Skip to main content
SpringerLink
Log in

Foliar anthocyanins in Pelargonium × hortorum are unable to alleviate light stress under photoinhibitory conditions

  • Published:
Photosynthetica

Abstract

Photosynthetic organs are often characterized by anthocyanins being accumulated either in the epidermal or in the mesophyll cells making these tissues to turn reddish-brown in colour. It has been hypothesized that these pigments protect underlying chloroplasts from light-stress because they absorb photons of the photosynthetically active waveband. However, the photoprotective role of anthocyanins has not been undoubtedly shown on a broad range of species. In this study, green and anthocyanic areas of leaves of Pelargonium × hortorum, the latter possessing variable levels of anthocyanins, were compared using pigment analysis and pulse amplitude modulated in vivo chlorophyll (Chl) fluorescence. Quenching analysis of the induction and dark relaxation curves of slow Chl fluorescence kinetics showed that at photoinhibitory conditions [by applying above-saturation light intensity of 1,600 μmol(quantum) m−2 s−1 white light at low (4°C) temperature], anthocyanic areas were at least equally sensitive to photoinhibition as green leaf areas. In fact, the level of photoinhibition tended to be proportional to the level of anthocyanin accumulation suggesting that this characteristic was indicative of the photoinhibitory risk. The results of the present study clearly show that anthocyanins in leaf areas of Pelargonium do not afford a photoprotective advantage.

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

ANOVA :

analysis of variance

Car (x+c):

total carotenoids

Chl(s):

chlorophyll(s)

F:

chlorophyll fluorescence yield

Fo :

minimal fluorescence at the dark-adapted state

Fo′:

minimal fluorescence at the light-adapted state

Fm :

maximal fluorescence at the dark-adapted state

Fm′:

maximal fluorescence at the light-adapted state

Fm″:

maximal fluorescence during the dark relaxation phase

FR:

far-red

Fs :

steady-state level fluorescence

Fv :

variable fluorescence at the dark-adapted state

NPQ:

nonphotochemical quenching

PAM:

pulse amplitude modulated

PAR:

photosynthetically active radiation

PFD:

photon flux density

PSII:

photosystem II

qE :

energy-dependent fluorescence quenching component

qI :

photoinhibitory fluorescence quenching component

qN :

nonphotochemical fluorescence quenching coefficient

qP :

photochemical fluorescence quenching coefficient

qT :

transition state fluorescence quenching component

ΦPSII = ΔF/Fm′:

effective quantum yield of PSII photochemistry

ΦPSIIo = Fv/Fm :

maximum (intrinsic) quantum yield of PSII photochemistry

References

  • Adams, W.W., III, Demmig-Adams, B.: The xanthophyll cycle and sustained thermal energy dissipation activity in Vinca minor and Euonymus kiautschovicus in winter. — Plant Cell Environ. 18: 117–127, 1995.

    Article  Google Scholar 

  • Anderson, J.M.: Photoregulation of the composition, function, and structure of thylakoid membranes. — Ann. Rev. Plant Physiol. 37: 93–136, 1986.

    Article  CAS  Google Scholar 

  • Baker, N.R.: Chlorophyll fluorescence: a probe of photosynthesis in vivo. — Ann. Rev. Plant Biol. 59: 89–113, 2008.

    Article  CAS  Google Scholar 

  • Burger, J., Edwards, G.E.: Photosynthetic efficiency, and photodamage by UV and visible radiation, in red versus green leaf coleus varieties. — Plant Cell Physiol. 37: 395–399, 1996.

    Article  CAS  Google Scholar 

  • Dodd, I.C., Critchley, C., Woodall, G.S., Stewart, G.R.: Photoinhibition in differently coloured juvenile leaves of Syzygium species. — J. Exp. Bot. 49: 1437–1445, 1998.

    CAS  Google Scholar 

  • Döring, T.F., Archetti, M., Hardie, J.: Autumn leaves seen through herbivore eyes. — Proc. R. Soc. B 276: 121–127, 2009.

    Article  PubMed  Google Scholar 

  • Esteban, R., Fernández-Marín, B., Becerril, J.M., García-Plazaola, J.I.: Photoprotective implications of leaf variegation in E. dens-canis L. and P. officinalis L. — J. Plant Physiol. 165: 1255–1263, 2008.

    Article  PubMed  CAS  Google Scholar 

  • Genty, B., Brintais, J.-M., Baker, N.R.: The relationship between the quantum yield of photosyntetic electron transport and quenching of chlorophyll fluorescence. — Biochim. Biophys. Acta 990: 87–92, 1989.

    Article  CAS  Google Scholar 

  • Gould, K.S., Dudle, D.A., Neufeld, H.S.: Why some stems are red: cauline anthocyanins shield photosystem II against high light stress. — J. Exp. Bot. 61: 2707–2717, 2010.

    Article  PubMed  CAS  Google Scholar 

  • Gould, K.S., Neill, S.O., Vogelmann, T.C.: A unified explanation for anthocyanins in leaves? — Adv. Bot. Res. 37: 167–192, 2002a.

    Article  CAS  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, 2002b.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Jadrná, P., Plavcová, O., Kobza, F.: Morphological changes in colchicine-treated Pelargonium × hortorum L.H. Bailey greenhouse plants. — Hortic. Sci. 37: 27–33, 2010.

    Google Scholar 

  • Krause, G.H., Weis, E.: Chlorophyll fluorescence and photosynthesis: the basics. — Ann. Rev. Plant Physiol. Plant Mol. Biol. 42: 313–349, 1991.

    Article  CAS  Google Scholar 

  • Kyparissis, A., Grammatikopoulos, G., Manetas, Y.: Leaf morphological and physiological adjustments to the spectrally selective shade imposed by anthocyanins in Prunus cerasifera. — Tree Physiol. 27: 849–857, 2007.

    Article  PubMed  CAS  Google Scholar 

  • Kytridis, V.-P., Karageorgou, P., Levizou, E., Manetas, Y.: Intra-species variation in transient accumulation of leaf anthocyanins in Cistus creticus during winter: Evidence that anthocyanins may compensate for an inherent photosynthetic and photoprotective inferiority of the red-leaf phenotype. — J. Plant Physiol. 165: 952–959, 2008.

    Article  PubMed  CAS  Google Scholar 

  • Kytridis, V.-P., Manetas, Y.: Mesophyll versus epidermal anthocyanins as potential in vivo antioxidants: evidence linking the putative antioxidant role to the proximity of oxy-radical source. — J. Exp. Bot. 57: 2203–2210, 2006.

    Article  PubMed  CAS  Google Scholar 

  • Liakopoulos, G., Nikolopoulos, D., Klouvatou, A., Vekkos, K.- A., Manetas, Y., Karabourniotis, G.: The photoprotective role of epidermal anthocyanins and surface pubescence in young leaves of grapevine (Vitis vinifera). — Ann. Bot. 98: 257–265, 2006.

    Article  PubMed  CAS  Google Scholar 

  • Lichtenthaler, H.K.: Chlorophylls and carotenoids: Pigments of photosynthetic biomembranes — Methods Enzymol.. 148: 350–382, 1987.

    Article  CAS  Google Scholar 

  • Logan, B.A., Adams, W.W., III, Demmig-Adams, B.: Avoiding common pitfalls of chlorophyll fluorescence analysis under field conditions. — Funct. Plant Biol. 34: 853–859, 2007.

    Article  CAS  Google Scholar 

  • Mancinelli, A.L., Yang, C.-P.H., Lindquist, P., Anderson, O.R., Rabino, I.: Photocontrol of anthocyanin synthesis. III. The action of streptomycin on the synthesis of chlorophyll and anthocyanin. — Plant Physiol. 55: 251–257, 1975.

    Article  PubMed  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 

  • Matsubara, S., Krause, G.H., Aranda, J, et al.: Sun-shade patterns of leaf carotenoid composition in 86 species of neotropical forest plants. — Funct. Plant Biol. 36: 20–36, 2009.

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Neill, S., Gould, K.S.: Optical properties of leaves in relation to anthocyanin concentration and distribution. — Can. J. Bot. 77: 1777–1782, 1999.

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Nielsen, S.L., Simonsen, A.-M.: Photosynthesis and photoinhibition in two differently coloured varieties of Oxalis triangularis — the effect of anthocyanin content. — Photosynthetica 49: 346–352, 2011.

    Article  CAS  Google Scholar 

  • Nikiforou, C., Manetas, Y.: Strength of winter leaf redness as an indicator of stress vulnerable individuals in Pistacia lentiscus. — Flora 205: 424–427, 2010.

    Article  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 

  • Sun, J., Nishio, J.N., Vogelmann, T.C.: Green light drives CO2 fixation deep within leaves. — Plant Cell Physiol. 39: 1020–1026, 1998.

    Article  CAS  Google Scholar 

  • Takahashi, S., Milward, S.E., Yamori, W., Evans, J.R., Hillier, W., Badger, M.R.: The solar action spectrum of photosystem II damage. — Plant Physiol. 153: 988–993, 2010.

    Article  PubMed  CAS  Google Scholar 

  • Terashima, I., Fujita, T., Inoue, T., Chow, W.S., Oguchi, R.: Green light drives leaf photosynthesis more efficiently than red light in strong white light: revisiting the enigmatic question of why leaves are green. — Plant Cell Physiol. 50: 684–697, 2009.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • van den Berg, A.K., Vogelmann, T.C., Perkins, T.D.: Anthocyanin influence on light absorption within juvenile and senescing sugar maple leaves do anthocyanins function as photoprotective visible light screens? — Funct. Plant Biol. 36: 793–800, 2009.

    Article  Google Scholar 

  • van Kooten, O., Snel, J.F.H.: The use of chlorophyll fluorescence nomenclature in plant stress physiology. — Photosynth. Res. 25: 147–150, 1990.

    Article  Google Scholar 

  • van Wijk, K.J., van Hasselt, P.R.: Photoinhibition of photosystem II in vivo is preceded by down-regulation through light-induced acidification of the lumen: Consequences for the mechanism of photoinhibition in vivo. — Planta 189: 359–368, 1993.

    Article  Google Scholar 

  • Walters, R.G., Horton, P.: Resolution of components of nonphotochemical chlorophyll fluorescence quenching in barley leaves. — Photosynth. Res. 27: 121–133, 1991.

    Article  CAS  Google Scholar 

  • Zeliou, K., Manetas, Y., Petropoulou, Y.: Transient winter leaf reddening in Cistus creticus characterizes weak (stress-sensitive) individuals, yet anthocyanins cannot alleviate the adverse effects on photosynthesis. — J. Exp. Bot. 60: 3031–3042, 2009.

    Article  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 

  • Zhang, K.-M., Yu, H.-J., Shi, K., Zhou, Y.-H., Yu, J.-Q., Xia, X.-J.: Photoprotective roles of anthocyanins in Begonia semperflorens. — Plant Sci. 179: 202–208, 2010.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratory of Plant Physiology, Department of Agricultural Biotechnology, Agricultural University of Athens, Iera Odos 75, 118 55, Athens, Greece

    G. Liakopoulos & I. Spanorigas

Authors
  1. G. Liakopoulos
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. I. Spanorigas
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to G. Liakopoulos.

Additional information

Acknowledgements: The authors wish to thank Professor Yiannis Manetas (University of Patras, Greece) for useful discussion concerning the manuscript.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Liakopoulos, G., Spanorigas, I. Foliar anthocyanins in Pelargonium × hortorum are unable to alleviate light stress under photoinhibitory conditions. Photosynthetica 50, 254–262 (2012). https://doi.org/10.1007/s11099-012-0031-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11099-012-0031-9

Additional key words

Search

Navigation