Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Sun-shade patterns of leaf carotenoid composition in 86 species of neotropical forest plants

Shizue Matsubara A D , G. Heinrich Krause B C , Jorge Aranda C , Aurelio Virgo C , Kim G. Beisel A , Peter Jahns B and Klaus Winter C
+ Author Affiliations
- Author Affiliations

A Institut für Phytosphäre (ICG-3), Forschungszentrum Jülich, 52425 Jülich, Germany.

B Institut für Biochemie der Pflanzen, Heinrich-Heine-Universität Düsseldorf, Universitätsstraße 1, 40225 Düsseldorf, Germany.

C Smithsonian Tropical Research Institute, Apartado Postal 0843-03092, Panama, Republic of Panama.

D Corresponding author. Email: s.matsubara@fz-juelich.de

Functional Plant Biology 36(1) 20-36 https://doi.org/10.1071/FP08214
Submitted: 4 August 2008  Accepted: 10 November 2008   Published: 7 January 2009

Abstract

A survey of photosynthetic pigments, including 86 species from 64 families, was conducted for leaves of neotropical vascular plants to study sun-shade patterns in carotenoid biosynthesis and occurrence of α-carotene (α-Car) and lutein epoxide (Lx). Under low light, leaves invested less in structural components and more in light harvesting, as manifested by low leaf dry mass per area (LMA) and enhanced mass-based accumulation of chlorophyll (Chl) and carotenoids, especially lutein and neoxanthin. Under high irradiance, LMA was greater and β-carotene (β-Car) and violaxanthin-cycle pool increased on a leaf area or Chl basis. The majority of plants contained α-Car in leaves, but the α- to β-Car ratio was always low in the sun, suggesting preference for β-Car in strong light. Shade and sun leaves had similar β,ε-carotenoid contents per unit Chl, whereas sun leaves had more β,β-carotenoids than shade leaves. Accumulation of Lx in leaves was found to be widely distributed among taxa: >5 mmol mol Chl−1 in 20% of all species examined and >10 mmol mol Chl−1 in 10% of woody species. In Virola elongata (Benth.) Warb, having substantial Lx in both leaf types, the Lx cycle was operating on a daily basis although Lx restoration in the dark was delayed compared with violaxanthin restoration.

Additional keywords: carotene, carotenoid biosynthesis, chlorophyll, leaf dry mass, Virola, xanthophyll cycle.


Acknowledgements

We thank Barbara Krause, Maria Graf and Claudia Walraf for competent assistance. This study was supported by the Andrew W. Mellon Foundation, the Smithsonian Tropical Research Institute and Deutsche Forschungsgemeinschaft (DFG).


References


Anderson JM, Chow WS, Goodchild DJ (1988) Thylakoid membrane organization in sun/shade acclimation. Australian Journal of Plant Physiology 15, 11–26. open url image1

Björkman O (1981) Responses to different quantum flux densities. In ‘Encyclopedia of plant physiology. Vol. 12A. Physiological plant ecology I: responses to the physical environment’. (Eds OL Lange, PS Nobel, CB Osmond, H Ziegler) pp. 57–107. (Springer-Verlag: New York)

Bungard RA, Ruban AV, Hibberd JM, Press MC, Horton P, Scholes JD (1999) Unusual carotenoid composition and a new type of xanthophyll cycle in plants. Proceedings of the National Academy of Sciences of the United States of America 96, 1135–1139.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Cardini F, Pucci S, Calamassi R (2006) Quantitative variations of individual carotenoids in relationship with the leaflet development of six species of the genus Ceratozamia (Cycads). Journal of Plant Physiology 163, 128–140.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Correa M , Goldames C , deStapf MS (2004) ‘Catálogo de las Plantas Vasculares de Panamá.’ (University of Panama and Smithsonian Tropical Research Institute: Panama City, Panama)

Cunningham FX, Gannt E (1998) Genes and enzymes of carotenoid biosynthesis in plants. Annual Review of Plant Physiology and Plant Molecular Biology 49, 557–583.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Czeczuga B (1986) Investigations on carotenoids in Embryophyta. 6. Carotenoids in gymnosperms. Biochemical Systematics and Ecology 14, 13–15.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Dall’Osto L, Cazzaniga S, North H, Marion-Poll A, Bassi R (2007a) The Arabidopsis aba4–1 mutant reveals a specific function for neoxanthin in protection against photooxidative stress. The Plant Cell 19, 1048–1064.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Dall’Osto L, Fiore A, Cazzaniga S, Giuliano G, Bassi R (2007b) Different roles of α- and β-branch xanthophylls in photosystem assembly and photoprotection. Journal of Biological Chemistry 282, 35056–35068.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Davison PA, Hunter CN, Horton P (2002) Overexpression of β-carotene hydroxylase enhances stress tolerance in Arabidopsis. Nature 418, 203–206.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

DellaPenna D, Pogson BJ (2006) Vitamin synthesis in plants: tocopherols and carotenoids. Annual Review of Plant Biology 57, 711–738.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Demmig B, Winter K, Krüger A, Czygan F-C (1987) Photoinhibition and zeaxanthin formation in intact leaves. Plant Physiology 84, 218–224.
CAS | Crossref | PubMed |
open url image1

Demmig-Adams B (1998) Survey of thermal energy dissipation and pigment composition in sun and shade leaves. Plant & Cell Physiology 39, 474–482.
CAS |
open url image1

Demmig-Adams B, Adams WWIII (1992) Carotenoid composition in sun and shade leaves of plants with different life forms. Plant, Cell & Environment 15, 411–419.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Esteban R, Jiménez ET, Jiménez MS, Morales D, Hormaetxe K, Becerril JM, García-Plazaola JM (2007) Dynamics of violaxanthin and lutein epoxide xanthophyll cycles in Lauraceae tree species under field conditions. Tree Physiology 27, 1407–1414.
CAS | PubMed |
open url image1

Esteban R, Jiménez MS, Morales D, Jiménez ET, Hormaetxe K, Becerril JM, Osmond B, García-Plazaola JI (2008) Short- and long-term modulation of the lutein epoxide and violaxanthin cycles in two species of the Lauraceae: sweet bay laurel (Laurus nobilis L.) and avocado (Persea americana Mill.). Plant Biology 10, 288–297.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Färber A, Young AJ, Ruban AV, Horton P, Jahns P (1997) Dynamics of xanthophyll-cycle activity in different antenna subcomplexes in the photosynthetic membranes of higher plants. Plant Physiology 115, 1609–1618.
PubMed |
open url image1

Fiore A, Dall’Osto L, Fraser PD, Bassi R, Giuliano G (2006) Elucidation of the β-carotene hydroxylation pathway in Arabidopsis thaliana. FEBS Letters 580, 4718–4722.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Frank H, Cogdell RJ (1996) Carotenoids in photosynthesis. Photochemistry and Photobiology 63, 257–264.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

García-Plazaola JI, Hernández A, Errasti E, Becerril JM (2002) Occurrence and operation of the lutein epoxide cycle in Quercus species. Functional Plant Biology 29, 1075–1080.
Crossref | GoogleScholarGoogle Scholar | open url image1

García-Plazaola JI, Hormaetxe K, Hernández A, Olano JM, Becerril JM (2004) The lutein epoxide cycle in vegetative buds of woody plants. Functional Plant Biology 31, 815–823.
Crossref | GoogleScholarGoogle Scholar | open url image1

García-Plazaola JI, Matsubara S, Osmond CB (2007) The lutein epoxide cycle in higher plants: its relationships to other xanthophyll cycles and possible functions. Functional Plant Biology 34, 759–773.
Crossref | GoogleScholarGoogle Scholar | open url image1

Goodwin TW (1965) Distribution of carotenoids. In ‘Chemistry and biochemistry of plant pigments’. (Ed. TW Goodwin) pp. 127–140. (Academic Press: London)

Hirschberg J (2001) Carotenoid biosynthesis in flowering plants. Current Opinion in Plant Biology 4, 210–218.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Kim J, DellaPenna D (2006) Defining the primary route for lutein synthesis in plants: the role of Arabidopsis carotenoid β-ring hydroxylase CYP97A3. Proceedings of the National Academy of Sciences of the United States of America 103, 3474–3479.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Königer M, Harris GC, Virgo A, Winter K (1995) Xanthophyll-cycle pigments and photosynthetic capacity in tropical forest species: a comparative field study on canopy, gap and understory plants. Oecologia 104, 280–290.
Crossref | GoogleScholarGoogle Scholar | open url image1

Krause GH, Koroleva OY, Dalling JW, Winter K (2001) Acclimation of tropical tree seedlings to excessive light in simulated tree-fall gaps. Plant, Cell & Environment 24, 1345–1352.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Krause GH, Gallé A, Gademann R, Winter K (2003) Capacity of protection against ultraviolet radiation in sun and shade leaves of tropical forest plants. Functional Plant Biology 30, 533–542.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Krause GH, Grube E, Koroleva OY, Barth C, Winter K (2004) Do mature shade leaves of tropical tree seedlings acclimate to high sunlight and UV radiation? Functional Plant Biology 31, 743–756.
Crossref | GoogleScholarGoogle Scholar | open url image1

Krause GH, Gallé A, Virgo A, García M, Bucic P, Jahns P, Winter K (2006) High-light stress does not impair biomass accumulation of sun-acclimated tropical tree seedlings (Calophyllum longifolium Willd. and Tectona grandis L.f.). Plant Biology 8, 31–41.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Kühlbrandt W, Wang DN, Fujiyoshi Y (1994) Atomic model of plant light harvesting complex by electron crystallography. Nature 367, 614–621.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Liu Z, Yan H, Wang K, Kuang T, Zhang J, Gui L, An X, Chang W (2004) Crystal structure of spinach major light harvesting complex at 2.72 Å resolution. Nature 428, 287–292.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Llorens L, Aranda X, Abadia A, Fleck I (2002) Variations in Quercus ilex chloroplast pigment content during summer stress: involvement in photoprotection according to principal component analysis. Functional Plant Biology 29, 81–88.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Matsubara S, Gilmore AM, Osmond CB (2001) Diurnal and acclimatory responses of violaxanthin and lutein epoxide in the Australian mistletoe Amyema miquelii. Australian Journal of Plant Physiology 28, 793–800.
CAS |
open url image1

Matsubara S, Morosinotto T, Bassi R, Christian A-L, Fischer-Schliebs E , et al . (2003) Occurrence of the lutein–epoxide cycle in mistletoes of the Loranthaceae and Viscaceae. Planta 217, 868–879.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Matsubara S, Naumann M, Martin R, Nichol C, Rascher U, Morosinotto T, Bassi R, Osmond CB (2005) Slowly reversible de-epoxidation of lutein–epoxide in deep shade leaves of a tropical tree legume may ‘lock-in’ lutein-based photoprotection during acclimation to strong light. Journal of Experimental Botany 56, 461–478.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Matsubara S, Morosinotto T, Osmond CB, Bassi R (2007) Short- and long-term operation of the lutein–epoxide cycle in light-harvesting antenna complexes. Plant Physiology 144, 926–941.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Matsubara S, Krause GH, Seltmann M, Virgo A, Kursar TA, Jahns P, Winter K (2008) Lutein–epoxide cycle, light harvesting and photoprotection in species of the tropical tree genus Inga. Plant, Cell & Environment 31, 548–561.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Müller P, Li X-P, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiology 125, 1558–1566.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Munné-Bosch S, Peñuelas J, Asensio D, Llusià J (2004) Airborne ethylene may alter antioxidant protection and reduced tolerance of Holm oak to heat and drought stress. Plant Physiology 136, 2937–2947.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Niyogi KK, Björkman O, Grossman AR (1997) The roles of specific xanthophylls in photoprotection. Proceedings of the National Academy of Sciences of the United States of America 94, 14162–14167.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Pogson BJ, Rissler HM (2000) Genetic manipulation of carotenoid biosynthesis and photoprotection. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 355, 1395–1403.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Pogson BJ, McDonald KA, Truong M, Britton G, DellaPenna D (1996) Arabidopsis carotenoid mutants demonstrate that lutein is not essential for photosynthesis in higher plants. The Plant Cell 8, 1627–1639.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Pogson BJ, Niyogi KK, Björkman O, DellaPenna D (1998) Altered xanthophyll compositions adversely affect chlorophyll accumulation and nonphotochemical quenching in Arabidopsis mutants. Proceedings of the National Academy of Sciences of the United States of America 95, 13324–13329.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Rabinowitch HD, Budowski P, Kedar N (1975) Carotenoids and epoxide cycles in mature-green tomatoes. Planta 122, 91–97.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Reich PB, Walters MB, Ellsworth DS (1997) From tropics to tundra: global convergence in plant functioning. Proceedings of the National Academy of Sciences of the United States of America 94, 13730–13734.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Ruban AV, Berera R, Ilioaia C, van Stokkum IHM, Kennis JTM, Pascal AA, van Amerongen H, Robert B, Horton P, van Grondelle R (2007) Identification of a mechanism of photoprotective energy dissipation in higher plants. Nature 450, 575–579.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Santiago LS, Wright SJ (2007) Leaf functional traits of tropical forest plants in relation to growth form. Functional Ecology 21, 19–27.
Crossref | GoogleScholarGoogle Scholar | open url image1

Scheer H (2003) The pigments. In ‘Light-harvesting antennas in photosynthesis’. (Eds R Green, WW Parson), pp. 29–81. (Kluwer Academic Publishers: Dordrecht, the Netherlands)

Siefermann-Harms D (1994) Light and temperature control of season-dependent changes in the α- and β-carotene content of spruce needles. Journal of Plant Physiology 143, 488–494.
CAS |
open url image1

Snyder AM, Clark BM, Bungard RA (2005) Light-dependent conversion of carotenoids in the parasitic angiosperm Cuscuta reflexa L. Plant, Cell & Environment 28, 1326–1333.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Telfer A (2002) What is β-carotene doing in the photosystem II reaction centre? Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 357, 1431–1440.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Thayer SS, Björkman O (1990) Leaf xanthophyll content and composition in sun and shade determined by HPLC. Photosynthesis Research 23, 331–343.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Watson TL, Close DC, Davidson NJ, Davies NW (2004) Pigment dynamics during cold-induced photoinhibition of Acacia melanoxylon. Functional Plant Biology 31, 481–489.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z , et al . (2004) The worldwide leaf economics spectrum. Nature 428, 821–827.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Yamamoto HY , Bassi R (1996) Carotenoids: localization and function. In ‘Advances in photosynthesis. Vol. 4. Oxygenic photosynthesis: the light reactions’. (Eds DR Ort, CF Yocum) pp. 539–563. (Kluwer Academic Publishers: Dordrecht, the Netherlands)

Yamamoto HY, Nakayama TOM, Chichester CO (1962) Studies on the light and dark interconversions of leaf xanthophylls. Archives of Biochemistry and Biophysics 97, 168–173.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Young A (1993) Factors that affect the carotenoid composition of higher plants and algae. In ‘Carotenoids in photosynthesis’. (Eds A Young, G Britton) pp. 160–205. (Chapman & Hall: London)