Advertisement

Photosynthesis Research

, Volume 63, Issue 1, pp 9–21 | Cite as

Photosystem II efficiency and mechanisms of energy dissipation in iron-deficient, field-grown pear trees (Pyrus communis L.)

  • Fermín Morales
  • Ramzi Belkhodja
  • Anunciación Abadía
  • Javier Abadía
Article

Abstract

The dark-adapted Photosystem II efficiency of field-grown pear leaves, estimated by the variable to maximum chlorophyll fluorescence ratio, was little affected by moderate and severe iron deficiency. Only extremely iron-deficient leaves showed a decreased Photosystem II efficiency after dark adaptation. Midday depressions in Photosystem II efficiency were still found after short-term dark-adaptation in iron-deficient leaves, indicating that Photosystem II down-regulation occurred when the leaves were illuminated by excessive irradiance. The actual Photosystem II efficiency at steady-state photosynthesis was decreased by iron deficiency both early in the morning and at midday, due to closure of Photosystem II reaction centers and decreases of the intrinsic Photosystem II efficiency. Iron deficiency decreased the amount of light in excess of that which can be used in photosynthesis not only by decreasing absorptance, but also by increasing the relative amount of light dissipated thermally by the Photosystem II antenna. When compared to the controls, iron-deficient pear leaves dissipated thermally up to 20% more of the light absorbed by the Photosystem II, both early in the morning and at midday. At low light iron-deficient leaves with high violaxanthin cycle pigments to chlorophyll ratios had increases in pigment de-epoxidation, non-photochemical quenching and thermal dissipation. Our data suggest that ΔpH could be the major factor controlling thermal energy dissipation, and that large (more than 10-fold) changes in the zeaxanthin plus antheraxanthin to chlorophyll molar ratio caused by iron deficiency were associated only to moderate increases in the extent of photoprotection.

chlorophyll fluorescence energy dissipation field-grown pear iron deficiency Photosystem II efficiency Pyrus communis 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Abadía J and Abadía A (1993) Iron and plant pigments. In: Barton LL and Hemming BC (eds) Iron Chelation in Plants and Soil Microorganisms, pp 327–344. Academic Press, San Diego, CaliforniaGoogle Scholar
  2. Abadía J, Morales F and Abadía A (1999) Photosystem II efficiency in low chlorophyll, iron-deficient leaves. Plant Soil (in press)Google Scholar
  3. Adams III WW and Demmig-Adams B (1995) The xanthophyll cycle and sustained thermal energy dissipation activity in Vinca minor and Euonymus kiautschovicus in winter. Plant Cell Environ 18: 117–127Google Scholar
  4. Adams III WW, Demmig-Adams, B, Verhoeven AS and Barker DH (1995) 'Photoinhibition' during winter stress: Involvement of sustained xanthophyll cycle-dependent energy dissipation. Aust J Plant Physiol 22: 261–276Google Scholar
  5. Aro E-M, Virgin I and Andersson B (1993) Photoinhibition of Photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143: 113–134PubMedGoogle Scholar
  6. Ball, MC, Hodges VS and Laughlin GP (1991) Cold-induced photoinhibition limits regeneration of snow gum at tree-line. Funct Ecol 5: 663–668Google Scholar
  7. Belkhodja, R, Morales F, Quílez R, López-Millán A-F, Abadía A and Abadía J (1998) Iron deficiency causes changes in chlorophyll fluorescence due to the reduction in the dark of the Photosystem II acceptor side. Photosynth Res 56: 265–276CrossRefGoogle Scholar
  8. Bilger W and 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: 173–185CrossRefGoogle Scholar
  9. Björkman O and Powles SB (1984) Inhibition of photosynthetic reactions under water stress: Interaction with light level. Planta 161: 490–504CrossRefGoogle Scholar
  10. Bungard RA, McNeil D and Morton JD (1997) Effects of nitrogen on the photosynthetic apparatus of Clematis vitalba grown at several irradiances. Aust J Plant Physiol 24: 205–214Google Scholar
  11. Chylla RA and Whitmarsh J (1989) Inactive Photosystem II complexes in leaves. Turnover rate and quantification. Plant Physiol 90: 765–772Google Scholar
  12. de las Rivas J, Abadía A and Abadía J (1989) A new reversed phase HPLC method resolving all major higher plant photosynthetic pigments. Plant Physiol 91: 190–192Google Scholar
  13. Demmig B, Winter K, Krüger A and 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
  14. Demmig-Adams B (1990) Carotenoids and photoprotection: a role for the xanthophyll zeaxanthin. Biochim Biophys Acta 1020: 1–24Google Scholar
  15. Demmig-Adams B and Adams III WW (1992) Photoprotection and other responses of plants to high light stress. Ann Rev Plant Physiol Plant Mol Biol 43: 599–626CrossRefGoogle Scholar
  16. Demmig-Adams B and Adams III WW (1996) Xanthophyll cycle and light stress in nature: Uniform response to excess direct sunlight among higher plant species. Planta 198: 460–470CrossRefGoogle Scholar
  17. Demmig-Adams B, Adams III WW, Logan BA and Verhoeven AS (1995) Xanthophyll cycle-dependent energy dissipation and flexible PS II efficiency in plants acclimated to light stress. Aust J Plant Physiol 22: 249–260Google Scholar
  18. Demmig-Adams B, Adams III WW, Barker DH, Logan BA, Bowling DR and Verhoeven AS (1996) Using chlorophyll fluorescence to assess the fraction of absorbed light allocated to thermal dissipation of excess excitation. Physiol Plant 98: 253–264CrossRefGoogle Scholar
  19. Falk S and Samuelsson G (1992) Recovery of photosynthesis and Photosystem II fluorescence in Chlamydomonas reinhardtii after exposure to three levels of high light. Physiol Plant 85: 61–68CrossRefGoogle Scholar
  20. Farage PK and Long SP (1987) Damage to maize photosynthesis in the field during periods when chilling is combined with high photon fluxes. In: Biggins J (ed) Progress in Photosynthesis Research, Vol 4, pp 139–142. Martinus Nijhoff Publishers, Dordrecht, The NetherlandsGoogle Scholar
  21. Farage PK and Long SP (1991) The occurrence of photoinhibition in an over-wintering crop of oil-seed rape (Brassica napus L.) and its correlation with changes in crop growth. Planta 185: 279–286CrossRefGoogle Scholar
  22. Feild TS, Nedbal L and Ort DR (1998) Nonphotochemical reduction of the plastoquinone pool in sunflower leaves originates from chlororespiration. Plant Physiol 116: 1209–1218CrossRefPubMedGoogle Scholar
  23. Gamon JA and Pearcy RW (1990) Photoinhibition in Vitis californica. The role of temperature during high-light treatment. Plant Physiol 92: 487–494Google Scholar
  24. Genty B, Briantais J-M and Baker NR (1989) The relationship between quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990: 87–92Google Scholar
  25. Gilmore AM and Yamamoto HY (1993) Linear models relating xanthophylls and lumen acidity to non-photochemical fluorescence quenching. Evidence that antheraxanthin explains zeaxanthin-independent quenching. Photosynth Res 35: 67–78CrossRefGoogle Scholar
  26. Godde D and Dannehi H (1994) Stress-induced chlorosis and increase in D1-protein turnover precede photoinhibition in spinach suffering under magnesium/sulphur deficiency. Planta 195: 291–300CrossRefGoogle Scholar
  27. Godde D and Hefer M (1994) Photoinhibition and light-dependent turnover of the D1 reaction-centre polypeptide of Photosystem II are enhanced by mineral-stress conditions. Planta 193: 290–299CrossRefGoogle Scholar
  28. Harbinson J, Genty B and Baker NR (1989) Relationship between the quantum efficiencies of Photosystems I and II in pea leaves. Plant Physiol 90: 1029–1034Google Scholar
  29. Krause GH (1988) Photoinhibition of photosynthesis. An evaluation of damaging and protective mechanisms. Physiol Plant 74: 566–574Google Scholar
  30. Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Meth Enzymol 148: 350–382Google Scholar
  31. Ludlow MM and Björkman O (1984) Paraheliotropic leaf movement in Siratro as a protective mechanism against droughtinduced damage to primary photosynthetic reactions: Damage by excessive light and heat. Planta 161: 505–518CrossRefGoogle Scholar
  32. Morales F, Abadía A and Abadía J (1990) Characterization of the xanthophyll cycle and other photosynthetic pigment changes induced by iron deficiency in sugar beet (Beta vulgaris L.). Plant Physiol 94: 607–613Google Scholar
  33. Morales F, Abadía A and Abadía J (1991) Chlorophyll fluorescence and photon yield of oxygen evolution in iron-deficient sugar beet (Beta vulgaris L.) leaves. Plant Physiol 97: 886–893Google Scholar
  34. Morales F, Susín S, Abadía A, Carrera M and Abadía J (1992) Photosynthetic characteristics of iron chlorotic pear (Pyrus communis L.). J Plant Nutr 15: 1783–1790Google Scholar
  35. Morales F, Abadía A, Belkhodja R and Abadía J (1994) Iron deficiency-induced changes in the photosynthetic pigment composition of field-grown pear (Pyrus communis L.) leaves. Plant Cell Environ 17: 1153–1160Google Scholar
  36. Morales F, Abadía A and Abadía J (1998a) Photosynthesis, quenching of chlorophyll fluorescence and thermal energy dissipation in iron-deficient sugar beet leaves. Aust J Plant Physiol 25: 403–412Google Scholar
  37. Morales F, Grasa R, Abadía A and Abadía J (1998b) Iron chlorosis paradox in fruit trees. J Plant Nutr 21: 815–825Google Scholar
  38. Öquist G and Ogren E (1985) Effects of winter stress on photosynthetic electron transport and energy distribution between the two photosystems of pine as assayed by chlorophyll fluorescence kinetics. Photosynth Res 7: 19–30CrossRefGoogle Scholar
  39. Ottander C and Öquist G (1991) Recovery of photosynthesis in winter-stressed Scots pine. Plant Cell Environ 14: 345–349Google Scholar
  40. Powles SB (1984) Photoinhibition of photosynthesis induced by visible light. Ann Rev Plant Physiol 35: 15–44Google Scholar
  41. Römheld V (1999) The chlorosis paradox: Fe inactivation in leaves as a secondary event in Fe deficiency chlorosis. J Plant Nutr 22: in pressGoogle Scholar
  42. Ruban AV, Young AJ, Pascal AA and Horton P (1994) The effects of illumination on the xanthophyll composition of the Photosystem II light-harvesting complexes of spinach thylakoid membranes. Plant Physiol 104: 227–234PubMedGoogle Scholar
  43. Sanz M, Cavero J and Abadía J (1992) Iron chlorosis in the Ebro river basin, Spain. J Plant Nutr 15: 1971–1981Google Scholar
  44. Somersalo S and Krause GH (1990) Reversible photoinhibition of unhardened and cold-acclimated spinach leaves at chilling temperatures. Planta 180: 181–187CrossRefGoogle Scholar
  45. Spiller S and Terry N (1980) Limiting factors in photosynthesis. II. Iron stress diminishes photochemical capacity by reducing the number of photosynthetic units. Plant Physiol 65: 121–125Google Scholar
  46. Terry N (1980) Limiting factors in photosynthesis. I. Use of iron stress to control photochemical capacity in vivo. Plant Physiol 65: 114–120Google Scholar
  47. Terry N and Abadía J (1986) Function of iron in chloroplasts. J Plant Nutr 9: 609–646Google Scholar
  48. van Kooten O and Snel JFH (1990) The use of chlorophyll fluorescence in plant stress physiology. Photosynth Res 25: 147–150CrossRefGoogle Scholar
  49. Verhoeven AS, Adams III WW and Demmig-Adams B (1996) Close relationship between the state of the xanthophyll cycle pigments and Photosystem II efficiency during recovery from winter stress. Physiol Plant 96: 567–576CrossRefGoogle Scholar
  50. Verhoeven AS, Demmig-Adams B and Adams III WW (1997) Enhanced employment of the xanthophyll cycle and thermal energy dissipation in spinach exposed to high light and N stress. Plant Physiol 113: 817–824PubMedGoogle Scholar
  51. Verhoeven AS, Adams III WW, Demmig-Adams B, Croce R and Bassi R (1999) Xanthophyll cycle pigment localization and dynamics during exposure to low temperatures and light stress in Vinca major. Plant Physiol 120: 727–737CrossRefPubMedGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2000

Authors and Affiliations

  • Fermín Morales
    • 1
  • Ramzi Belkhodja
    • 1
  • Anunciación Abadía
    • 1
  • Javier Abadía
    • 1
  1. 1.Departamento de Nutrición Vegetal, Estación Experimental de Aula DeiConsejo Superior de Investigaciones Científicas (C.S.I.C.)ZaragozaSpain

Personalised recommendations