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High susceptibility to photoinhibition of young leaves of tropical forest trees

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Abstract

Photoinhibition of photosynthesis was studied in young (but almost fully expanded) and mature canopy sun leaves of several tropical forest tree species, both under controlled conditions (exposure of detached leaves to about 1.8 mmol photons·m-2·s-1) and in the field. The degree of photoinhibition was determined by means of the ratio of variable to maximum chlorophyll (Chl) fluorescence emission (FV/FM) and also by gas-exchange measurements. For investigations in situ, young and mature leaves with similar exposure to sunlight were compared. The results show a consistently higher degree of photoinhibition in the young leaves. In low light, fast recovery was observed in both types of leaves in situ, as well as in the laboratory. The fluorescence parameter 1 — FS/F′M (where FS = stationary fluorescence and f′M = maximum fluorescence during illumination) was followed in situ during the course of the day in order to test its suitability as a measure of the photosynthetic yield of photosystem II (PSII). Electron-transport rates were calculated from these fluorescence signals and compared with rates of net CO2 assimilation. Measurements of diurnal changes in PSII ‘yield’ confirmed the increased susceptibility of young leaves to photoinhibition. Calculated electron transport qualitatively reflected net CO2 uptake in situ during the course of the day. Photosynthetic pigments were analyzed in darkened and illuminated leaves. Young and mature leaves showed the same Chl a/b ratio, but young leaves contained about 50% less Chl a + b per unit leaf area. The capacity of photosynthetic O2 evolution per unit leaf area was decreased to a similar extent in young leaves. On a Chl basis, young leaves contained more α-carotene, more xanthophyll cycle pigments and, under strong illumination, more zeaxanthin than mature leaves. The high degree of reversible photoinhibition observed in these young sun leaves probably represents a dynamic regulatory process protecting the photosynthetic apparatus from severe damage by excess light.

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Abbreviations

Chl:

chlorophyll

FO :

initial chlorophyll fluorescence

FM :

maximum total fluorescence

FV :

maximum variable fluorescence (= FM — FO)

JF :

rate of PSII-driven electron transport ΦPSII = photosynthetic yield of PSII

PFD:

photon flux density (400–700 nm)

PS:

photosystem

References

  • Adams III WW (1988) Photosynthetic acclimation and photoinhibition of terrestrial and epiphytic CAM tissues growing in full sunlight and deep shade. Aust J Plant Physiol 15: 123–134

    Google Scholar 

  • Adams III WW, Terashima I, Brugnoli E, Demmig B (1988) Comparison of photosynthesis and photoinhibition in the CAM vine Hoya australis and several C3 vines growing on the coast of eastern Australia. Plant Cell Environ 11: 173–178

    Google Scholar 

  • Aro E-M, Virgin I, Andersson B (1993) Photoinhibition of photosystem II.Inactivation, protein damage and turnover. Biochim Biophys Acta 1143: 113–134

    Google Scholar 

  • Björkman O, Demmig B (1987) Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. Planta 170: 489–504

    Google Scholar 

  • Bolhàr-Nordenkampf HR, Hofer M, Lechner EG (1991) Analysis of light-induced reduction of the photochemical capacity in field-grown plants.Evidence for photoinhibition? Phosynth Res 27: 31–39

    Google Scholar 

  • Demmig B, Björkman O (1987) Comparison of the effect of excessive light on chlorophyll fluorescence (77 K) and photon yield of O2 evolution in leaves of higher plants. Planta 171: 171–184

    CAS  Google Scholar 

  • Demmig B, Winter K, Krüger A, Czygan F-C (1987) Photoinhibition and zeaxanthin formation in intact leaves.A possible role of the xanthophyll cycle in the dissipation of excess light energy. Plant Physiol 84: 218–224

    Google Scholar 

  • Demmig-Adams B (1990) Carotenoids and photoprotection in plants: A role for the xanthophyll zeaxanthin. Biochim Biophys Acta 1020:1–24

    Article  CAS  Google Scholar 

  • Demmig-Adams B, Adams III WW (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 

  • Demmig-Adams B, Adams III WW, Winter K, Meyer A, Schreiber U, Pereira JS, Krüger A, Czygan F-C, Lange OL (1989) Photochemical efficiency of photosystem II, photon yield of O2 evolution, photosynthetic capacity, and carotenoid composition during the midday depression of net CO2 uptake in Arbutus unedo growing in Portugal. Planta 177: 377–387

    Google Scholar 

  • Genty B, Briantais J-M, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990: 87–92

    CAS  Google Scholar 

  • Giersch C, Krause GH (1991) A simple model relating photoinhibitory fluorescence quenching in chloroplasts to a population of altered photosystem II reaction centers. Photosynth Res 30: 115–121

    Google Scholar 

  • 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

    Google Scholar 

  • Harbinson J, Genty B, Baker NR (1990) The relationship between CO2 assimilation and electron transport in leaves. Photosynth Res 25: 213–224

    Google Scholar 

  • Horton P, Ruban AV, Walters RG (1994) Regulation of light harvesting in green plants.Indication by nonphotochemical quenching of chlorophyll fluorescence. Plant Physiol 106: 415–420

    Google Scholar 

  • Königer M, Harris GC, Virgo A, Winter K (1995) Xanthophyll-cycle pigments and photosynthetic capacity in tropical forest species: a comparitive field study on canopy, gap and understory plants. Oecologia, in press

  • Krall JP, Edwards GE (1992) Relationship between photosystem II activity and CO2 fixation in leaves. Physiol Plant 86: 180–187

    Article  CAS  Google Scholar 

  • Krause GH (1988) Photoinhibition of photosynthesis.An evaluation of damaging and protective mechanisms. Physiol Plant 74: 566–574

    CAS  Google Scholar 

  • Krause GH (1994) Photoinhibition induced by low temperatures. In: Baker NR, Bowyer JR (eds) Photoinhibition of photosynthesis. From molecular mechansisms to the field. BIOS Scientific Publishers, Oxford, pp 331–348

    Google Scholar 

  • Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annu Rev Plant Physiol Plant Mol Biol 42: 313–349

    Article  CAS  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

    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 

  • Oberhuber W, Edwards GE (1993) Temperature dependence of the linkage of quantum yield of photosystem II to CO2 fixation in C4 and C3 plants. Plant Physiol 101: 507–512

    Google Scholar 

  • Oberhuber W, Dai Z-Y, Edwards GE (1993) Light dependence of quantum yields of photosystem II and CO2 fixation in C3 and C4 plants. Photosynth Res 35: 265–274

    Google Scholar 

  • Ögren E (1988) Photoinhibition of photosynthesis in willow leaves under field conditions. Planta 175: 229–236

    Google Scholar 

  • Ögren E (1991) Prediction of photoinhibition of photosynthesis from measurements of fluorescence quenching components. Planta 184: 538–544

    Google Scholar 

  • Ögren E, Evans JR (1992) Photoinhibition of photosynthesis in situ in six species of Eucalyptus. Aust J Plant Physiol 19: 223–232

    Google Scholar 

  • Ögren E, Öquist G (1984) Photoinhibition of photosynthesis in Lemna gibba as induced by interaction between light and temperature.III. Chlorophyll fluorescence at 77 K. Physiol Plant 62: 193–200

    Google Scholar 

  • Ögren E, Rosenqvist E (1992) On the significance of photoinhibition of photosynthesis in the field and its generality among species. Photosynth Res 33: 63–71

    Google Scholar 

  • Ögren E, Sjöström M (1990) Estimation of the effect of photoinhibition on the carbon gain in leaves of a willow canopy. Planta 181: 560–567

    Google Scholar 

  • Öquist G, Chow WS (1992) On the relationship between the quantum yield of photosystem II electon transport, as determined by chlorophyll fluorescence and the quantum yield of CO2-dependent O2 evolution. Photosynth Res 33: 51–62

    Google Scholar 

  • Öquist G, Chow WS, Anderson JM (1992a) Photoinhibition of photosynthesis represents a mechanism for the long-term regulation of photosystem II. Planta 186: 450–460

    Google Scholar 

  • Öquist G, Anderson JM, McCaftery S, Chow WS (1992b) Mechanistic differences in photoinhibition of sun and shade plants. Planta 188: 422–431

    Google Scholar 

  • Schnettger B, Leitsch J, Krause GH (1992) Photoinhibition of photosystem 2 in vivo occurring without net D1 protein degradation. Photosynthetica 27: 261–265

    Google Scholar 

  • Schnettger B, Critchley C, Santore UJ, Graf M, Krause GH (1994) Relationship between photoinhibition of photosynthesis, D1 protein turnover and chloroplast structure: effects of protein synthesis inhibitors. Plant Cell Environ 17: 55–64

    Google Scholar 

  • Seaton GGR, Walker DA (1990) Chlorophyll fluorescence as a measure of photosynthetic carbon assimilation. Proc R Soc London Ser B 242: 29–35

    Google Scholar 

  • Somersalo S, Krause GH (1989) Photoinhibition at chilling temperature.Fluorescence characteristics of unhardened and cold-acclimated spinach leaves. Planta 177: 400–416

    Google Scholar 

  • Somersalo S, Krause GH (1990) Effects of freezing and subsequent light stress on photosynthesis of spinach leaves. Plant Physiol Biochem 28: 467–475

    Google Scholar 

  • Thayer S, Björkman O (1990) Leaf xanthophyll content and composition in sun and shade determined by HPLC. Photosynth Res 23: 331–343

    Google Scholar 

  • Thiele A, Krause GH (1994) Xanthophyll cycle and thermal energy dissipation in photosystem II: Relationship between zeaxanthin formation, energy-dependent fluorescence quenching and photoinhibition. J Plant Physiol 144: 324–332

    Google Scholar 

  • van Wijk KJ, van Hasselt PR (1990) The quantum efficiency of photosystem II and its relation to non-photochemical quenching of chlorophyll fluorescence; the effect of measuring light and growth temperature. Photosynth Res 25: 233–240

    Google Scholar 

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Author notes

  1. G. Heinrich Krause

    Present address: Institute of Plant Biochemistry, Heinrich Heine University Düsseldorf, Universitätsstrasse 1, D-40225, Düsseldorf, Germany

Authors and Affiliations

  1. Smithsonian Tropical Research Institute, Apartado 2072, Balboa, Republic of Panama

    G. Heinrich Krause, Aurelio Virgo & Klaus Winter

Authors
  1. G. Heinrich Krause
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  2. Aurelio Virgo
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  3. Klaus Winter
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Additional information

The authors thank Catherine Lovelock, Smithsonian Tropical Research Institute, Panama City, Panama, for valuable comments on the manuscript and Milton Garcia, Smithsonian Tropical Research Institute, for assistance in leaf absorptance measurements. The study was supported by a Visiting Fellow award of the Smithsonian Institution to G.H.K. and grants of the Mellon Foundation and the Deutsche Forschungsgemeinschaft (SFB 189).

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Krause, G.H., Virgo, A. & Winter, K. High susceptibility to photoinhibition of young leaves of tropical forest trees. Planta 197, 583–591 (1995). https://doi.org/10.1007/BF00191564

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