Skip to main content
SpringerLink
Log in

Photosynthesis, photoprotection, and growth of shade-tolerant tropical tree seedlings under full sunlight

  • Regular Paper
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

High solar radiation in the tropics is known to cause transient reduction in photosystem II (PSII) efficiency and CO2 assimilation in sun-exposed leaves, but little is known how these responses affect the actual growth performance of tropical plants. The present study addresses this question. Seedlings of five woody neotropical forest species were cultivated under full sunlight and shaded conditions. In full sunlight, strong photoinhibition of PSII at midday was documented for the late-successional tree species Ormosia macrocalyx and Tetragastris panamensis and the understory/forest gap species, Piper reticulatum. In leaves of O. macrocalyx, PSII inhibition was accompanied by substantial midday depression of net CO2 assimilation. Leaves of all species had increased pools of violaxanthin-cycle pigments. Other features of photoacclimation, such as increased Chl a/b ratio and contents of lutein, β-carotene and tocopherol varied. High light caused strong increase of tocopherol in leaves of T. panamensis and another late-successional species, Virola surinamensis. O. macrocalyx had low contents of tocopherol and UV-absorbing substances. Under full sunlight, biomass accumulation was not reduced in seedlings of T. panamensis, P. reticulatum, and V. surinamensis, but O. macrocalyx exhibited substantial growth inhibition. In the highly shade-tolerant understory species Psychotria marginata, full sunlight caused strongly reduced growth of most individuals. However, some plants showed relatively high growth rates under full sun approaching those of seedlings at 40 % ambient irradiance. It is concluded that shade-tolerant tropical tree seedlings can achieve efficient photoacclimation and high growth rates in full sunlight.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Agyeman VK, Swaine MD, Thompson J (1999) Response of tropical forest tree seedlings to irradiance and the derivation of a light response index. J Ecol 87:815–827

    Article  Google Scholar 

  • Barth C, Krause GH (1999) Inhibition of photosystems I and II in chilling-sensitive and chilling-tolerant plants under light and low-temperature stress. Z Naturforsch 54c:645–657

    Google Scholar 

  • Bergmüller E, Porfirova S, Dörmann P (2003) Characterization of an Arabidopsis mutant deficient in γ-tocopherol methyltransferase. Plant Mol Biol 52:1181–1190

    Article  PubMed  Google Scholar 

  • Cazzonelli CI (2011) Carotenoids in nature: insights from plants and beyond. Funct Plant Biol 38:833–847

    Article  CAS  Google Scholar 

  • Chow WS, Qian L, Goodchild DJ, Anderson JM (1988) Photosynthetic acclimation of Alocasia macrorrhiza (L.) G. Don to growth irradiance: structure, function and composition of chloroplasts. Aust J Plant Physiol 15:107–122

    Article  CAS  Google Scholar 

  • Condit R, Hubbell SP, Foster RB (1996) Changes in tree species abundance in a neotropical forest: impact of climate change. J Trop Ecol 12:231–256

    Article  Google Scholar 

  • Condit R, Pérez R, Daguerre N (2011) Trees of Panama and Costa Rica. Princeton University Press, Princeton

    Google Scholar 

  • Dall’Ostro L, Lico C, Alric J, Giuliano G, Havaux M, Bassi R (2006) Lutein is needed for efficient chlorophyll triplet quenching in the major LHCII antenna complex of higher plants and effective photoprotection in vivo under strong light. BMC Plant Biol 6:Art. No. 32

  • Demmig-Adams B (1998) Survey of thermal energy dissipation and pigment composition in sun and shade leaves. Plant Cell Physiol 39:474–482

    Article  CAS  Google Scholar 

  • Demmig-Adams B, Adams WW III (1992) Photoprotection and other responses of plants to high light stress. Annu Rev Plant Physiol Plant Mol Biol 43:599–626

    Article  CAS  Google Scholar 

  • Denslow JS, Schultz JC, Vitousek PM, Strain BR (1990) Growth responses of tropical shrubs to treefall gap environments. Ecology 71:165–179

    Article  Google Scholar 

  • Esteban R, Matsubara S, Jiménez MS, Morales D, Brito P, Lorenzo R, Fernández-Marín B, Becerril JM, García-Plazaola JI (2010) Operation and regulation of the lutein epoxide cycle in seedlings of Ocotea foetens. Funct Plant Biol 37:859–869

    Article  CAS  Google Scholar 

  • 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 Physiol 115:1609–1618

    PubMed  Google Scholar 

  • Franco AC, Lüttge U (2002) Midday depression in savanna trees: coordinated adjustments in photochemical efficiency, photorespiration, CO2 assimilation and water use efficiency. Oecologia 131:356–365

    Article  Google Scholar 

  • Frank H, Cogdell RJ (1996) Carotenoids in photosynthesis. Photochem Photobiol 63:257–264

    Article  PubMed  CAS  Google Scholar 

  • Fryer MJ (1992) The antioxidant effects of thylakoid Vitamin E (α-tocopherol). Plant Cell Environ 15:381–392

    Article  CAS  Google Scholar 

  • García-Plazaola JI, Becerril JM (1999) A rapid high-performance liquid chromatography method to measure lipophilic antioxidants in stressed plants: simultaneous determination of carotenoids and tocopherols. Phytochem Anal 10:307–313

    Article  Google Scholar 

  • García-Plazaola JI, Becerril JM, Hernández A, Niinemets U, Kollist H (2004) Acclimation of antioxidant pools to the light environment in a natural forest canopy. New Phytol 163:87–97

    Article  Google Scholar 

  • Havaux M, Niyogi KK (1999) The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism. Proc Natl Acad Sci USA 96:8762–8767

    Article  PubMed  CAS  Google Scholar 

  • Havaux M, Eymery F, Porfirova S, Rey P, Dörmann P (2005) Vitamin E protects against photoinhibition and photooxidative stress in Arabidopsis thaliana. Plant Cell 17:3451–3469

    Article  PubMed  CAS  Google Scholar 

  • Horton P, Ruban AV, Walters RG (1996) Regulation of light harvesting in green plants. Annu Rev Plant Physiol Plant Mol Biol 47:655–684

    Article  PubMed  CAS  Google Scholar 

  • Jahns P, Miehe B (1996) Kinetic correlation of recovery from photoinhibition and zeaxanthin epoxidation. Planta 198:202–210

    Article  CAS  Google Scholar 

  • Johnson MP, Havaux M, Triantaphylidès C, Ksas B, Pascal AA, Robert B, Davison PA, Ruban AV, Horton P (2007) Elevated zeaxanthin bound to oligomeric LHCII enhances the resistance of Arabidopsis to photooxidative stress by a lipid-protective, antioxidant mechanism. J Biol Chem 282:22605–22608

    Article  PubMed  CAS  Google Scholar 

  • Krause GH, Jahns P (2004) Non-photochemical energy dissipation determined by chlorophyll fluorescence quenching: characterization and function. In: Papageorgiou GC, Govindjee (eds) Chlorophyll fluorescence: a signature of photosynthesis. Kluwer Academic Publishers, Dordrecht, pp 463–495

    Google Scholar 

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

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • 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 Physiol 121:1349–1358

    Article  PubMed  CAS  Google Scholar 

  • Krause GH, Koroleva OY, Dalling JW, Winter K (2001) Acclimation of tropical tree seedlings to excessive light in simulated tree-fall gaps. Plant Cell Environ 24:1345–1352

    Article  CAS  Google Scholar 

  • Krause GH, Gallé A, Gademann R, Winter K (2003a) Capacity of protection against ultraviolet radiation in sun and shade leaves of tropical forest plants. Funct Plant Biol 30:533–542

    Article  CAS  Google Scholar 

  • Krause GH, Grube E, Virgo A, Winter K (2003b) Sudden exposure to solar UV-B radiation reduces net CO2 uptake and photosystem I efficiency in shade-acclimated tropical tree seedlings. Plant Physiol 131:745–752

    Article  PubMed  CAS  Google Scholar 

  • 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 Biol 8:31–41

    Article  PubMed  CAS  Google Scholar 

  • Krause GH, Jahns P, Virgo A, García M, Aranda J, Wellmann E, Winter K (2007) Photoprotection, photosynthesis and growth of tropical tree seedlings under near-ambient and strongly reduced solar ultraviolet-B radiation. J Plant Physiol 164:1311–1322

    Article  PubMed  CAS  Google Scholar 

  • Krause GH, Winter K, Krause B, Jahns P, García M, Aranda J, Virgo A (2010) High-temperature tolerance of a topical tree, Ficus insipida: methodological reassessment and climate change considerations. Funct Plant Biol 37:890–900

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Li Z, Ahn TK, Avenson JT, Ballotari M, Cruz JA, Kramer DN, Bassi R, Fleming GR, Keasling JD, Niyogi KK (2009) Lutein accumulation in the absence of zeaxanthin restores nonphotochemical quenching in the Arabidopsis thaliana npq1 mutant. Plant Cell 21:1798–1812

    Article  PubMed  CAS  Google Scholar 

  • Long SP, Humphries S, Falkowski PG (1994) Photoinhibition of photosynthesis in nature. Annu Rev Plant Physiol Plant Mol Biol 45:633–662

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Marimon BS, Felfili JM, Marimon BH, Franco AC, Fagg CW (2008) Initial development and biomass allocation in seedlings of Brosimum rubescens Taub. (Moraceae) at different shading levels. Acta Bot Bras 22:941–953

    Article  Google Scholar 

  • 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 topical tree genus Inga. Plant Cell Environ 31:548–561

    Article  PubMed  CAS  Google Scholar 

  • Matsubara S, Krause GH, Arand J, Virgo A, Beisel KG, Jahns P, Winter K (2009) Sun-shade patterns of leaf caroteneoid composition in 86 species of neotropical forest plants. Funct Plant Biol 36:20–36

    Article  CAS  Google Scholar 

  • Muraoka H, Tang Y, Terashima I, Koizumi H, Washitani I (2000) Contributions of diffusional limitation, photoinhibition and photorespiration to midday depression of photosynthesis in Arisaema heterophyllum in natural high light. Plant Cell Environ 23:235–250

    Article  CAS  Google Scholar 

  • Nilkens M, Kress E, Lambrev P, Miloslavina Y, Müller M, Holzwarth A, Jahns P (2010) Identification of a slowly inducible zeaxanthin-dependent component of non-photochemical quenching of chlorophyll fluorescence generated under steady-state conditions in Arabidopsis. Biochim Biophys Acta 1797:466–475

    Article  PubMed  CAS  Google Scholar 

  • Peng C-L, Lin Z-F, Su Y-Z, Lin G-Z, Dou H-Y, Zhao C-X (2006) The antioxidative function of Lutein: electron spin resonance studies and chemical detection. Funct Plant Biol 33:829–846

    Article  Google Scholar 

  • Poorter L (1999) Growth responses of 15 rain-forest species to a light gradient: the relative importance of morphological and physiological traits. Funct Ecol 13:396–410

    Article  Google Scholar 

  • Poorter H, Niinemets Ü, Walter A, Fiorani F, Schurr U (2010) A method to construct dose-response curves for a wide rage of environmental factors and plant traits by means of a meta-analysis of phenotypic data. J Exp Bot 61:2043–2055

    Article  PubMed  CAS  Google Scholar 

  • Poorter H, Niklas KJ, Reich PB, Oleksyn J, Poot P, Mommer L (2012) Biomass allocation to leaves, stems and roots: meta-analyses of interspecific variation and environmental control. New Phytol 93:30–50

    Article  Google Scholar 

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

    Google Scholar 

  • Sims DA, Pearcy RW (1989) Photosynthetic characteristics of a tropical forest understory herb, Alocasia macrorrhiza, and a related crop species, Colocasia esculenta grown in contrasting light environments. Oecologia 79:53–59

    Article  Google Scholar 

  • Takahashi S, Badger MR (2011) Photoprotection in plants: a new light on photosystem II damage. Trends Plant Sci 16:53–60

    Article  PubMed  CAS  Google Scholar 

  • Tevini M, Steinmüller D (1985) Composition and function of plastoglobuli. II. Lipid composition of leaves and plastoglobuli during beach senescence. Planta 163:91–96

    Article  CAS  Google Scholar 

  • 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. J Plant Physiol 151:286–292

    Article  CAS  Google Scholar 

  • 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. Aust J Plant Physiol 25:189–195

    Article  Google Scholar 

  • Valladares F, Wrigth SJ, Lasso E, Kitajima K, Pearcy RW (2000) Plastic phenotypic response to light of 16 congeneric shrubs from a Panamanian rainforest. Ecology 81:1925–1936

    Article  Google Scholar 

  • Veenendaal EM, Swaine MD, Lecha TR, Walsh MF, Abebrese IK, Owusu-Afriyie K (1996) Responses of West African forest tree seedlings to irradiance and soil fertility. Funct Ecol 10:501–511

    Article  Google Scholar 

  • Zotz G, Harris G, Königer M, Winter K (1995) High rates of photosynthesis in the tropical pioneer tree, Ficus insipida Willd. Flora 190:265–272

    Google Scholar 

Download references

Acknowledgments

We thank Maria Graf for competent assistance in HPLC analyses. The study was supported by the Smithsonian Tropical Research Institute, Panama, and Deutsche Forschungsgemeinschaft (DFG), Germany.

Author information

Authors and Affiliations

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

    G. Heinrich Krause, Klaus Winter, Barbara Krause, Aurelio Virgo, Jorge Aranda & Milton García

  2. IBG-2: Pflanzenwissenschaften, Forschungszentrum Jülich, 52425, Jülich, Germany

    Shizue Matsubara

  3. Institute of Plant Biochemistry, Heinrich Heine University Düsseldorf, Universitätsstrasse 1, 40225, Düsseldorf, Germany

    G. Heinrich Krause & Peter Jahns

Authors
  1. G. Heinrich Krause
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Klaus Winter
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shizue Matsubara
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Barbara Krause
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Peter Jahns
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Aurelio Virgo
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jorge Aranda
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Milton García
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to G. Heinrich Krause.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Krause, G.H., Winter, K., Matsubara, S. et al. Photosynthesis, photoprotection, and growth of shade-tolerant tropical tree seedlings under full sunlight. Photosynth Res 113, 273–285 (2012). https://doi.org/10.1007/s11120-012-9731-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-012-9731-z

Keywords

Search

Navigation