, Volume 49, Issue 4, pp 497–506 | Cite as

Photoprotective function of betacyanin in leaves of Amaranthus cruentus L. under water stress

  • T. NakashimaEmail author
  • T. Araki
  • O. Ueno
Original Papers


The photoprotective function of leaf betacyanin in water-stressed Amaranthus cruentus plants was examined by comparing leaves of two strains which differ significantly in the amount of betacyanin. At 0, 1, and 2 days after the imposed water stress, leaves were subjected to high-light (HL) treatment to assess their photosynthetic capacity and photoinhibition susceptibility. The water stress equally reduced leaf relative water content (RWC), gas-exchange rate and chlorophyll (Chl) contents in both leaves, indicating that the severity of water stress was comparable between the strains. Consequently, the extent of photoinhibition after the HL treatment increased in both strains as water stress developed; however, it was significantly greater in acyanic leaves than in betacyanic leaves, suggesting lower photoinhibition susceptibility in the betacyanic strain. The betacyanic leaves also exhibited approximately 30% higher values for photochemical quenching coefficient (qP) during the period of water stress despite the nonphotochemical quenching coefficient (qN) did not differ significantly between the strains. These results may be partially explained by the increased amount of leaf betacyanin under water stress. Moreover, a decrease in Chl content in betacyanic leaves might have enhanced light screening effect of betacyanin by increasing relative abundance of betacyanin to Chl molecule. In addition, reduced Chl content increased light penetrability of leaves. As a result, the extent of photoinhibition at the deeper tissue was exacerbated and the Chl fluorescence emitted from these tissues was more readily detected, facilitating assessment of photoinhibition at deeper tissues where the effect of betacyanic light screening is considered to be most apparent. Our results demonstrated that leaf betacyanin contributes to total photoprotective capacity of A. cruentus leaves by lowering excitation pressure on photosystem II (PSII) via attenuation of potentially harmful excess incident light under water stress.

Additional key words

betacyanin grain amaranthus light screening maximum quantum yield of photosystem II photoinhibition water deficit 





day(s) after treatment


difference in transmission spectra between the strains

F0 and Fm

minimum and maximum fluorescence yield of dark-adapted leaves, respectively


variable fluorescence in dark-adapted state

Fm′, F0′, and Fs

maximum, minimum, and steady-state fluorescence yield of light-adapted leaves, respectively


variable fluorescence in light-adapted state


maximum quantum yield of PSII


stomatal conductance


high light


percent inhibition of Fv/Fm after HL treatment


net photosynthetic rate


photosynthetic photon flux density




primary quinone acceptor of PSII

qN and qP

nonphotochemical and photochemical quenching coefficient, respectively


reactive oxygen species


leaf relative water content


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We thank Dr. M. Katsuta (National Institute of Crop Science, National Agriculture and Food Research Organization, Tsukuba, Japan) for kindly providing seeds of A. cruentus, Dr. S. Agarie (Faculty of Agriculture, Kagawa University, Kagawa, Japan) for lecturing us the method of betacyanin quantification, and Dr. S. Yamashita (Faculty of Agriculture, Kyushu University, Fukuoka, Japan) for allowing us to use the spectroscope.


  1. Asada, K.: The water-water cycle as alternative photon and electron sinks. — Phil. Trans. R. Soc. Lond. B. 355: 1419–1431, 2000.CrossRefGoogle Scholar
  2. 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.Google Scholar
  3. Buschmann, C.: Photochemical and non-photochemical quenching coefficients of the chlorophyll fluorescence: comparison of variation and limits. — Photosynthetica 37: 217–224, 1999.CrossRefGoogle Scholar
  4. Carmo-Silva, A.E., Powers, S.J., Keys, A.J., Arrabaca, M.C., Parry, M.A. J.: Photorespiration in C4 grasses remains slow under drought conditions. — Plant Cell Environ. 31: 925–940, 2008.PubMedCrossRefGoogle Scholar
  5. Chalker-Scott, L.: Do anthocyanins function as osmoregulators in leaf tissues? — Adv. Bot. Res. 37: 104–129, 2002.Google Scholar
  6. Du, Y.C., Kawamitsu, Y., Nose, A., Hiyane, S., Murayama, S., Wasano, K., Uchida, Y.: Effects of water stress on carbon exchange rate and activities of photosynthetic enzymes in leaves of sugarcane (Saccharum sp.). — Aust. J. Plant Physiol. 23: 719–726, 1996.CrossRefGoogle Scholar
  7. Elliott, D.C.: Analysis of variability in the Amaranthus betacyanin assay for cytokinins. — Plant Physiol. 63: 274–276, 1979.PubMedCrossRefGoogle Scholar
  8. Escudero, N.L., de Arellano M.L., Luco, J.M., Giménez, M.S., Mucciarelli, S.I.: Comparison of the chemical composition and nutritional value of Amaranthus cruentus flour and its protein concentrate. — Plant Food Human Nutr. 59:15–21, 2004.CrossRefGoogle Scholar
  9. Flexas, J., Escalona, J.M. and Medrano, H.: Down-regulation of photosynthesis by drought under field conditions in grapevine leaves. — Funct. Plant Biol. 25: 893–900, 1998.Google Scholar
  10. Flexas, J., Medrano, H.: Energy dissipation in C3 plants under drought. — Funct. Plant Biol. 29: 1209–1215, 2002.CrossRefGoogle Scholar
  11. Gaume, A., Mächler, F., De León, C, Narro, L., Frossard, E.: Low-P tolerance by maize (Zea mays L.) genotypes: significance of root growth, and organic acids and acid phosphatase root exudation. — Plant Soil 228: 253–264, 2001.CrossRefGoogle Scholar
  12. 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
  13. Ghannoum, O.: C4 photosynthesis and water stress. — Ann. Bot. 103: 635–644, 2009.PubMedCrossRefGoogle Scholar
  14. Gould, K.S., Kuhn, D.N., Lee, D.W., Oberbauer, S.F.: Why leaves are sometimes red? — Nature 378: 241–242, 1995.CrossRefGoogle Scholar
  15. Gould, K.S., Markham, K.R., Smith, R.H., Goris, J.J.: Functional role of anthocyanins in the leaves of Quintinia serrata A. Cunn. — J. Exp. Bot. 51: 1107–1115, 2000.PubMedCrossRefGoogle Scholar
  16. Hayakawa, K., Agarie, S.: Physiological roles of betacyanin in halophyte, Suaeda japonica Makino. — Plant Prod. Sci. 13: 351–359, 2010.CrossRefGoogle Scholar
  17. Hughes, N.M., Neufield, 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, 2005.PubMedCrossRefGoogle Scholar
  18. Hughes, N.M., Smith, W.K.: Attenuation of incident light in Galax urceolata (Diapensiaceae): concerted influence of adaxial and abaxial anthocyanic layers on photoprotection. — Amer. J. Bot. 94: 784–790, 2007.CrossRefGoogle Scholar
  19. Hura, T., Hura, K., Grzesiak, M., Rzepka, A.: Effect of longterm drought stress on leaf gas exchange and fluorescence parameters in C3 and C4 plants. — Acta Physiol. Plant. 29: 103–113, 2007.CrossRefGoogle Scholar
  20. Koizumi, M., Takahashi, K., Mineuchi, K., Nakamura, T. Kano, H.: Light gradients and the transverse distribution of chlorophyll fluorescence in mangrove and Camellia leaves. — Ann. Bot. 81: 527–533, 1998.CrossRefGoogle Scholar
  21. Krause, G.H., Weis, E.: Chlorophyll fluorescence and photosynthesis: the basics. — Annu. Rev. Plant Physiol. Plant Mol. Biol. 42: 313–349, 1991.CrossRefGoogle Scholar
  22. Lichtenthaler, H.K., Buschmann, C., Knapp, M: How to correctly determine the different chlorophyll fluorescence parameters and the chlorophyll fluorescence decrease ratio RFD of leaves with the PAM fluorometer. — Photosynthetica 43: 379–393, 2005.CrossRefGoogle Scholar
  23. Liu, F., Stützel, H.: Leaf water relations of vegetable amaranth (Amaranthus spp.) in response to soil drying. — Eur. J. Agron. 16: 137–150, 2002.CrossRefGoogle Scholar
  24. Long, S.P., Hallgren, J.E.: Measurements of CO2 assimilation by plants in the field and the laboratory. — In: Coombs, J., Hall, D.O., Long, S.P., Scurlock, J.M.O. (ed.): Techniques in Bioproductivity and Photosynthesis. 2nd Ed. Pp. 62–94. Pregamon Press, Oxford — New York — Toronto — Sydney — Frankfurt 1985.Google Scholar
  25. Manetas, Y.: Why some leaves are anthocyanic and why most anthocyanic leaves are red? — Flora 201: 163–177, 2006.CrossRefGoogle Scholar
  26. 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.CrossRefGoogle Scholar
  27. Medrano, H., Bota, J., Abadía, A., Sampol, B., Escalona, J.M., Flexas, J.: Effects of drought on light-energy dissipation mechanisms in high-light acclimated, field grown grapevines. — Funct. Plant Biol. 29: 1197–1207, 2002.CrossRefGoogle Scholar
  28. Munné-Bosch, S., Alegre, L.: Die and let live: leaf senescence contributes to plant survival under drought stress. — Funct. Plant Biol. 31: 203–216, 2004.CrossRefGoogle Scholar
  29. Oberbauer, S.F., Starr, G.: The role of anthocyanins for photosynthesis of Alaskan artic evergreens during snowmelt. — Adv. Bot. Res. 37: 129–145, 2002.CrossRefGoogle Scholar
  30. Ögren, E., Sjöström, M.: Estimation of the effect of photoinhibition on the carbon gain in leaves of a willow canopy. — Planta 181: 560–567, 1990.CrossRefGoogle Scholar
  31. Oguchi, R., Douwstra, P., Fujita, T., Chow, W.S., Terashima, I.: Intra-leaf gradients of photoinhibition induced by different color lights: implications for the dual mechanisms of photoinhibition and for the application of conventional chlorophyll fluorometers. — New Phytol. 191: 146–159, 2011.PubMedCrossRefGoogle Scholar
  32. 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 F0′. — Photosynth. Res. 54: 135–142, 1997.CrossRefGoogle Scholar
  33. Porra, R.J., Thompson, W.A., Kriedemann, P.E.: Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. — Biochim. Biophys. Acta 975: 384–394, 1989.CrossRefGoogle Scholar
  34. Ripley, B.S., Gilbert, M.E., Ibrahim, D.G., Osborne, P.C.: Drought constraints on C4 photosynthesis: stomatal metabolic limitation in C3 and C4 subspecies of Alloteropsis semialata. — J. Exp. Bot. 58: 1351–1363, 2007.PubMedCrossRefGoogle Scholar
  35. Schindler, C., Lichtenthaler, H. K.: Photosynthetic CO2 assimilation, chlorophyll fluorescence and zeaxanthin accumulation in field grown maple tree in the course of a sunny and a cloudy day. — J. Plant Physiol. 148: 399–412, 1994.Google Scholar
  36. Shu, Z., Shao, L., Huang, H.-Y., Zeng, X.-Q., Lin, Z.-F., Chen, G.-Y., Peng, C.-L.: Comparison of thermostability of PSII between the chromatic and green leaf cultivars of Amaranthus tricolor L. — Photosynthetica 47: 548–558, 2009.CrossRefGoogle Scholar
  37. Solovchenko, A.E., Merzlyak, M.N.: Screening of visible and UV radiation as a photoprotective mechanism in plant. — Russ. J. Plant Physiol. 55: 803–822, 2008.Google Scholar
  38. Sun, J., Nishio, J.N., Vogelmann, T.C.: Green light drives CO2 fixation deep within leaves. — Plant Cell Physiol. 39: 1020–1026, 1998.Google Scholar
  39. Takahashi, S., Badger, M.R.: Photoprotection in plants: a new light on photosystem II damage. — Trends Plant Sci. 16: 53–60, 2011.PubMedCrossRefGoogle Scholar
  40. 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.PubMedCrossRefGoogle Scholar
  41. 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: revising the enigmatic question of why leaves are green. — Plant Cell Physiol. 50: 684–697, 2009.PubMedCrossRefGoogle Scholar
  42. Tezara, W., Driscoll, S., Lawlor, D.W.: Partitioning of photosynthetic electron flow between CO2 assimilation and O2 reduction in sunflower plants under water deficit. — Photosynthetica 46: 127–134, 2008.CrossRefGoogle Scholar
  43. Tezara, W., Mitchell, V.J., Driscoll, S.D. Lawlor, D.W.: Water stress inhibits plant photosynthesis by decreasing coupling factor and ATP. — Nature 401: 914–917, 1999.CrossRefGoogle Scholar
  44. van Kooten, O., Snel, J.F.H.: The use of chlorophyll fluores cence nomenclature in plant stress physiology. — Photosynth. Res. 25: 147–150, 1990.CrossRefGoogle Scholar
  45. Vogelmann, T.C., Han, T.: Measurement of gradients of absorbed light in spinach leaves from chlorophyll fluorescence profiles. — Plant Cell Environ. 23:1303–1311, 2000.CrossRefGoogle Scholar
  46. Wang, C.-Q., Liu, T.: Involvement of betacyanin in chilling-induced photoinhibition in leaves of Suaeda salsa. — Photosynthetica 45: 182–188, 2007.CrossRefGoogle Scholar
  47. Zeliou, K., Manetas, Y., Petropoulou, Y.: Transient winter leaf reddening in Citrus creticus characterizes weak (stresssensitive) individuals, yet anthocyanins cannot alleviate the adverse effects on photosynthesis. — J. Exp. Bot. 60: 3031–3042, 2009.PubMedCrossRefGoogle Scholar
  48. Zhu, X., Ort, D.R., Whitmarsh, J. Long, S.P.: The slow reversibility of photosystem II thermal energy dissipation on transfer from high to low light may cause large losses in carbon gain by crop canopies: a theoretical analysis. — J. Exp. Bot. 55: 1167–1175, 2004.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  1. 1.Graduate School of Bioresource and Bioenvironmental SciencesKyushu UniversityFukuokaJapan
  2. 2.Faculty of AgricultureEhime UniversityEhimeJapan
  3. 3.Faculty of AgricultureKyushu UniversityFukuokaJapan

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