title: Coordination of anthocyanin decline and photosynthetic maturation in juvenile leaves of three deciduous tree species.
abstract: Juvenile leaves in high-light environments commonly appear red as a result of anthocyanin pigments, which play a photoprotective role during light-sensitive ontogenetic stages. The loss of anthocyanin during leaf development presumably corresponds to a decreased need for photoprotection, as photosynthetic maturation allows leaves to utilize higher light intensities. However, the relationship between photosynthetic development and anthocyanin decline has yet to be quantitatively described. In this study, anthocyanin concentration was measured against photopigment content, lamina thickness, anatomical development, and photosynthetic CO(2) exchange in developing leaves of three deciduous tree species. In all species, anthocyanin disappearance corresponded with development of c. 50% mature photopigment concentrations, c. 80% lamina thickness, and differentiation of the mesophyll into palisade and spongy layers. Photosynthetic gas exchange correlated positively with leaf thickness and chlorophyll content, and negatively with anthocyanin concentration. Species with more rapid photosynthetic maturation lost anthocyanin earliest in development. Chlorophyll a/b ratios increased with leaf age, and were lower than those of acyanic species, consistent with a shading effect of anthocyanin. These results suggest that anthocyanin reassimilation is linked closely with chloroplast and whole-leaf developmental processes, supporting the idea that anthocyanins protect tissues until light processing and carbon fixation have matured to balance energy capture with utilization.
authors: Department of Biology, Wake Forest University, Winston-Salem, North Carolina 27106 USA.
authors: Nicole M
authors: NM
authors: Hughes
authors: Liberal Studies Department, Dartmouth College, Hanover, New Hampshire 03755 USA.
authors: Christianna B
authors: CB
authors: Morley
authors: Department of Biology, Wake Forest University, Winston-Salem, North Carolina 27106 USA.
authors: William K
authors: WK
authors: Smith
mesh_terms: D031002:Acer / Q000502:physiology; D000872:Anthocyanins / Q000378:metabolism*; D007887:Fabaceae / Q000502:physiology; D031317:Liquidambar / Q000502:physiology; D010788:Photosynthesis / Q000502:physiology*; D018515:Plant Leaves / Q000166:cytology / Q000502:physiology*; D013045:Species Specificity; D014197:Trees / Q000502:physiology*
chemical_list: D000872:Anthocyanins
references: Barker DH, Seaton GGR, Robinson SA. 1997. Internal and external photoprotection in developing leaves of the CAM plant Cotyledon orbiculata. Plant, Cell & Environment 20: 617-624.
references: Cai Z-Q, Slot M, Fan Z-X. 2005. Leaf development and photosynthetic properties of three tropical tree species with delayed greening. Photosynthetica 43: 91-98.
references: Chalker-Scott L. 1999. Environmental significance of anthocyanins in plant stress responses. Photochemistry and Photobiology 70: 1-9.
references: Choinski JS Jr, Ralph P, Eamus D. 2003. Changes in photosynthesis during leaf expansion in Corymbia gummifera. Australian Journal of Botany 51: 111-118.
references: Coley PD. 1981. Ecological and evolutionary responses of tropical trees to herbivory: a quantitative analysis of grazing damage, plant defenses and growth rates. PhD thesis. Chicago, IL, USA: University of Chicago.
references: Coley PD. 1983. Herbivory and defensive characteristics of tree species in a lowland tropical forest. Ecological Monographs 53: 209-233.
references: Coley PD, Aide TM. 1989. Red coloration of tropical young leaves: a possible antifungal defence? Journal of Tropical Ecology 5: 293-300.
references: Cui M, Vogelmann TC, Smith WK. 1991. Chlorophyll and light gradients in sun and shade leaves of Spinacia oleracea. Plant, Cell & Environment 14: 493-500.
references: Demmig-Adams B. 1998. Survey of thermal energy dissipation and pigment composition in sun and shade leaves. Plant Cell Physiology 39: 474-482.
references: Dominy NJ, Lucas PW, Ramsden LW, Riba-Hernandez P, Stoner KE, Turner IM. 2002. Why are young leaves red? Oikos 98: 163-176.
references: Evans JR, Vogelmann TC, Williams WE, Gorton H. 2004. Light capture by the leaf. Photosynthetic adaptation: chloroplast to the landscape. New York, NY, USA: Springer, 15-41.
references: Gould KS. 2004. Nature's swiss army knife: the diverse protective roles of anthocyanins in leaves. Journal of Biomedicine and Biotechnology 5: 314-320.
references: Hamilton WD, Brown SP. 2001. Autumn tree colours as a handicap signal. Proceedings of the Royal Society of London B, Biological Sciences 268: 1489-1493.
references: Hoflacher H, Bauer H. 1982. Light acclimation in leaves of the juvenile and adult life phases of ivy (Hedera helix). Physiologia Plantarum 49: 366-372.
references: Hopkins WG, Hüner NPA. 2004a. Photosynthetic electron transport. In: Hopkins WG, Hüner NP, eds. Introduction to plant physiology. New York, NY, USA: John Wiley, 68-71.
references: Hopkins WG, Hüner NPA. 2004b. Lateral heterogeneity is the unequal distribution of thylakoid complexes. In: Hopkins WG, Hüner NP, eds. Introduction to plant physiology. New York, NY, USA: John Wiley, 75-76.
references: Hughes NM. 2004. Functional role of anthocyanins in high light winter leaves of the evergreen herb Galax urceolata. MSc thesis. Boone, NC, USA: Appalachian State University.
references: Hughes NM, Smith WK. (2007). Attenuation of incident light in Galax urceolata (Diapensiaceae): concerted influence of adaxial and abaxial anthocyanic layers on photoprotection. American Journal of Botany 94: 784-790.
references: Jiang CD, Gao HY, Zou QI, Jiang GM, Li LH. 2006. Leaf orientation, photorespiration and xanthophyll cycle protect young soybean leaves against high irradiance in field. Environmental and Experimental Botany 55: 87-96.
references: Jones CS. 1995. Does shade prolong juvenile leaf development? A morphological analysis of leaf shape changes in Cucurbita argyrosperma subsp. sororia (Cucurbitaceae). American Journal of Botany 82: 346-359.
references: Karageorgou P, Manetas Y. 2006. The importance of being red when young: anthocyanins and the protection of young leaves of Quercus coccifera from insect herbivory and excess light. Tree Physiology 26: 613-621.
references: Krause GH, Virgo A, Winter K. 1995. High susceptibility to photoinhibition of young leaves of tropical forest trees. Planta 197: 583-591.
references: Kursar TA, Coley PD. 1992. Delayed greening in tropical leaves: an antiherbivore defense? Biotropica 24: 256-262.
references: Lee DW, Brammeier S, Smith AP. 1987. The selective advantages of anthocyanins in developing leaves of mango and cacao. Biotropica 19: 40-49.
references: Lee DW, Collins TM. 2001. Phylogenetic and ontogenetic influences on the distribution of anthocyanins in betacyanins in leaves of tropical plants. International Journal of Plant Sciences 162: 1141-1153.
references: Lee DW, Lowry JB, Stone BC. 1979. Abaxial anthocyanin layer in leaves of tropical rain forest plants: enhancer of light capture in deep shade. Biotropica 11: 70-77.
references: Lee DW, O’Keefe J, Holbrook NM, Feild TS. 2003. Pigment dynamics and autumn leaf senescence in a New England deciduous forest, eastern USA. Ecological Research 18: 677-694.
references: Liakopoulos G, Nikolopoulos D, Klouvatou A, Vekkos K-A, Manetas Y, Karabourniotis G. 2006. The Photoprotective Role of Epidermal Anthocyanins and Surface Pubescence in Young Leaves of Grapevine (Vitis vinifera). Annals of Botany 98: 257-265.
references: Manetas Y. 2006. Why some leaves are anthocyanic and why most anthocyanic leaves are red. Flora 201: 163-177.
references: Manetas Y, Drinia A, Petropoulou Y. 2002. High contents of anthocyanins in young leaves are correlated with low pools of xanthophyll cycle components and low risk of photoinhibition. Photosynthetica 40: 349-354.
references: Manetas Y, Petropoulou Y, Psaras GK, Drinia A. 2003. Exposed red (anthocyanic) leaves of Quercus coccifera display shade characteristics. Functional Plant Biology 30: 265-270.
references: Miranda V, Baker NR, Long SP. 1981a. Limitation of photosynthesis in different regions of the Zea mays leaf. New Phytologist 89: 179-190.
references: Miranda V, Baker NR, Long SP. 1981b. Anatomical variation along the length of the Zea mays leaf in relation to photosynthesis. New Phytologist 88: 595-605.
references: Murray JR, Hackett WP. 1991. Dihydroflavonol reductase activity in relation to differential anthocyanin accumulation in juvenile and mature phase Hedera helix L. Plant Physiology 97: 343-351.
references: Neill SO, Gould KS, Kilmartin PA, Mitchell KA, Markham KR. 2002. Antioxidant capacities of green and cyanic leaves in the sun species Quintinia serrata. Functional Plant Biology 29: 1437-1443.
references: Niinemets U, Tenhunen JD, Beyschlag W. 2004. Spatial and age-dependent modification of photosynthetic capacity in four Mediterrean oak species. Functional Ecology 31: 1179-1193.
references: Numata S, Kachi N, Okuda T, Manokaran N. 2004. Delayed greening, leaf expansion, and damage to sympatric Shorea species in a lowland rain forest. Journal of Plant Research 117: 19-25.
references: Pettigrew WT, Vaughn KC. 1998. Physiological, structural, and immunological characterization of leaf and chloroplast development in cotton. Protoplasma 202: 23-37.
references: Porra RJ. 2002. The chequered history of the development and use of simultaneous equations for the accurate determination of chlorophylls a and b. Photosynthesis Research 73: 149-156.
references: Price JR, Sturgess VC. 1938. A survey of anthocyanin. VI. Biochemical Journal 32: 1658-1660.
references: Rice-Evans CA, Miller NH, Paganga G. 1997. Antioxidant properties of phenolic compounds. Trends in Plant Science 2: 152-159.
references: Smith AM. 1909. On the internal temperatures of leaves in tropical insolation, with special reference to the effect of their colour on temperature; also observations on the periodicity of the appearance of young coloured leaves of trees growing in Peradinaya Gardens. Annals of the Royal Botanical Garden. Peradinaya 5: 229-297.
references: Smith WK, Vogelmann TC, DeLucia EH, Bell DT, Shepherd KA. 1997. Leaf form and photosynthesis. Bioscience 47: 785-793.
references: Stone BC. 1979. Protective coloration of young leaves in certain Malaysian palms. Biotropica 11: 26.
references: Sun J, Nishio JN. 2001. Why abaxial illumination limits photosynthetic carbon fixation in spinach leaves. Plant and Cell Physiology 42: 1-8.
references: Sun J, Nishio JN, Vogelmann TC. 1996. High-light effects on CO2 fixation gradients across leaves. Plant, Cell & Environment 19: 1261-1271.
references: Vogelmann TC, Nishio JN, Smith WK. 1996. Leaves and light capture: light propagation and gradients of carbon fixation within leaves. Trends in Plant Science 1: 65-70.
references: Wallace LL, Dunn EL. 1980. Comparative photosynthesis of three gap phase successional tree species. Oecologia 45: 331-340.
references: Wang H, Cao G, Prior RL. 1997. Oxygen radical absorbing capacity of anthocyanins. Journal of Agricultural Food Chemistry 45: 304-309.
references: Wellburn AR. 1994. Determination of chlorophyll-a and chlorophyll-b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. Journal of Plant Physiology 144: 307-313.