Planta

, Volume 192, Issue 4, pp 537–544 | Cite as

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
  • Adam M. Gilmore
  • Olle Björkman
Article

Abstract

The relationships among the leaf adenylate energy charge, the xanthophyll-cycle components, and photosystem II (PSII) fluorescence quenching were determined in leaves of cotton (Gossypium hirsutum L. cv. Acala) under different leaf temperatures and different intercellular CO2 concentrations (Ci). Attenuating the rate of photosynthesis by lowering the Ci at a given temperature and photon flux density increased the concentration of high-energy adenylate phosphate bonds (adenylate energy charge) in the cell by restricting ATP consumption (A.M. Gilmore, O. Björkman 1994, Planta 192, 526–536). In this study we show that decreases in photosynthesis and increases in the adenylate energy charge at steady state were both correlated with decreases in PSII photo-chemical efficiency as determined by chlorophyll fluorescence analysis. Attenuating photosynthesis by decreasing Ci also stimulated violaxanthin-de-epoxidation-dependent nonradiative dissipation (NRD) of excess energy in PSII, measured by nonphotochemical fluorescence quenching. However, high NRD levels, which indicate a large trans-thylakoid proton gradient, were not dependent on a high adenylate energy charge, especially at low temperatures. Moreover, dithiothreitol at concentrations sufficient to fully inhibit violaxanthin de-epoxidation and strongly inhibit NRD, affected neither the increased adenylate energy charge nor the decreased PSII photo-chemical efficiency that result from inhibiting photosynthesis. The build-up of a high adenylate energy charge in the light that took place at low Ci and low temperatures was accompanied by a slowing of the relaxation of non-photochemical fluorescence quenching after darkening. This slowly relaxing component of nonphotochemical quenching was also correlated with a sustained high adenylate energy charge in the dark. These results indicate that hydrolysis of ATP that accumulated in the light may acidify the lumen and thus sustain the level of NRD for extended periods after darkening the leaf. Hence, sustained nonphotochemical quenching often observed in leaves subjected to stress, rather than being indicative of photoinhibitory damage, apparently reflects the continued operation of NRD, a photoprotective process.

Key words

Adenylate energy charge ATPase activity Energy dissipation Gossypium Photosynthesis Stress (low temperature, low CO2xanthophyll cycle 

Abbreviations

A

antheraxanthin

adenylate kinase

(myokinase), ATP:AMPphosphotransferase

Ci

intercellular CO2 concentration

DPS

de-epoxidation state of violaxanthin, ([Z+A]/[V+A+Z])

DTT

dithiothreitol

ΔpH

trans-thylakoid proton gradient

ɛ

[2ATP+ADP]

F′

steady-state fluorescence in the presence of NRD

FM

maximal fluorescence in the absence of NRD

F′M

maximal fluorescence in the presence of NRD

NRD

nonradiative energy dissipation

PET

photosynthetic electron transport rate

PFD

photon flux density

ΦPSII

photon yield of PSII photochemistry at the actual reduction state in the light or dark

QA

the primary electron acceptor of PSII

[ATP+ADP+AMP]

SVN

Stern-Volmer nonphotochemical quenching

V

violaxanthin

Z

zeaxanthin

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References

  1. Avron, M., Schreiber, U. (1977) Proton gradients as possible intermediary energy transducers during ATP-driven reverse electron flow in chloroplasts. FEBS Lett. 77, 1–6Google Scholar
  2. Baker, N.R., Horton, P. (1987) Chlorophyll fluorescence quenching during photoinhibition. In: Photoinhibition, pp. 145–168, Kyle, D.J., Osmond, C.B., Arntzen, C.J., eds., Elsevier Science Publishers B.V.Google Scholar
  3. Bilger, W., Björkman, O. (1990) Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis. Photosynth. Res. 25, 173–185Google Scholar
  4. Bilger, W., Björkman, O. (1991) Temperature dependence of violaxanthin de-epoxidation and non-photochemical fluorescence quenching in intact leaves of Gossypium hirsutum L. and Malva parviflora L. Planta 184, 226–234Google Scholar
  5. Bilger, W., Heber, U., Schreiber, U. (1988) Kinetic relationship between energy-dependent fluorescence quenching, light-scattering, chlorophyll luminescence and proton pumping in intact leaves. Z. Naturforsch. 43c, 877–887Google Scholar
  6. Bilger, W., Björkman, O., Thayer, S.S. (1989) Light-induced spectral absorbance changes in relation to photosynthesis and the epoxidation state of xanthophyll cycle components in cotton leaves. Plant Physiol. 91, 542–551Google Scholar
  7. Björkman, O., Demmig-Adams, B. (1993) Regulation of photosynthetic light energy capture, conversion and dissipation in leaves of higher plants. In: Ecological studies, vol. 100, Schulze, E.-D., Caldwell, M., eds., Springer-Verlag (in press)Google Scholar
  8. Björkman, O., Demmig, B., Andrews, T.J. (1988) Mangrove photosynthesis: Response to high-irradiance stress. Aust. J. Plant Physiol. 15, 43–61Google Scholar
  9. Bomsel, J.-L., Pradet, A. (1967) Étude des adénosine-5′-mono, di, et tri-phosphates dans les tissus végétaux. II. Évolution in vivo de l'ATP, l'ADP et l'AMP dans les feuilles de blé en fonction de différentes conditions de milieu. Physiol. Vég. 5, 223–236Google Scholar
  10. Bomsel, J.-L., Pradet, A. (1968) Study of adenosine 5′-mono, di- and triphosphates in plant tissues. IV. Regulation of the level of nucleotides, in vivo, by adenylate kinase: Theoretical and experimental study. Biochim. Biophys. Acta 162, 230–242Google Scholar
  11. Brugnoli, E., Björkman, O. (1992a) Chloroplasts movements in leaves: influence on chlorophyll fluorescence and measurements of light-induced absorbance changes related to ΔpH and zeaxanthin formation. Photosynth. Res. 32, 23–35Google Scholar
  12. Brugnoli, E., Björkman, O. (1992b) Growth of cotton under continuous salinity stress: influence on allocation pattern, stomatal and non-stomatal components of photosynthesis and dissipation of excess light energy. Planta 187, 335–347Google Scholar
  13. Demmig-Adams, B., Adams, W.W. III (1992) Photoprotection and other responses of plants to high light stress. Annu. Rev. Plant Physiol. Plant Mol. Biol. 43, 599–626Google Scholar
  14. Demmig-Adams, B., Winter, K., Krüger, A., Czygan, F.-C. (1989a) Zeaxanthin and the induction and relaxation kinetics of the dissipation of excess excitation energy in leaves in 2% O2, 0% CO2. Plant Physiol. 90, 887–893Google Scholar
  15. Demmig-Adams, B., Winter, K., Krüger, A., Czygan, F.-C. (1989b) Zeaxanthin synthesis, energy dissipation, and photoprotection of photosystem II at chilling temperatures. Plant Physiol. 90, 894–898Google Scholar
  16. Demmig, B., Björkman, O. (1987) Comparison of the effect of excessive light on chlorophyll fluorescence (77K) and photon yield of O2 evolution in leaves of higher plants. Planta 171, 171–184Google Scholar
  17. Demmig, B., Winter, K., Krüger, A., Czygan, F.-C. (1988) Zeaxanthin and the heat dissipation of excess light energy in Nerium oleander exposed to a combination of high light and water stress. Plant Physiol. 87, 17–24Google Scholar
  18. Dietz, K.J., Heber, U. (1984) Rate-limiting factors in leaf photosynthesis. Biochim. Biophys. Acta 767, 432–443Google Scholar
  19. Gilmore, A.M., Björkman, O. (1994) Adenine nucleotides and the xanthophyll cycle in leaves I. Effects of CO2- and temperature-limited photosynthesis on the adenylate energy charge and violaxanthin de-epoxidation. Planta 192, 526–536Google Scholar
  20. Gilmore, A.M., Yamamoto, H.Y. (1992) Dark induction of zeaxanthin-dependent nonphotochemical fluorescence quenching mediated by ATP. Proc. Natl. Acad. Sci. USA 89, 1899–1903Google Scholar
  21. Gilmore, A.M., Yamamoto, H.Y. (1993a) Linear models relating xanthophylls and lumen acidity to non-photochemical fluorescence quenching. Evidence that antheraxanthin explains zeaxanthin-independent quenching. Photosynth. Res. 35, 67–78Google Scholar
  22. Gilmore, A.M., Yamamoto, H.Y. (1993b) Zeaxanthin-dependent quenching of the variable fluorescence arising from ATP-induced reverse electron flow. In: Proceedings of the 9th Annual Congress of Photosynthesis, Murata, N. ed., Dordrecht: Kluwer Academic Publishers, in pressGoogle Scholar
  23. Hager, A. (1969) Lichtbedingte pH-Erniedrigung in einem Chloroplasten-Kompartiment als Ursache der enzymatischen Violaxanthin → Zeaxanthin-Umwandlung; Beziehungen zur Photophosphorylierung. Planta 89, 224–243Google Scholar
  24. Heber, U. (1969) Conformational changes of chloroplasts induced by illumination of leaves in vivo. Biochim. Biophys. Acta 180, 302–319Google Scholar
  25. Heber, U. (1973) Stoichiometry of reduction and phosphorylation during illumination of intact chloroplasts. Biochim. Biophys. Acta 305, 140–152Google Scholar
  26. Heber, U., Santarius, K.A. (1970) Direct and indirect transfer of ATP and ADP across the chloroplast envelope. Z. Naturforsch. 25b, 718–728Google Scholar
  27. Kobayashi, Y., Köster, S., Heber, U. (1982) Light scattering, chlorophyll fluorescence and state of the adenylate system in illuminated spinach leaves. Biochim. Biophys. Acta 682, 44–54Google Scholar
  28. Öquist, G., Huner, N.P.A. (1993) Cold-hardening-induced resistance to photoinhibition of photosynthesis in winter rye is dependent upon an increased capacity for photosynthesis. Planta 189, 150–156Google Scholar
  29. Ottander, C., Hundal, T., Andersson, B., Huner, N.P.A., Öquist, G. (1993) Photosystem II reaction centres stay intact during low temperature photoinhibition. Photosynth. Res. 35, 191–200Google Scholar
  30. Oxborough, K., Horton, P. (1988) A study of the regulation and function of energy-dependent quenching in pea chloroplasts. Biochim. Biophys. Acta 934, 135–143Google Scholar
  31. Powles, S.B. (1984) Photoinhibition of photosynthesis induced by visible light. Annu. Rev. Plant Physiol. 35, 15–44Google Scholar
  32. Santarius, K.A., Heber, U. (1965) Changes in the intracellular levels of ATP, ADP, AMP and Pi and regulatory function of the adenylate system in leaf cells during photosynthesis. Biochim. Biophys. Acta 102, 39–54Google Scholar
  33. Schäfer, C., Björkman, O. (1989) Relationship between efficiency of photosynthetic energy conversion and chlorophyll fluorescence quenching in upland cotton (Gossypium hirsutum L.). Planta 178, 367–376Google Scholar
  34. Schreiber, U. (1980) Light-activated ATPase and ATP-driven reverse electron transport in intact chloroplasts. FEBS Lett. 122, 121–124Google Scholar
  35. Schreiber, U., Avron, M. (1979) Properties of ATP-driven reverse electron flow in chloroplasts. Biochim. Biophys. Acta 546, 436–447Google Scholar
  36. Schreiber, U., Neubauer, C. (1990) O2-dependent electron flow, membrane energization and the mechanism of non-photochemical quenching of chlorophyll fluorescence. Photosynth. Res. 25, 279–293Google Scholar
  37. Sellami, A. (1976) Évolution des adénosine phosphates et de la charge énergétique dans les compartiments chloroplastique et nonchloroplastique des feuilles de blé. Biochim. Biophys. Acta 423, 524–539Google Scholar
  38. Sellami, A., Bomsel, J.-L. (1975) Évolution de la charge énergétique du pool adénylique des feuilles de blé au cours de l'anoxie. Étude de la réversibilité des phénomènes observés. Physiol. Vég. 13, 611–617Google Scholar
  39. Siebke, K., Laisk, A., Oja, V., Kiirats, O., Raschke, K., Heber, U. (1990) Control of photosynthesis in leaves revealed by rapid gas exchange and measurements of the assimilatory force FA. Planta 185, 513–522Google Scholar
  40. Thayer, S.S., Björkman, O. (1990) Leaf xanthophyll content and composition in sun and shade determined by HPLC. Photosynth. Res. 23, 331–343Google Scholar
  41. van Kooten, O., Snel, J.F.H. (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth. Res. 25, 147–150Google Scholar
  42. Yabuki, N., Ashihara, H. (1992) AMP deaminase and the control of adenylate catabolsim in suspension-cultured Catharanthus roseus cells. Phytochemistry 31, 1905–1909Google Scholar
  43. Yamamoto, H.Y. (1962) Studies on the light and dark interconversions of leaf xanthophylls. Arch. Biochem. Biophys. 97, 168–173Google Scholar

Copyright information

© Springer-Verlag 1994

Authors and Affiliations

  • Adam M. Gilmore
    • 1
  • Olle Björkman
    • 1
  1. 1.Department of Plant BiologyCarnegie Institution of WashingtonStanfordUSA

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