Role of anthocyanins in high-light stress response

ABSTRACT

Anthocyanins are red-to-blue color non-photochemical active flavonoid pigments. Chemically dyes are low molecular weight secondary metabolites. Their distribution in plant cells is mainly limited to peripheral tissues and structures, such as upper mesophyll, exposed to strong light radiation and related to their function as screening pigments. The onset of synthesis and accumulation may be initiated in response to radiation that exceeds the ability of photosynthetic machinery to utilize absorbed energy as well as low temperature or sudden high light exposition. Dyes absorb the excess radiation reaching the plant, minimizing the risk of oxidative damage. We analysed anthocyanin role in light-stress alleviation of poinsettia leaves characterized by low (green leaf) and high accumulation of screening pigments (red leaf). Analyses allow assessing photosynthetic efficiency, chlorophyll and anthocyanin content and distribution of pigments in leaf blade. Better understanding of the anthocyanins function, synthesis and distribution as screening dyes may be crucial for selection of crop varieties characterized by increased anthocyanin accumulation. It may be beneficial as increased accumulation enhances light-stress resistance. Moreover, antioxidant properties and better pronounced coloration make fruits and vegetables more attractive to customers.

References

• Asen S. (1958). Anthocyanins in bracts of Euphorbia pulcherrima as revealed by paper chromatographic and spectrophotometric methods. Plant Physiology, 33: 14-17
• Alfenito M.R., Souer E., Goodman C.D., Buell R., Mol J., Koes R., Walbot V. (1998). Functional complementation of anthocyanin sequestration in the vacuole by widely divergent glutathione S-transferase. Plant Cell, 10: 1135-1149
• Andersen P.C., Lombard P.B., Westwood M.N. (1984). Leaf conductance, growth, and survival of willow and deciduous fruit tree species under flooded soil conditions. Journal of the American Society of for Horticultural Science, 109: 132-138
• Awad A.S., Edwards D.G., Campbell L.C. (1990). Phosphorus enhancement of salt tolerance of tomato. Crop Science, 30: 123-128
• Balakumar T., Vincent V.H.B., Paliwal K. (1993). On the interaction of UV-B radiation (280–315 nm) with water stress in crop plants. Physiologia Plantarum, 87: 217-222
• Ball M.C., Hodges V.S., Laughlin G.P. (1991). Cold-induced photoinhibition limits regeneration of snow gum at tree-line. Functional Ecology, 5: 663-668
• Banerji D., Sharma V. (1979). Parallelism in hill activity and anthocyanidin content in Euphorbia pulcherrima. Phytochemistry, 18: 1767
• Bors W., Michel C., Saran M. (1994). Flavonoid antioxidants: rate constants for reactions with oxygen radicals. Methods in Enzymology, 234: 420-429
• Brouillard R., Dangles O. (1993). Flavonoids and flower colour. [in:] Harborne JB, The Flavonoids. Advances in Research Since 1986. London, UK: Chapman & Hall Ltd, 565-588
• Buening M.K., Chang R.L., Huang M.T., Fortner J.G., Wood A.W., Conney A.H. (1981). Activation and inhibition of benzo(a)pyrene and aflatoxin Bi metabolism in human liver microsomes by naturally occuring flavonoids. Cancer Research, 41: 67-72
• Chalker-Scott L. (1999). Environmental significance of anthocyanins in plant stress responses. Photochemistry and Photobiology, 70: 1-9
• Chlebicki A. 2004. Od pasożytnictwa do mutualizmu, konsekwencje długotrwałych interakcji. Kosmos, 53: 33
• Christie P.J., Alfenito M.R., Walbot V. (1994). Impact of low-temperature stress on general phenylpropanoid and anthocyanin pathways: Enhancement of transcript abundance and anthocyanin pigmentation in maize seedlings. Planta, 194: 541–549.
• Close D.C., Beadle C.L., Brown P.H., Holz G.K. (2000). Cold-induced photoinhibition affects establishment of Eucalyptus nitens (Deane and Maiden) Maiden and Eucalyptus globulus Trees, 15: 32-41
• Cobbina J., Miller M.H. (1987). Purpling in maize hybrids as influenced by temperature and soil phosphorus. Agronomy Journal, 79: 576-582
• Demmig-Adams B., Adams W.W. (1992). Photoprotection and other responses of plants to high light stress. Annual Review of Plant Physiology and Plant Molecular Biology, 43: 599-626
• Diaz M., Ball E., Lüttge U. (1990). Stress-induced accumulation of the xanthophyl rhodoxanthin in leaves of Aloe vera. Plant Physiology and Biochemistry, 28: 679-682
• Foot J.P., Caporn S.J.M., Lee J.A., Ashenden T.W. (1996). The effect of long-term ozone fumigation on the growth, physiology and frost sensitivity of Calluna vulgaris. New Phytologist, 133: 503-511
• Fang Y., Smith M.A.L., Pépin M.F. (1999). Effects of exogenous methyl jasmonate in elicited anthocyanin-producing cell cultures of ohelo (Vaccinium phalae). In Vitro Cellular & Developmental Biology-Plant, 35(1): 106-113
• Foyer C.H., Lelandais M., Kunert K.J. (1994). Photooxidative stress in plants. Physiologia Plantarum, 92: 696-717
• Goodman C.D., Casati P., Walbot V. (2004). A multidrug resistance-associated protein involved in anthocyanin transport in Zea mays. The Plant Cell, 16: 1812-1826
• Gould K.S., Markham K.R., Smith R.H., Goris J.J. (2000). Functional role of anthocyanins in the leaves of Quitinia serrata Cunn. Journal of Experimental Botany, 51: 1107-1115
• Grotewold E. (2006). The genetics and biochemistry of floral Annual Review of Plant Biology, 57: 761-780
• Hammerschmidt R., Nicholson R.L. (1977). Resistance of maize to anthracnose: Changes in host phenols and pigments. Phytopathology, 67: 251-258
• Harborne J.B., Grayer R.J. (1994). Flavonoids and insects. [in:] Harborne J.B., ed. The Advances in Research Since 1986. Boca Raton, USA: Chapman & Hall/CRC, 589–618.
• Harborne J.B. (1965). Flavonoids: Distribution and contribution to plant colour. [in:] Goodwin T.W., ed. Chemistry and Biochemistry of Plant Pigments. London, UK: Academic Press, 247-278
• Haselgrove L., Botting D., Van Heeswijck R., Høj P.B., Dry P.R., Ford C., Iland P.G. (2000). Canopy microclimate and berry composition: The effect of bunch exposure on the phenolic composition of Vitis vinifera cv, Shiraz grape berries. Australian Journal of Grape and Wine, Research 6: 141-149
• Himi E., Maekawa M., Noda K. (2011). Differential expression of three flavanone 3‑hydroxylase genes in grains and coleoptiles of wheat. International Journal of Plant Genomics, 1-11
• Hipskind J., Wood K., Nicholson R.L. (1996). Localized stimulation of anthocyanin accumulation and delineation of pathogen ingress in maize genetically resistant to Bipolaris maydis race O. Physiological and Molecular Plant Pathology, 49: 247–256.
• Huner N.P.A., Öquist G., Sarhan F. (1998). Energy balance and acclimation to light and cold. Trends in Plant Science, 3: 224-230
• Ishikawa T. (1992). The ATP-dependent glutathione S-conjugate export pump. Trends in Biochemical Sciences, 17(11): 463-468
• Jankiewicz L.S. (2007). Tajemnice piękna kwiatów i niektóre problemy jakie wyniknęły przy ich badaniu. Kosmos, 56: 143-148
• Jovanovic S.V., Simic M.G. (2000). Antioxidants in nutrition. Annals of the New York Academy of Sciences, 899: 326-334
• Kacperska A. 2002. Reakcje roślin na abiotyczne czynniki stresowe. Stres radiacyjny. [in:] Fizjologia roślin pod redakcją Jana Kopcewicza i Stanisława Lewaka, Wydawnictwo Naukowe PWN, Warszawa, 637.
• Kay Q.O.N., Daoud H.S., Stirton C.H. (1981). Pigment distribution, light reflection and cell structure in petals. The Botanical Journal of the Linnean Society, 83: 57-84
• Kitamura S., Shikazono N., Tanaka A. (2004). Transparent Testa 19 is involved in the accumulation of both anthocyanins and proanthocyanidins in Arabidopsis. The Plant Journal, 37: 104-114
• Kitamura S. (2006). Transport of Flavonoids: From Cytosolic Synthesis to Vacuolar Accumulation. [in:] The Science of Flavonoids, 10: 123-146
• Koes R., Verweij W., Quattrocchio F. (2005). Flavonoids: a colorful model for the regulation and evolution of biochemical pathways. Trends in Plant Science, 10: 237.
• Lancaster J.E., Grant J.E., Lister C.E., Taylor M.C. (1994). Skin colour in apples – Influence of copigmentation and plastid pigments on shade and darkness of red colour in five genotypes. Journal of the American Society for Horticultural Science, 119: 63-69
• Lee D.W., Graham R. (1986). Leaf optical properties of rainforest sun and extreme shade plants. American Journal of Botany, 73: 1100-1108
• Lee D.W., Lowry J.B., Stone B.C. (1979). Abaxial anthocyanin layer in leaves of tropical rain forest plants: enhancer of light capture in deep shade. Biotropica, 11: 70-77
• Leyva A., Jarillo T.A., Salinas J., Martinez-Zapater J.M. (1995). Low temperature induces the accumulation of phenylalanine ammonia-lyase and chalcone synthase mRNAs of Arabidopsis thaliana in a light-dependent manner. Plant Physiology 108: 39-46
• Lichtenthaler H.K., Wellburn A.R. (1983). Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochemical Society Transactions, 11: 591-592
• Lo Piero A.R. (2015). The state of the art in biosynthesis of anthocyanins and its regulation in pigmented sweet oranges [(Citrus sinensis) L. Osbeck]. Journal of Agricultural and Food Chemistry, 63(16): 4031-4041
• Long S.P., Humphries S., Falkowski P.G. (1994). Photoinhibition of photosynthesis in nature. Annual Review of Plant Physiology and Plant Molecular Biology, 45: 633-662
• Marinova K., Pourcel L., Weder B., Schwarz M., Barron D., Routaboul J.M., Debeaujon I., Klein M. (2007). The Arabidopsis MATE transport TT12 acts as a vacuolar flavonoid/H⁺-antiporter active in proanthocyanidin-accumulating cells of the seed coat. The Plant Cell, 19: 2023-2038
• Markham K.R., Gould K.S., Winefield C.S., Mitchell K.A., Bloor S.J., Boase M.R. (2000). Anthocyanic vacuolar inclusions – their nature and significance in flower colouration. Phytochemistry, 55: 327-336
• Marrs K.A., Alfenito M.R., Lloyd A.M., Walbot V. (1995). A glutathione S‑transferase involved in vacuolar transfer encoded by the maize gene Bronze-2. Nature, 375: 397-400
• Martin C., Bhatt K., Baumann K., Jin H., Zachgo S., Roberts K., Schwarz-Sommer Z., Glover B., Perez-Rodrigues M. (2002). The mechanism of cell fate determination in petals. Philosophical Transactions of the Royal Society of London Series B, Biological Sciences, 357: 809-813
• Maugé C., Granier T., d’Estaintot B.L., Gargouri M., Manigand C., Schmitter J.M., Chaudière J., Gallois B. (2010). Crystal structure and catalytic mechanism of leucoanthocyanidin reductase from Vitis vinifera. Journal of Molecular Biology, 397(4): 1079-1091
• McClure J.W. (1975). Physiology and functions of flavonoids. [in:] Harborne J.B., Mabry T.J., Mabry H., eds. The Flavonoids. London, UK: Chapman & Hall Ltd, 970-1055
• Louis, O. N. Maitera, G. Boro, J. T. Barminas. Determination of Total Phenolic Content and Some Selected Metals in Extracts of Moringa oleifera, Cassia tora, Ocimum gratissimum, Vernonia baldwinii and Telfairia occidentalis Plant Leaves. World News of Natural Sciences 11 (2017) 11-18
• Merzlyak M.N., Chivkunova O.B., Solovchenko A.E., Naqvi K.R. (2008). Light absorption by anthocyanins in juvenile, stressed, andsenescing leaves. Journal of Experimental Botany, 59: 3903-3911
• Mueller L.A., Goodman C.D., Silady R.A., Walbot V. (2000). AN9, a petunia glutathione S-transferase required for anthocyanin sequestration, is a flavonoid-binding protein. Plant Physiology, 123: 1561-1570
• Neill S.O., Gould K.S., Kilmartin P.A., Mitchell K.A., Markham K.R. (2002). Antioxidant activities of red versus green leaves in Elatostema rugosum. Plant, Cell and Environment, 25: 539-547
• Niyogi K.K. (1999). Photoprotection revisited: genetic and molecular approaches. Annual Review of Plant Physiology and Plant Molecular Biology, 50: 333-359
• Nozzolillo C., Isabelle P., Das G. (1990). Seasonal changes in the phenolic constituents of jack pine seedlings (Pinus banksiana). Canadian Journal of Botany, 68: 2010-2017
• Ntefidou M., Manetas Y. (1996). Optical properties of hairs during the early growth stages of leaf development in Platanus orientalis. Australian Journal of Plant Physiology, 23: 535-538
• Oren-Shamir M., Levi-Nissim A. (1997). Temperature effects on the leaf pigmentation of Continus coggygria ‘Royal Purple’. Journal of Horticultural Science, 72: 425-432
• Pecket R.C., Small J. (1980). Occurrence, location and development of anthocyanoplasts. Phytochemistry, 19: 2571-2576
• Agboje Ivie, Ehondor Nosayaba, Imogoh Shegun, T. O. A. Adeyemi. Growth Rate and Biomass Production of Entandrophragma angolense (Welw.) Seedlings as Affected by Different Organic Soil Amendments. World News of Natural Sciences 9 (2017) 35-44
• Petroni K., Tonelli C. (2011). Recent advances on the regulation of anthocyanin synthesis in reproductive organs. Plant Science, 181(3): 219-229
• Pietrini F., Massacci A. (1998). Leaf anthocyanin content changes in Zea mays grown at low temperature: Significance for the relationship between quantum yield of PSII and the apparent quantum yield of CO₂ assimilation. Photosynthesis Research, 58: 213-219
• Poustka F., Irani N.G., Feller A., Lu Y., Pourcel L., Frame K., Grotewold E. (2007). A trafficking pathway for anthocyanins overlaps with the endoplasmic reticulum-to vacuole proteinsorting route in Arabidopsis and contributes to the formation of vacuolar inclusions. Plant Physiology, 145: 1323-1335
• Pomar F., Ros Barcelo A. (2007). Are red leaves photosynthetically active? Biologia Plantarum, 51: 799-800
• Rajendran L., Suvarnalatha G., Ravishankar G.A., Venkataraman L.V. (1994). Enhancement of anthocyanin production in callus cultures of Daucus carota under the influence of fungal elicitors. Applied Microbiology and Biotechnology, 42: 227-231
• Rice-Evans C.A., Miller N.J., Paganga G. (1997). Antioxidant properties of phenolic compounds. Trends in Plant Science, 2: 152-159
• Sahagún-Godínez E., Lomeli-Sencion J. (1997). Pedilanthus diazlunanus (Euphorbiaceae): pollination by hymenopterans in a bird-pollinated genus. American Journal of Botany, 84(11): 1584-1584.
• Saslowsky D., Winkel-Shirley B. (2001). Localization of flavonoid enzymes in Arabidopsis roots. The Plant Journal 27: 37-48
• Smillie R.M., Hetherington SE. (1999). Photoabatement by anthocyanin shields photosynthetic systems from light stress. Photosynthetica, 36: 451-463
• Steponkus P.L., Lanphear F.O. (1969). The relationship of anthocyanin content to cold hardiness of Hedera helix. Hortscience, 4: 55-56
• Steyn W.J., Wand S.J.E., Holcroft D.M., Jacobs G. (2002). Anthocyanins in vegetative tissues: a proposed unified function in photoprotection. New Phytologist, 155: 349-351
• Strzałka K. (2002). Procesy anaboliczne. Związki fenolowe. [in:] Fizjologia roślin pod redakcją Jana Kopcewicza i Stanisława Lewaka, Wydawnictwo Naukowe PWN, Warszawa, 376-378
• Szweykowska A., Szweykowski J. (1993). Słownik botaniczny, Wiedza Powszechna, Warszawa, 695.
• Tanner G.J., Francki K.T., Abrahams S., Watson J.M., Larkin P.J., Ashton A.R. (2003). Proanthocyanidin biosynthesis in plants. Purification of legume leucoanthocyanidin reductase and molecular cloning of its cDNA. Journal of Biological Chemistry, 278: 31647-31656
• Taubbert D., Breitenbach T., Lazar A., Censarek P., Harlfinger S., Berkels R., Klaus W., Roesen R. (2003). Reaction rate constants of superoxide scavenging by plant antioxidants. Free Radical Biology and Medicine, 35(12): 1599-1607
• Wang H., Cao G., Prior R.L. (1997). Oxygen radical absorbing capacity of anthocyanins. Journal of Agricultural Food Chemistry, 45: 304-309
• Weger H.G., Silim S.N., Guy R.D. (1993). Photosynthetic acclimation to low temperature by western red cedar seedlings. Plant, Cell and Environment, 16: 711-717
• Winkel-Shirley B. (2001). Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiology, 126: 485-493
• Woodrow L., Grodzinski B. (1987). Ethylene evolution from bracts and leaves of poinsettia, Euphorbia pulcherrima Journal of Experimental Botany, 38(12): 2024-2032
• Yamasaki H., Sakihama Y., Ikehara N. (1997). Flavonoid-peroxidase reaction as a detoxification mechanism of plant cells against H₂O₂. Plant Physiology, 115: 1405-1412
• Yamasaki H. (1997). A function of colour. Trends in Plant Science, 2: 7-8
• Yang Z.M., Zheng S.J., Hu A.T., Zheng Y.F., Yan J.Y. (2000). Response of cucumber plants to increased UV-B radiation under water stress. Journal of Environmental Sciences, 12: 236-240
• Zhang H., Wang L., Deroles S., Bennett R., Davies K. (2006). New insight into the structures and formation of anthocyanic vacuolar inclusions in flower petals. BMC Plant Biology, 6: 29
• Zhao J., Dixon R.A. (2010). The ‘ins’ and ‘outs’ of flavonoid transport. Trends In Plant Science, 15(2): 72-80

Download all article in PDF

WSN 81(2) (2017) 145-163

ADVERTISEMENT