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

Do mature shade leaves of tropical tree seedlings acclimate to high sunlight and UV radiation?

G. Heinrich Krause A B E , Esther Grube B C , Olga Y. Koroleva B , Carina Barth B D and Klaus Winter A
+ Author Affiliations
- Author Affiliations

A Smithsonian Tropical Research Institute, Apartado 2072, Balboa, Ancon, Panama.

B Institute of Plant Biochemistry, Heinrich Heine University Düsseldorf, Universitätsstr. 1, 40 225 Düsseldorf, Germany.

C Current address: Botanical Institute, University of Köln, Gyrhofstr. 15, 50 931 Köln, Germany.

D Current address: Boyce Thompson Institute for Plant Research at Cornell University, Tower Road, Ithaca, NY, 14 853, USA.

E Corresponding author; email: ghkrause@uni-duesseldorf.de

Functional Plant Biology 31(7) 743-756 https://doi.org/10.1071/FP03239
Submitted: 8 December 2003  Accepted: 19 April 2004   Published: 22 July 2004

Abstract

Seedlings of neotropical forest trees grown in low light were exposed to 0.5–9 h d–1 direct sunlight, for up to 3 months, to test the capability of mature shade leaves to acclimate to full solar visible and UV radiation. Photosynthetic pigments and the antioxidant, ascorbate, were analysed in leaves of two pioneer and two late-succession species. Seedlings of one or two of these species were used to assess further acclimative responses. Sun-exposure for 0.5 or 1 h d–1 resulted in strongly decreased α-carotene and increased β-carotene and lutein levels. The pool size of xanthophyll-cycle pigments (sum of viola-, anthera- and zeaxanthin) was increased and their turnover was enhanced. These changes were associated with an increase in the capacity of non-photochemical fluorescence quenching and its ‘energy-dependent’ component, qE, and with reduced susceptibility to photoinhibition of PSII. Prolonged exposure to full direct sunlight (approximately 4 or 9 h d–1) resulted in a marked decrease of chlorophyll a + b content and increase in chlorophyll a / b ratios and the pool of xanthophyll-cycle pigments (based on chlorophyll), leading to extremely high zeaxanthin levels during high-light periods. Contents of ascorbate and UV-B-absorbing substances were substantially increased. PSI activity exhibited a response to full sunlight that is characteristic of sun leaves. Rates of net photosynthetic CO2 assimilation under saturating light were increased. The data show that mature shade leaves of seedlings of both early- and late-succession tree species can substantially acclimate to full-sunlight conditions by employing similar physiological mechanisms.

Keywords: Anacardium excelsum, ascorbate, Calophyllum longifolium, chlorophyll a / b, Ficus insipida, photosynthetic pigments, Virola surinamensis.


Acknowledgments

We thank Barbara Krause, Ingrid Prikulis and Aurelio Virgo for competent assistance and Elisabeth King for reading the manuscript. The study was supported by the Andrew W. Mellon foundation, the Smithsonian Tropical Research Institute and the Deutsche Forschungsgemeinschaft.


References


Adams WW, Demmig-Adams B, Verhoeven AS, Barker DH (1995) ‘Photoinhibition’ during winter stress: involvement of sustained xanthophyll cycle-dependent energy dissipation. Australian Journal of Plant Physiology 22, 261–276. open url image1

Adams WW, Demmig-Adams B, Rosenstiel TN, Brightwell AK, Ebbert V (2002) Photosynthesis and photoprotection in overwintering plants. Plant Biology 4, 545–557.
Crossref | GoogleScholarGoogle Scholar | open url image1

Anderson JM, Chow WS, Park Y-I (1995) The grand design of photosynthesis: acclimation of the photosynthetic apparatus to environmental cues. Photosynthesis Research 46, 129–139. open url image1

Asada K (1994) Mechanisms for scavenging reactive molecules generated in chloroplasts under light stress. ‘Photoinhibition of photosynthesis. From molecular mechanisms to the field’. (Eds NR Baker, JR Bowyer) pp. 129–142. (BIOS Scientific Publishes: Oxford, UK)

Barth C, Krause GH (1999) Inhibition of photosystems I and II in chilling-sensitive and chilling-tolerant plants under light and low-temperature stress.  54, 645–647. open url image1

Barth C, Krause GH, Winter K (2001) Responses of photosystem I compared with photosystem II to high-light stress in tropical shade and sun leaves. Plant, Cell and Environment 24, 163–176. open url image1

Bungard RA, Press MV, Scholes JD (2000) The influence of nitrogen on rain forest dipterocarp seedlings exposed to a large increase in irradiance. Plant, Cell and Environment 23, 1183–1194.
Crossref | GoogleScholarGoogle Scholar | open url image1

Caldwell MM, Teramura AH, Tevini M (1989) The changing solar ultraviolet climate and the ecological consequences for higher plants. Trends in Ecology and Evolution 4, 363–367.
Crossref | GoogleScholarGoogle Scholar | open url image1

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

Demmig-Adams B, Adams WW (1992) Photoprotection and other responses of plants to high light stress. Annual Review of Plant Physiology and Plant Molecular Biology 43, 599–626.
Crossref | GoogleScholarGoogle Scholar | open url image1

Demmig-Adams B, Adams WW (1996) The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends in Plant Science 1, 21–26.
Crossref | GoogleScholarGoogle Scholar | open url image1

Demmig-Adams B, Adams WW (1996) Chlorophyll and carotenoid composition in leaves of Euonymus kiautschovicus acclimated to different degrees of light stress in the field. Australian Journal of Plant Physiology 23, 649–659. open url image1

Demmig-Adams B, Winter K, Winkelmann E, Krüger A, Czygan F-C (1989) Photosynthetic characteristics and the ratios of chlorophyll, β-carotene, and the components of the xanthophyll cycle upon a sudden increase in growth light regime in several plant species. Botanica Acta 102, 319–325. 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. open url image1

Gilmore AM, Björkman O (1994) Adenine nucleotides and the xanthophyll cycle in leaves. II. Comparison of the effects of CO2- and temperature-limited photosynthesis on photosystem II fluorescence quenching, the adenylate energy charge and violaxanthin de-epoxidation in cotton. Planta 192, 537–544. open url image1

Gilmore AM, Matsubara S, Ball MC, Barker DH, Itoh S (2003) Excitation energy flow in the photosynthetic apparatus of overwintering evergreens. Plant, Cell and Environment 26, 1021–1034.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hansen U, Fiedler B, Rank B (2002) Variation of pigment composition and antioxidative systems along the canopy light gradient in a mixed beech/oak forest: a comparative study on deciduous tree species differing in shade tolerance. Trees 16, 354–364.
Crossref | GoogleScholarGoogle Scholar | open url image1

Havaux M, Niyogi KK (1999) The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism. Proceedings of the National Academy of Sciences USA 96, 8762–8767.
Crossref | GoogleScholarGoogle Scholar | open url image1

Kirchgeßner H-D, Reichert K, Hauff K, Steinbrecher R, Schnitzler J-P, Pfündel EE (2003) Light and temperature, but not UV radiation, affect chlorophylls and carotenoids in Norway spruce needles (Picea abies (L.) Karst.). Plant, Cell and Environment 26, 1169–1179.
Crossref | GoogleScholarGoogle Scholar | open url image1

Klughammer C, Schreiber U (1998) Measuring P700 absorbance changes in the near infrared spectral region with a dual wavelength pulse modulation system. ‘Photosynthesis. Mechanisms and effects. Vol. 5’. (Ed. G Garab) (Kluwer Academic Publishers: Dordrecht, The Netherlands)

Kolb CA, Käser MA, Kopecky J, Zotz G, Riederer M, Pfündel EE (2001) Effects of natural intensities of visible and ultraviolet radiation on epidermal ultraviolet screening and photosynthesis in grape leaves. Plant Physiology 127, 863–875.
Crossref | GoogleScholarGoogle Scholar | 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. open url image1

Krause GH (1994) Photoinhibition induced by low temperatures. ‘Photoinhibition of photosynthesis. From molecular mechanisms to the field’. (Eds NR Baker, JR Bowyer) pp. 331–348. (Bios Scientific Publishers: Oxford, UK)

Krause GH (1994) The role of oxygen in photoinhibition of photosynthesis. ‘Causes of photooxidative stress and amelioration of defense systems in plants’. (Eds CF Foyer, PM Mullineaux) pp. 43–76. (CRC Press: Boca Raton, FL)

Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annual Review of Plant Physiology and Plant Molecular Biology 42, 313–349.
Crossref | GoogleScholarGoogle Scholar | open url image1

Krause GH, Winter K (1996) Photoinhibition of photosynthesis in plants growing in natural tropical forest gaps. A chlorophyll fluorescence study. Botanica Acta 109, 456–462. open url image1

Krause GH, Jahns P (2003) Pulse amplitude modulated chlorophyll fluorometry and its application in plant science. ‘Light-harvesting antennas in photosynthesis’. (Eds BR Green, WW Parson) pp. 373–399. (Kluwer Academic Publishers: Dordrecht, The Netherlands)

Krause GH, Virgo A, Winter K (1995) High susceptibility to photoinhibition of young leaves of tropical forest trees. Planta 197, 583–591. open url image1

Krause GH, Schmude C, Garden H, Koroleva OY, Winter K (1999) Effects of solar ultraviolet radiation on the potential efficiency of photosystem II in leaves of tropical plants. Plant Physiology 121, 1349–1358.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Krause GH, Carouge N, Garden H (1999) Long-term effects of temperature shifts on xanthophyll cycle and photoinhibition in spinach (Spinacia oleracea).  Australian Journal of Plant Physiology 26, 125–134. 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 and Environment 24, 1345–1352.
Crossref | GoogleScholarGoogle Scholar | 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 | open url image1

Krause GH, Grube E, Virgo A, Winter K (2003) Sudden exposure to solar UV-B radiation reduces net CO2 uptake and photosystem I efficiency in shade-acclimated tropical tree seedlings. Plant Physiology 131, 745–752.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kurasová I, Cajánek M, Kalina J, Urban O, Spunda V (2002) Characterization of acclimation of Hordeum vulgare to high irradiation based on different responses of photosynthetic activity and pigment composition. Photosynthesis Research 72, 71–83.
Crossref | GoogleScholarGoogle Scholar | open url image1

Law MY, Charles SA, Halliwell B (1983) Glutathione and ascorbic acid in spinach (Spinacia oleracea) chloroplasts. The effect of hydrogen peroxide and paraquat. Biochemical Journal 210, 899–903.
PubMed |
open url image1

Leitsch J, Schnettger B, Critchley C, Krause GH (1994) Two mechanisms of recovery from photoinhibition in vivo: reactivation of photosystem II related and unrelated to D1-protein turnover. Planta 194, 15–21. open url image1

Liakoura V, Bornman JF, Karabourniotis G (2003) The ability of abaxial and adaxial epidermis of sun and shade leaves to attenuate UV-A and UV-B radiation in relation to the UV absorbing capacity of the whole leaf methanolic extracts. Physiologia Plantarum 117, 33–43. open url image1

Lovelock CE, Jebb M, Osmond CB (1994) Photoinhibition and recovery in tropical plant species: response to disturbance. Oecologia 97, 297–307. open url image1

Madronich S, McKenzie RL, Caldwell MM, Björn LO (1995) Changes in ultraviolet radiation reaching the earth’s surface. Ambio 24, 143–152. open url image1

Markstädter C, Queck I, Baumeister J, Riederer M, Schreiber U, Bilger W (2001) Epidermal transmittance of leaves of Vicia faba for UV radiation as determined by two different methods. Photosynthesis Research 67, 17–25.
Crossref | GoogleScholarGoogle Scholar | open url image1

Maxwell K, Marrison JL, Leech RM, Griffith H, Horton P (1999) Chloroplast acclimation in leaves of Guzmania monostachia in response to high light. Plant Physiology 121, 89–95.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Mulkey SS, Pearcy RW (1992) Interactions between acclimation and photoinhibition of photosynthesis of a tropical understorey herb, Alocasia macrorrhiza, during simulated canopy gap formation. Functional Ecology 6, 719–729. open url image1

Niyogi KK, Shih C, Chow WS, Pogson B, DellaPenna D, Björkman O (2001) Photoprotection in a zeaxanthin- and lutein-deficient double mutant of Arabidopsis.  Photosynthesis Research 67, 139–145.
Crossref | GoogleScholarGoogle Scholar | open url image1

Oguchi R, Hikosaka K, Hirose T (2003) Does the photosynthetic light-acclimation need change in leaf anatomy? Plant, Cell and Environment 26, 505–512. open url image1

Öquist G, Anderson JM, McCaffery S, Chow WS (1992) Mechanistic differences in photoinhibition of sun and shade plants. Planta 188, 422–431. open url image1

Ruban AV, Horton P (1995) Regulation of non-photochemical quenching of chlorophyll fluorescence in plants. Australian Journal of Plant Physiology 22, 221–230. open url image1

Schöner S, Krause GH (1990) Protective systems against active oxygen species in spinach: response to cold acclimation in excess light. Planta 180, 383–389. open url image1

Searles PS, Flint SD, Caldwell MM (2001) A meta-analysis of plant field studies simulating stratospheric ozone depletion. Oecologia 127, 1–10.
Crossref | GoogleScholarGoogle Scholar | open url image1

Somersalo S, Krause GH (1990) Photoinhibition at chilling temperatures and effects of freezing stress on cold acclimated spinach leaves in the field. Physiologia Plantarum 79, 617–622.
Crossref | GoogleScholarGoogle Scholar | open url image1

Streb P, Aubert S, Gout E, Bligny R (2003) Cold- and light-induced changes of metabolite and antioxidant levels in two high mountain plant species Soldanella alpina and Ranunculus glacialis and a lowland species Pisum sativum.  Physiologia Plantarum 118, 96–104.
Crossref | GoogleScholarGoogle Scholar | 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. open url image1

Thiele A, Krause GH (1994) Xanthophyll cycle and thermal energy dissipation in photosystem II: relationship between zeaxanthin formation, energy-dependent fluorescence quenching and photoinhibition. Journal of Plant Physiology 144, 324–332. open url image1

Thiele A, Schirwitz K, Winter K, Krause GH (1996) Increased xanthophyll cycle activity and reduced D1 protein inactivation related to photoinhibition in two plant systems acclimated to excess light. Plant Science 115, 237–250.
Crossref | GoogleScholarGoogle Scholar | open url image1

Thiele A, Winter K, Krause GH (1997) Low inactivation of D1 protein of photosystem II in young canopy leaves of Anacardium excelsum under high-light stress. Journal of Plant Physiology 151, 286–292. open url image1

Thiele A, Krause GH, Winter K (1998) In situ study of photoinhibition of photosynthesis and xanthophyll cycle activity in plants growing in natural gaps of the tropical forest. Australian Journal of Plant Physiology 25, 189–195. open url image1