Photosynthesis Research

, Volume 58, Issue 3, pp 259–268 | Cite as

Compensatory changes in Photosystem II electron turnover rates protect photosynthesis from photoinhibition

  • Michael J. Behrenfeld
  • Ondrej Prasil
  • Zbigniew S. Kolber
  • Marcel Babin
  • Paul G. Falkowski
Article

Abstract

Exposure of algae or higher plants to bright light can result in a photoinhibitory reduction in the number of functional PS II reaction centers (n) and a consequential decrease in the maximum quantum yield of photosynthesis. However, we found that light-saturated photosynthetic rates (Pmax) in natural phytoplankton assemblages sampled from the south Pacific ocean were not reduced despite photoinhibitory decreases in n of up to 52%. This striking insensitivity of Pmax to photoinhibition resulted from reciprocal increases in electron turnover (\({1 \mathord{\left/ {\vphantom {1 {\tau _{PSII} }}} \right. \kern-\nulldelimiterspace} {\tau _{PSII} }}\))through the remaining functional PS II centers. Similar insensitivity of Pmax was also observed in low light adapted cultures of Thalassiosira weissflogii (a marine diatom), but not in high light adapted cells where Pmax decreased in proportion to n. This differential sensitivity to decreases in n occurred because \({1 \mathord{\left/ {\vphantom {1 {\tau _{PSII} }}} \right. \kern-\nulldelimiterspace} {\tau _{PSII} }}\) was close to the maximum achievable rate in the high light adapted cells, whereas \({1 \mathord{\left/ {\vphantom {1 {\tau _{PSII} }}} \right. \kern-\nulldelimiterspace} {\tau _{PSII} }}\) was initially low in the low light adapted cells and could thus increase in response to decreases in n. Our results indicate that decreases in plant productivity are not necessarily commensurate with photoinhibition, but rather will only occur if decreases in n are sufficient to maximize \({1 \mathord{\left/ {\vphantom {1 {\tau _{PSII} }}} \right. \kern-\nulldelimiterspace} {\tau _{PSII} }}\) or incident irradiance becomes subsaturating.

carbon fixation phytoplankton 

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References

  1. Babin M, Morel A and Gagnon R (1994) An incubator designed for extensive and sensitive measurements of phytoplankton photosynthetic parameters. Limnol Oceanogr 39: 694–702Google Scholar
  2. Baker NR, Farage PK, Stirling CM and Long SP (1994) Photoinhibition of crop photosynthesis in the field at low temperatures. In: Baker NR and Bowyer JR (eds) Photoinhibition of Photosynthesis: From Molecular Mechanisms to the Field, pp 25–49. BIOS Scientific Publishers, OxfordGoogle Scholar
  3. Barber J (1991) Photoinactivation of the isolated Photosystem II reaction centre and its prevention. In: Douglas RH, Moan J and Ronto G (eds) Light Biology and Medicine, pp 21–22. Plenum Press, New YorkGoogle Scholar
  4. Barber J (1992b) The Photosystems: Structure, Function, and Molecular Biology. Elsevier, New YorkGoogle Scholar
  5. Barber J and Andersson B (1992a) Too much of a good thing: light can be good and bad for photosynthesis. Trends Biochem Sci 17: 61–66Google Scholar
  6. Björkman O (1987a) Low temperature chlorophyll fluorescence in leaves and its relationship to photon yield of photosynthesis in photoinhibition. In: Kyle DJ, Osmond CB and Arntzen CJ (eds) Photoinhibition, pp 123–144. Elsevier Publishers, AmsterdamGoogle Scholar
  7. Björkman O (1987b) High-irradiance stress in higher plants and interaction with other stress factors. In: Biggins J (ed) Progress in Photosynthesis Research, pp 1.11–1.18. Martinus Nijhoff Publishers, Dordrecht, The NetherlandsGoogle Scholar
  8. Crofts AR, Baroli I, Kramer D and Taoka S (1993) Kinetics of electron-transfer between Q(A) and Q(B) in wild-type and herbicide-resistant mutants of Chlamydomonas reinhardtii. Z Naturforsch 48c: 259–266Google Scholar
  9. Cullen JJ, Lewis MR, Davis CO and Barber RT (1992) Photosynthetic characteristics and estimated growth rates indicate grazing is the proximate control of primary production in the equatorial Pacific. J Geophys Res 97: 639–654Google Scholar
  10. Doty MS and Oguri M (1957) Evidence for a photosynthetic daily periodicity. Limnol Oceanogr 2: 37–40Google Scholar
  11. Dubinsky Z, Falkowski PG and Wyman K (1986) Light harvesting and utilization by phytoplankton. Plant Cell Physiol 27: 1335–1349Google Scholar
  12. Escoubas J-M, Lomas M, LaRoche J and Falkowski PG (1995) Light intensity regulation of cab gene transcription is signaled by the redox state of the plastoquinone pool. Proc Natl Acad Sci USA 92: 10237–10241Google Scholar
  13. Ewart AJ (1895–1897) On assimilatory inhibition in plants. J Linn Soc Bot 31: 364–461Google Scholar
  14. Falkowski PG (1992) Molecular ecology of phytoplankton photosynthesis. In: Falkowski PG and Woodhead AD (eds) Primary Productivity and Biogeochemical Cycles in the Sea, pp 47–67. Plenum Press, New YorkGoogle Scholar
  15. Falkowski PG and Kolber Z (1995) Variations in chlorophyll fluorescence yields in phytoplankton in the world oceans. Aust J Plant Physiol 22: 341–355Google Scholar
  16. Falkowski PG and Raven J (1997) Aquatic Photosynthesis. Blackwell Science, OxfordGoogle Scholar
  17. Falkowski PG, Owens TG, Ley AC and Mauzerall DC (1981) Effect of growth irradiance levels on the ratio of reaction centers in two species of marine phytoplankton. Plant Physiol 68: 969–973Google Scholar
  18. Falkowski PG, Dubinsky Z and Wyman K (1985) Growth-irradiance relationships in phytoplankton. Limnol Oceanogr 30: 311–321Google Scholar
  19. Falkowski PG, Greene R and Kolber Z (1994) Light utilization and photoinhibition of photosynthesis in marine phytoplankton. In: Baker NR and Bowyer JR (eds) Photoinhibition of Photosynthesis: From Molecular Mechanisms to the Field, pp 407–432. BIOS Scientific Publishers, OxfordGoogle Scholar
  20. Gargas E, Hare I, Martens P and Edler L (1979) Diel changes in phytoplankton photosynthetic efficiency in brackish waters. Mar Biol 52: 113–122Google Scholar
  21. Gong H and Ohad I (1991) The PQ/PQH2 ratio and occupancy of Photosystem II-QB site by plastoquinone control the degradation of Å1 protein during photoinhibition in vivo. J Biol Chem 266: 21293–21299Google Scholar
  22. Guillard RRL and Ryther JH (1962) Studies of marine planktonic diatoms: I. Cyclotella nana Hustedt, and Detonula confervacea (Cleve). Gran Can J Microbiol 8: 229–239Google Scholar
  23. Heber U, Neimanis S and Dietz K.-J (1988) Fractional control of photosynthesis by the QB protein, the cytochrome f/b 6 complex and other components of the photosynthetic apparatus. Planta 173: 267–274Google Scholar
  24. Herron HA and Mauzerall D (1971) The development of photosynthesis in a greening mutant of Chlorella and an analysis of the light saturation curve. Plant Physiol 50: 141–148Google Scholar
  25. Kok B (1956) On the inhibition of photosynthesis by intense light. Biochim Biophys Acta 21: 234–244Google Scholar
  26. Kolber Z and Falkowski PG (1993) Use of active fluorescence to estimate phytoplankton photosynthesis in situ. Limnol Oceanogr 38: 1646–1665Google Scholar
  27. Kolber Z, Prasil O and Falkowski PG (1998) Measurements of variable chlorophyll fluorescence using fast repetition rate techniques: I. Defining methodology and experimental protocols. Biochim Biophys Acta 1367: 88–106Google Scholar
  28. Kolber Z, Zehr J and Falkowski PG (1988) Effects of growth irradiance and nitrogen limitation on photosynthetic energy conversion in Photosystem II. Plant Physiol 88: 923–929Google Scholar
  29. Krause GH (1994) Photoinhibition induced by low temperatures. In: Baker NR and Bowyer JR (eds) Photoinhibition of Photosynthesis: From Molecular Mechanisms to the Field, pp 331–348. BIOS Scientific Publishers, OxfordGoogle Scholar
  30. Krause GH and Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Ann. Rev Plant Physiol Plant Mol Biol 42: 313–349Google Scholar
  31. Kyle DJ (1987) The biochemical basis of photoinhibition of Photosystem II. In: Kyle DJ, Osmond CB and Arntzen CJ (eds) Photoinhibition, pp 197–226. Elsevier Publishers, AmsterdamGoogle Scholar
  32. Kyle DJ, Ohad I and Arntzen CJ (1984) Membrane protein damage and repair: Selective loss of a quinone-protein function in chloroplast membranes. Proc Natl Acad Sci USA 81: 4070–4074Google Scholar
  33. Leverenz JW (1994) Factors determining the nature of the light dosage response curve of leaves. In: Baker NR and Bowyer JR (eds) Photoinhibition of Photosynthesis: from Molecular Mechanisms to the Field, pp 239–254. BIOS Scientific Publishers, OxfordGoogle Scholar
  34. Leverenz JW, Falk S, Pilström C-M and Samuelsson G (1990) The effects of photoinhibition on the photosynthetic light-response curve of green plant cells (Chlamydomonas reinhardtii). Planta 182: 161–168Google Scholar
  35. Ley AC and Mauzerall D (1982) Absolute absorption cross-sections for Photosystem II and the minimum quantum requirement for photosynthesis in Chlorella vulgaris. Biochim Biophys Acta 680: 95–106Google Scholar
  36. Long SP, Humphries S and Falkowski PG (1994) Photoinhibition of photosynthesis in nature. Ann Rev Plant Physiol Plant Mol Biol 45: 633–662Google Scholar
  37. MacCaull WA and Platt T (1977) Diel variations in the photosynthetic parameters of coastal marine phytoplankton. Limnol Oceanogr 22: 723–731Google Scholar
  38. Malone TC, Garside C and Neale PJ (1980) Effects of silicate depletion on photosynthesis by diatoms in the plume of the Hudson river. Mar Biol 58: 197–204Google Scholar
  39. Michel H and Deisenhofer J (1988) Relevance of the photosynthetic reaction center from purple bacteria to the structure of Photosystem II. Biochemistry 27: 1–7Google Scholar
  40. Myers J and Graham J-R (1971) The photosynthetic unit of Chlorella measured by repetitive short flashes. Plant Physiol 48: 282–286Google Scholar
  41. Neale PJ (1987) Algal photoinhibition and photosynthesis in the aquatic environment. In: Kyle DJ, Osmond CB and Arntzen CJ (eds) Photoinhibition, pp 39–65. Elsevier Publishers, AmsterdamGoogle Scholar
  42. Ort DR, Oxborough K and Wise RR (1994) Depression of photosynthesis in crops with water deficits. In: Baker NR and Bowyer JR (eds) Photoinhibition of Photosynthesis: From Molecular Mechanisms to the Field, pp 315–329. BIOS Scientific Publishers, OxfordGoogle Scholar
  43. Osmond CB (1994) What is photoinhibition? Some insights from comparisons of shade and sun plants. In: Baker NR and Bowyer JR (eds) Photoinhibition of Photosynthesis: From Molecular Mechanisms to the Field, pp 1–24. BIOS Scientific Publishers, OxfordGoogle Scholar
  44. Parsons TR, Maita Y, Lalli CM (1984). A Manual of Chemical and Biological Methods for Seawater Analysis (1st ed). Pergamon Press, OxfordGoogle Scholar
  45. Platt T, Gallegos CL and Harrison WG (1980) Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. J Mar Res 38: 687–701Google Scholar
  46. Prasil O, Adir N and Ohad I (1992) Dynamics of Photosystem II: mechanism of photoinhibition and recovery processes. In: Barber J (ed) The Photosystems: Structure, Function and Molecular Biology, pp 295–348. Elsevier Publishers, AmsterdamGoogle Scholar
  47. Raven J (1994) The cost of photoinhibition to plant communities. In: Baker NR and Bowyer JR (eds) Photoinhibition of Photosynthesis: From Molecular Mechanisms to the Field, pp 449–464. BIOS Scientific Publishers, OxfordGoogle Scholar
  48. Sournia A (1974) Circadian periodicities in natural populations of marine phytoplankton. Adv Mar Biol 12: 325–389Google Scholar
  49. Stitt M (1986) Limitation of photosynthesis by carbon metabolism, I. Evidence for excess electron transport capacity in leaves carrying out photosynthesis in saturating light and CO2. Plant Physiol 81: 1115–1122Google Scholar
  50. Sukenik A, Bennett J and Falkowski PG (1987) Light-saturated photosynthesis – limitation by electron transport or carbon fixation? Biochim Biophys Acta 891: 205–215Google Scholar
  51. Talling JF (1957) The phytoplankton population as a compound photosynthetic system. New Phytol 56: 133–149Google Scholar
  52. Walters RG and Horton P (1993) Theoretical assessment of alternative mechanisms for non-photochemical quenching of PS II fluorescence in barley leaves. Photosynth Res 36: 119–139Google Scholar
  53. Weinbaum SA, Gressel J, Reisfeld A and Edelman M (1979) Characterization of the 32,000 Dalton chloroplast membrane protein: Probing its biological function in Spirodela. Plant Physiol 64: 828–832Google Scholar
  54. Yentsch CS and Ryther JH (1957) Short-term variations in phytoplankton chlorophyll and their significance. Limnol Oceanogr 2: 140–142Google Scholar

Copyright information

© Kluwer Academic Publishers 1998

Authors and Affiliations

  • Michael J. Behrenfeld
    • 1
  • Ondrej Prasil
    • 2
  • Zbigniew S. Kolber
    • 1
  • Marcel Babin
    • 3
  • Paul G. Falkowski
    • 1
  1. 1.Institute of Marine and Coastal SciencesRutgers UniversityNew BrunswickUSA; *Author for correspondence (e-mail
  2. 2.Institute of Microbiology, MBU, AVČRCzech Republic
  3. 3.Laboratoire de Physique et Chimie MarinesUniversité Peirre et Marie Curie and CNRSVillefranche-Sur-Mer FFrance

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