Skip to main content
SpringerLink
Log in

The antioxidative role of anthocyanins in Arabidopsis under high-irradiance

  • Published:
Biologia Plantarum

Abstract

To uncover the potential antioxidative role of anthocyanins in vivo in protecting photosynthetic tissues from photoinhibition, the effects of high irradiance [HI, 1300 μmol(photon) m−2 s−1] were studied using detached leaves derived from Arabidopsis wild-type (WT) and the mutant deficient in anthocyanin biosynthesis (tt3tt4). HI stress caused decreased chlorophyll content and photochemical efficiency, but increased cell-membrane leakage and contents of hydrogen peroxide and superoxide radical in the leaves of both Arabidopsis phenotypes, but the WT plants showed better HI tolerance than tt3tt4 mutant. HI caused a significant increase in the 1,1-diphenyl-2-picrylhydrazyl scavenging capacity in WT but not in the tt3tt4 mutant. The anthocyanins could not contribute substantially to light-shielding during the periods of HI stress, because the anthocyanin content in WT was very low and the colour of leaves was the same as in the tt3tt4 mutant. Thus, it was assumed that the better HI tolerance in WT was mostly related to the potential antioxidative role of anthocyanins.

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

Similar content being viewed by others

Abbreviations

OH· :

hydroxyl radical

CHS:

chalcone synthase

DAB:

diaminobenzidine

DFR:

dihydroflavono-4-reductase

DPPH:

1,1-diphenyl-2-picrylhydrazyl

ETR:

apparent electron transport rate

Fv/Fm :

variable to maximum fluorescence ratio (the maximum photosystem 2 quantum yield)

NBT:

nitroblue tetrazolium

\({{\rm{O}}_2}{ \cdot ^ - }\) :

superoxide radical

qP:

the coefficient of photochemical quenching

ROS:

reactive oxygen species

tt3tt4 :

tt3tt4 mutant deficient in anthocyanin biosynthesis

WT:

wild-type

ΦPS2 :

effective photosystem 2 quantum yield

References

  • Aarti, D., Tanaka, R., Ito, H., Tanaka, A.: High light inhibits chlorophyll biosynthesis at the level of 5-aminolevulinate synthesis during de-etiolation in cucumber (Cucumis sativus) cotyledons. — Photochem. Photobiol. 83: 171–176, 2007.

    Article  PubMed  CAS  Google Scholar 

  • Agati, G., Meyer S., Matteini P., Cerovic Z.G.: Assessment of anthocyanins in grape (Vitis vinifera L.) berries using a noninvasive chlorophyll fluorescence method. — J. Agr. Food Chem. 55: 1053–1061, 2007.

    Article  CAS  Google Scholar 

  • Albert, N.W., Lewis, D.H., Irving, L.J., Jameson, P.E., Davies, K.M.: Light-induced vegetative anthocyanin pigmentation in Petunia. — J. exp. Bot. 60: 2191–2202, 2009.

    Article  PubMed  CAS  Google Scholar 

  • Archetti, M., Döring, T.F., Hagen, S.B., Hughes, N.M., Leather, S.R., Lee, D.W., Lev-Yadun, S., Manetas, Y., Ougham, H.J., Schaberg, P.G., Thomas, H.: Unravelling the evolution of autumn colours: an interdisciplinary approach. — Trends Ecol. Evol. 24: 166–173, 2009.

    Article  PubMed  Google Scholar 

  • Aro, E.M., Virgin, I., Andersson, B.: Photoinhibition of photosystem II: Inactivation, protein damage and turnover. — Biochim. biophys. Acta 1143: 113–134, 1993.

    Article  PubMed  CAS  Google Scholar 

  • Beggs, C.J., Wellmann, E.: Photocontrol of flavonoid biosynthesis. — In: Kendrick, R.E., Kronenberg, G.H.M. (ed.): Photomorphogenesis in Plants. 2nd Ed. Pp. 733–750. Kluwer Academic Press, Dordrecht - Boston - London 1994.

    Chapter  Google Scholar 

  • Chalker-Scott, L.: Environmental significance of anthocyanins in plant stress responses. — Photochem. Photobiol. 70: 1–9, 1999.

    Article  CAS  Google Scholar 

  • Christie, P.J., Alfenito, M.R., Walbot, V.: Impact of low-temperature stress on general phenylpropanoid and anthocyanin pathways: enhancement of transcript abundance and anthocyanin pigmentation in maize. — Planta 194: 541–549, 1994.

    Article  CAS  Google Scholar 

  • Close, D.C., Davies, N.W., Beadle, C.L.: Temporal variation of tannins (galloylglucoses), flavonols and anthocyanins in leaves of Eucalyptus nitens seedlings: implications for light attenuation and antioxidant activities. — Aust. J. P1ant Physiol. 28: 1–10, 2001.

    Google Scholar 

  • De Jong, H.: Inheritance of anthocyanin pigmentation in the cultivated potato: a critical review. — Amer. J. Potato Res. 68: 585–593, 1991.

    Article  Google Scholar 

  • Ding, W., Song, L., Wang, X., Bi, Y.: Effect of abscisic acid on heat stress tolerance in the calli from two ecotypes of Phragmites communis. — Biol. Plant. 54: 607–613, 2010.

    Article  CAS  Google Scholar 

  • Dixon, R.A., Paiva, N.L.: Stress-induced phenylpropanoid metabolism. — Plant Cell 7: 1085–1097, 1995.

    Article  PubMed  CAS  Google Scholar 

  • Field, T., Lee, D., Holbrook, N.: Why leaves turn red in autumn. The role of anthocyanins in senescing leaves of red-osier dogwood. — Plant Physiol. 127: 556–574, 2001.

    Google Scholar 

  • Fukumoto, L.R., Mazza, G.: Assessing antioxidant and prooxidant activities of phenolic compounds. — J. Agr. Food Chem. 48: 3597–3604, 2000.

    Article  CAS  Google Scholar 

  • Garcia-Alonso, M., Rimbach, G., Sasai, M., Nakahara, M., Matsugo, S., Uchida, Y., Rivas-Gonzalo, J.C., De Pascual-Teresa, S.: Electron spin resonance spectroscopy studies on the free radical scavenging activity of wine anthocyanins and pyranoanthocyanins. — Mol. Nutr. Food Res. 49: 1112–1119, 2005.

    Article  PubMed  CAS  Google Scholar 

  • Gould, K.S., Kuhn, D.N., Lee, D.W., Oberbauer, S.F.: Why leaves are sometimes red. — Nature 378: 241–242, 1995.

    Article  CAS  Google Scholar 

  • Gould, K.S., Lister, C.: Flavonoid functions in plants. — In: Andersen, O.M., Markham, K.R. (ed.): Flavonoids: Chemistry, Biochemistry and Applications. Pp. 397–411. CRC Press, Boca Raton 2006.

    Google Scholar 

  • Gould, K.S., McKelvie, J., Markham, K.R.: Do anthocyanins function as antioxidants in leaves: imaging of H2O2 in red and green leaves after mechanical injury. — Plant Cell Environ. 25: 1261–1269, 2002a.

    Article  CAS  Google Scholar 

  • Gould, K.S., Vogelmann, T.C., Han, T., Clearwater, M.J.: Profiles of photosynthesis within red and green leaves of Quintinia serrata A. — Cunn. Physiol. Plant. 116: 127–133, 2002b.

    Article  CAS  Google Scholar 

  • Havaux, M., Niyogi, K.K.: The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism. — Proc. nat. Acad. Sci. USA 96: 8762–8767, 1999.

    Article  PubMed  CAS  Google Scholar 

  • Hidema, J., Makino, A., Kurita, Y., Mae, T., Ojima, K.: Changes in the levels of chlorophyll and light-harvesting chlorophyll a/b protein of PSII in rice leaves aged under different irradiances from full expansion through senescence. — Plant Cell Physiol. 33: 1209–1214, 1992.

    CAS  Google Scholar 

  • Hoch, W.A., Zeldin, E.L., McCown, B.H.: Physiological significance of anthocyanins during autumnal leaf senescence. — Tree Physiol. 21: 1–8, 2001.

    Article  PubMed  CAS  Google Scholar 

  • Huner, N.P.A., Öquist, G., Sarhan, F.: Energy balance and acclimation to light and cold. — Trends Plant Sci. 3: 224–230, 1998.

    Article  Google Scholar 

  • Hutzler, P., Fischbach, R., Heller, W., Jungblut, T.P., Reuber, S., Schmitz, R., Veit, M., Weissenbock, G., Schnitzler, J.P.: Tissue location of phenolic compounds in plants by confocal laser scanning microscopy. — J. exp. Bot. 49: 953–965, 1998.

    Article  CAS  Google Scholar 

  • Ismail, G.S.M., Mohamed, H.E.: Alteration in growth and thylakoid membrane lipid composition of Azolla caroliniana under phosphate deficiency. — Biol. Plant. 54: 671–676, 2010.

    Article  CAS  Google Scholar 

  • Lee, D.W., Collins, T.M.: Phylogenetic and ontogenetic influences on the distribution of anthocyanins and betacyanins in leaves of tropical plants. — Int. J. Plant Sci. 162: 1141–1153, 2001.

    Article  CAS  Google Scholar 

  • Lichtenthaler, H.K., Wellburn, A.R.: Determinations of total carotenoids and chlorophyll a and b in leaf extracts of different solvents. — Biochem. Soc. Trans. 603: 591–592, 1983.

    Google Scholar 

  • Lu, X., Zhou, W., Gao, F.: Chromosomal location of 45S rDNA and dfr gene in Citrus sinensis. — Biol. Plant. 54: 798–800, 2010.

    Article  CAS  Google Scholar 

  • Luo, Y., Li, F., Wang, G.P., Yang, X.H., Wang, W.: Exogenously-supplied trehalose protects thylakoid membranes of winter wheat from heat-induced damage. — Biol. Plant. 54: 495–501, 2010.

    Article  CAS  Google Scholar 

  • Manetas, Y.: Why some leaves are anthocyanic and why most anthocyanic leaves are red. — Flora 201: 163–177, 2006.

    Article  Google Scholar 

  • Manetas, Y., Petropoulou, Y., Psaras, G.K., Drinia, A.: Exposed red (anthocyanic) leaves of Quercus coccifera display shade characteristics. — Funct. Plant Biol. 30: 265–270, 2003.

    Article  CAS  Google Scholar 

  • Meng, X.C., Xing, T., Wang, X.J.: The role of light in the regulation of anthocyanin accumulation in Gerbera hybrida. — Plant Growth Regul. 44: 243–250, 2004.

    Article  CAS  Google Scholar 

  • Merzlyak, M.N., Chivkunova, O.B., Solovchenko, A.E., Naqvi, K.R.: Light absorption by anthocyanin in juvenile, stressed, and senescing leaves. — J. exp. Bot. 59: 3903–3911, 2008.

    Article  PubMed  CAS  Google Scholar 

  • Neil, S., Gould, K.S., Kilmartin, P.A., Mitchell, K.A., Markham, K.R.: Antioxidant activities of red versus green leaves in Elatostema rugosum. — Plant Cell Environ. 25: 539–547, 2002.

    Article  Google Scholar 

  • Neill, S.O., Gould, K.S.: Anthocyanins in leaves: light attenuators or antioxidant. — Funct Plant Biol. 30: 865–873, 2003.

    Article  CAS  Google Scholar 

  • Okada, K., Inoue, Y., Satoh, K., Katoh, S.: Effects of light on degradation of chlorophyll and proteins during senescence of detached rice leaves. — Plant Cell Physiol. 33: 1183–1191, 1992.

    CAS  Google Scholar 

  • Peer, W.A., Brown, D.E., Tague, B.W.: Flavonoid accumulation patterns of transparent testa mutants of Arabidopsis. — Plant Physiol. 126: 536–548, 2001.

    Article  PubMed  CAS  Google Scholar 

  • Peng, C.L., Chen, S.W., Lin, Z.F., Lin, G.Z.: [Detection of antioxidative capacity in plants by scavenging organic free radical DPPH.] — Progr. Biochem. Biophys. 27: 658–661, 2000. [In Chin.]

    CAS  Google Scholar 

  • Peng, C.L., Lin, Z.F., Lin, G.Z., Chen, S.W.: The anti-photooxidation of anthocyanin-rice leaves of a purple rice cultivar. — Sci. China Ser. C 49: 543–551, 2006.

    Article  CAS  Google Scholar 

  • Pietrini, F., Massaeei, A: Leaf anthocyanin content changes in Zea mays L. grown at low temperature: significance for the relationship between quantum yield of PS II and the apparent quantum yield of CO2 assimilation. — Photosynth. Res. 58: 213–219, 1998.

    Article  CAS  Google Scholar 

  • Piovan, A., Filippini, R.: Anthocyanins in Catharanthus roseus in vivo and in vitro: a review. — Phytochem. Rev. 6: 235–242, 2007.

    Article  CAS  Google Scholar 

  • Rascher, U., Hütt, M.T., Siebke, K., Osmond, B., Beck, F., Lüttge, U.: Spatio-temporal variation of metabolism in a plant circadian rhythm: the biological clock as an assembly of coupled individual oscillators. — Proc. nat. Acad. Sci. USA 98: 11801–11805, 2001.

    Article  PubMed  CAS  Google Scholar 

  • Romero-Puertas, M.C., Rodriguez-Serrano, M., Corpas, F.J., Gómez, M., Delrío, L.A., Sandalio, L.M.: Cadmium-induced subcellular accumulation of {ie104-1} and H2O2 in pea leaves. — Plant Cell Environ. 27: 1122–1134, 2004.

    Article  CAS  Google Scholar 

  • Saunders, J.A., McClure, J.W.: Distribution of flavonoids in chloroplasts of 25 species of vascular plants. — Phytochemistry 15: 809–810, 1976.

    Article  CAS  Google Scholar 

  • Schreiber, U., Gademann, R., Ralph, P.J., Larkum, A.W.D.: Assessment of photosynthetic performance of prochloron in Lissoclinum patella by in situ and in hospite chlorophyll fluorescence measurements. — Plant Cell Physiol. 38: 945–951, 1997.

    CAS  Google Scholar 

  • Shao, L., Shu, Z., Sun, S.L., Peng, C.L., Lin, Z.F., Yang, C.W.: Enhanced sensitivity of Arabidopsis anthocyanin mutants to photooxidation: a study with fluorescence imaging. — Funct. Plant Biol. 35: 714–724, 2008.

    Article  CAS  Google Scholar 

  • Shirley, B.W., Qubasek, W.L., Storz, G., Bruggemann, E., Koornneef, M., Ausubel, F.M., Goodman, H.M.: Analysis of Arabidopsis mutants deficient in flavonoid biosynthesis. — Plant J. 8: 659–671, 1995.

    Article  PubMed  CAS  Google Scholar 

  • Siebke, K., Weis, E.: Assimilation images of leaves of Glechoma hederacea: analysis of nonsynchronous stomata related oscillations. — Planta 196: 155–165, 1995.

    Article  CAS  Google Scholar 

  • Smillie, R.M., Hetherington, S.E.: Photoabatement by anthocyanin shields photosynthetic systems from light stress. — Photosynthetica 36: 451–463, 1999.

    Article  CAS  Google Scholar 

  • Steyn, W.J., Wand, S.J.E., Holcroft, D.M., Jacobs, G.: Anthocyanins in vegetative tissues: a proposed unified function in photoprotection. — New Phytol. 155: 349–361, 2002.

    Article  CAS  Google Scholar 

  • Takahashi, M.A., Asada, K.: Superoxide anion permeability of phospholipid-membranes and chloroplast thylacoids. — Arch. Biochem. Biophys. 226: 558–566, 1983.

    Article  PubMed  CAS  Google Scholar 

  • Tsuda, T., Shiga, K., Ohshima, K.: Inhibition of lipid peroxidation and the active oxygen radical scavenging effect of anthocyanin pigment isolated from Phaseolus vulgaris L. — Biochem. Pharmacol. 52: 1033–1039, 1996.

    Article  PubMed  CAS  Google Scholar 

  • Wade, H.K., Sohal, A.K., Jenkins, G.I.: Arabidopsis ICX1 is a negative regulator of several pathways regulating flavonoid biosynthesis genes. — Plant Physiol. 131: 707–715, 2003.

    Article  PubMed  CAS  Google Scholar 

  • Wang, H., Cao, G.H., Prior, R.L.: Oxygen radical absorbing capacity of anthocyanins. — J. Agr. Food Chem. 45: 304–309, 1997.

    Article  CAS  Google Scholar 

  • Yamasaki, H., Sakihama, Y., Ikehara, N.: Flavonoid-peroxidase reaction as a detoxification mechanism of plant cells against H2O2. — Plant Physiol. 115: 1405–1512, 1997.

    PubMed  CAS  Google Scholar 

  • Zeng, X.Q., Chow, W.S., Su, L.J., Peng, X.X., Peng, C.L.: Protective effect of supplemental anthocyanins on Arabidopsis leaves under high light. — Physiol. Plant. 138: 215–225, 2010.

    Article  PubMed  CAS  Google Scholar 

  • Zhao, B.L.: [Oxygen free radicals and natural antioxidants]. — Science Press, Beijing 1999. [In Chin.]

    Google Scholar 

  • Zuluaga, D.L., Gonzali, S., Loreti, E., Pucciariello, C., Degl’Innocenti, E., Guidi, L., Alpi, A., Perata, P.: Arabidopsis thaliana MYB75/PAP1 transcription factor induces anthocyanin production in transgenic tomato plants. — Funct. Plant Biol. 35: 606–618, 2008.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Prof. Wah Soon Chow from the Australian National University for his useful suggestions on the manuscript. This research is financially supported by National Natural Science Foundation of China (30770173, 30870385), The State Key Basic Research and Development Plan of China (973 Program; 2009CB118504). The first two authors contributed equally to this work

Author information

Authors and Affiliations

  1. College of Life Science, South China Normal University, Guangzhou, 510631, Guangdong, P.R. China

    Q. Zhang, L. -J. Su, X. -Q. Zeng, B. -Y. Sun & C. -L. Peng

  2. College of Agronomy and Biotechnology, Yunnan Agricultural University, Kunming, 650201, Yunnan, P.R. China

    J. -W. Chen

Authors
  1. Q. Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. L. -J. Su
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. -W. Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. X. -Q. Zeng
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. B. -Y. Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. C. -L. Peng
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to C. -L. Peng.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhang, Q., Su, L.J., Chen, J.W. et al. The antioxidative role of anthocyanins in Arabidopsis under high-irradiance. Biol Plant 56, 97–104 (2012). https://doi.org/10.1007/s10535-012-0022-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10535-012-0022-5

Additional key words

Search

Navigation