R., Akter R. et al.: In vitro free radical scavenging activity of methanol extract of the leaves of Mimusops elengi Linn.–Bangl. J. Vet. Med. 6: 197–202, 2008.Google Scholar
  42. Steyn W.J., Wand S.J., Jacobs G. et al.: Evidence for a photoprotective function of low-temperature-induced anthocyanin accumulation in apple and pear peel.–Physiol. Plantarum 136: 461–472, 2009.CrossRefGoogle Scholar
  43. Tucić B., Vuleta A., Jovanović S.M.: Protective function of foliar anthocyanins: In situ experiments on a sun-exposed population of Iris pumila L. (Iridaceae).–Pol. J. Ecol. 57: 779–783, 2009.Google Scholar
  44. van den Berg A.K., Perkins T.D.: Contribution of anthocyanins to the antioxidant capacity of juvenile and senescing sugar maple (Acer saccharum) leaves.–Funct. Plant Biol. 34: 714–719, 2007.CrossRefGoogle Scholar
  45. Wang L.-Z., Wang L.-M., Xiang H.-T. et al.: Relationship of photosynthetic efficiency and seed-setting rate in two contrasting rice cultivars under chilling stress.–Photosynthetica 54: 581–588, 2016.CrossRefGoogle Scholar
  46. Wellburn A.R.: The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution.–J. Plant Physiol. 144: 307–313, 1994.CrossRefGoogle Scholar
  47. Zeng X.Q., Chow W.S., Su L.J. et al.: Protective effect of supplemental anthocyanins on Arabidopsis leaves under high light.–Physiol. Plantarum 138: 215–225, 2010.CrossRefGoogle Scholar
  48. Zhang K.-M., Yu H.-J., Shi K. et al.: Photoprotective roles of anthocyanins in Begonia semperflorens.–Plant Sci. 179: 202–208, 20CrossRefGoogle Scholar
  49. Zhang Q., Zhang T.-J., Chow W.S. et al.: Photosynthetic characteristics and light energy conversions under different light environments in five tree species occupying dominant status at different stages of subtropical forest succession.–Funct. Plant Biol. 42: 609–619, 2015.CrossRefGoogle Scholar
  50. Zhang T.-J., Chow W.S., Liu X.-T. et al: A magic red coat on the surface of young leaves: Anthocyanins distributed in trichome layer protect Castanopsis fissa leaves from photoinhibition.–Tree Physiol. 36: 1296–1306, 2016.CrossRefPubMedGoogle Scholar

Copyright information

© The Institute of Experimental Botany 2018

Authors and Affiliations

  1. 1.School of Food Engineering and Biology TechnologyHanshan Normal UniversityChaozhou, Guangdong ProvinceChina
  2. 2.Guangzhou Key Laboratory of Subtropical Biodiversity and Biomonitoring, Guangdong Provincial Key Laboratory of Biotechnology for Plant Development, School of Life SciencesSouth China Normal UniversityGuangzhouChina
  3. 3.Division of Plant Sciences, Research School of Biology, College of Medicine, Biology and EnvironmentThe Australian National University, ActonAustralian Capital TerritoryAustralia

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