Skip to main content
Log in

Photosystem II efficiency in low chlorophyll, iron-deficient leaves

  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Iron deficiency (iron chlorosis) is the major nutritional stress affecting fruit tree crops in calcareous soils in the Mediterranean area. This work reviews the changes in PS II efficiency in iron-deficient leaves. The iron deficiency-induced leaf yellowing is due to decreases in the leaf concentrations of photosynthetic pigments, chlorophylls and carotenoids. However, carotenoids, and more specifically lutein and the xanthophylls of the V+A+Z (Violaxanthin+ Antheraxanthin+Zeaxanthin) cycle are less affected than chlorophylls. Therefore, iron-chlorotic leaves grown in either growth chambers or field conditions have increases in the molar ratios lutein/chlorophyll a and (V+A+Z)/chlorophyll a. These pigment changes are associated to changes in leaf absorptance and reflectance. In the chlorotic leaves the amount of light absorbed per unit chlorophyll increases. The low chlorophyll, iron-deficient leaves showed no sustained decreases in PS II efficiency, measured after dark adaptation, except when the deficiency was very severe. This occurred when plants were grown in growth chambers or in field conditions. However, iron-deficient leaves showed decreases in the actual PS II efficiency at steady-state photosynthesis, due to decreases in photochemical quenching and intrinsic PS II efficiency. Iron-chlorotic leaves were protected not only by the decrease in leaf absorptance, but also by down-regulation mechanisms enhancing non-photochemical quenching and thermal dissipation of the light absorbed by PS II within the antenna pigment bed.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Abadía J and Abadía A 1993 Iron and plant pigments. In Iron Chelation in Plants and Soil Microorganisms. Eds L L Barton and B C Hemming. pp 327-343. Academic Press, New York.

    Google Scholar 

  • Abadía A, Poc A and Abadía J 1991 Could iron nutrition status be evaluated through photosynthetic pigment changes? J. Plant Nutr. 14, 987-999.

    Article  Google Scholar 

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

    CAS  Google Scholar 

  • 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, 265-276.

    Article  CAS  Google Scholar 

  • Bolle-Jones E W and Notton B A 1953 The relative proportions of the chloroplast pigments as influenced by different levels of iron and potassium supply. Plant Soil 1, 87-100.

    Article  Google Scholar 

  • Chaney R L, Brown J C and Tiffin L O 1972 Obligatory reduction of ferric chelates in iron uptake by soybean. Plant Physiol. 50, 208-213.

    PubMed  CAS  Google Scholar 

  • Davis T, Jolley V, Walser R, Brown J and Blaylock A 1986 Net photosynthesis of Fe-efficient and Fe-inefficient soybean cultivars grown under varying iron levels. J. Plant Nutr. 9, 671-681.

    CAS  Google Scholar 

  • Demmig-Adams B 1990 Carotenoids and photoprotection: a role for the xanthophyll zeaxanthin. Biochim. Biophys. Acta 1020, 1-24.

    Article  CAS  Google Scholar 

  • Demmig-Adams B, Adams III W W, Logan B A and Verhoeven A S 1995 Xanthophyll cycle-dependent energy dissipation and flexible PS II efficiency in plants acclimated to light stress. Aust. J. Plant Physiol. 22, 249-260.

    CAS  Google Scholar 

  • Díez-Altarés M 1959 Fotodescomposición de clorofila en casos de deficiencia inducida de hierro. An. Estac. Exp. Aula Dei (Zaragoza) 6, 1-80.

    Google Scholar 

  • 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, 61-68.

    Article  CAS  Google Scholar 

  • Falkowski P G, Behrenfeld M and Kolber Z 1995 Variations in photochemical energy conversion efficiency in oceanic phytoplankton: scaling from reaction center to the global ocean. In Photosynthesis: from light to biosphere. Vol V. Ed. P Mathis. pp 755-759. Kluwer Academic Publishers, Dordrecht.

    Google Scholar 

  • Genty B, Briantais J-M and Baker N R 1989 The relationship between quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim. Biophys. Acta 990, 87-92.

    CAS  Google Scholar 

  • Genty B, Harbinson J, Cailly A L and Rizza F 1996 Fate of excitation at PS II in leaves: the nonphotochemical side. Presented at The Third BBSRC Robert Hill Symposium on Photosynthesis, March 31 to April 3, 1996, University of Sheffield, Department of Molecular Biology and Biotechnology, Western Bank, Sheffield, UK, abstract no. P28.

  • Gilmore A M, Hazlett T L and Govindjee 1995 Xanthophyll cycledependent quenching of Photosystem II chlorophyll a fluorescence: Formation of a quenching complex with a short fluorescence lifetime. Proc. Natl. Acad. Sci. USA 92, 2273-2277.

    Article  PubMed  CAS  Google Scholar 

  • Gilmore A M and Yamamoto H Y 1993 Linear models relating xanthophylls and lumen acidity to non-photochemical fluorescence quenching. Evidence that antheraxanthin explains zeaxanthin-independent quenching. Photosynth. Res. 35, 67-78.

    Article  CAS  Google Scholar 

  • Greene R M, Geider R J, Kolber Z and Falkowski P G 1992 Ironinduced changes in light harvesting and photochemical energy conversion processes in eukaryotic marine algae. Plant Physiol. 100, 565-575.

    PubMed  CAS  Google Scholar 

  • Guikema J A 1985 Fluorescence induction characteristics of Anacystis nidulans during recovery from iron deficiency. J. Plant Nutr. 8, 891-908.

    CAS  Google Scholar 

  • Heras L 1960 Influence of light intensity on the redox potential in leaves in cases of iron-induced chlorosis. Nature 188, 335-336.

    Article  CAS  Google Scholar 

  • Horton P, Ruban A V, Rees D, Pascal A A, Noctor G and Young A J 1991 Control of the light-harvesting function of chloroplast membranes by aggregation of the LHCII chlorophyll-protein complex. FEBS Lett. 292, 1-4.

    Article  PubMed  CAS  Google Scholar 

  • Horton P, Ruban A V and Walters R G 1996 Regulation of light harvesting in green plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47, 655-684.

    Article  PubMed  CAS  Google Scholar 

  • Hurley A K, Walser R H and Davis T D 1986a Net photosynthesis and chlorophyll content in silver maple after trunk injection of ferrous sulfate. J. Plant Nutr. 9, 683-693.

    CAS  Google Scholar 

  • Hurley A K, Walser R H, Davis T D and Barney D L 1986b Net photosynthesis, chlorophyll, and foliar iron in apple trees after injection with ferrous sulfate. HortSci. 21, 1029-1031.

    CAS  Google Scholar 

  • Iturbe-Ormaetxe I, Moran J F, Arrese-Igor C, Gogorcena Y, Klucas R V and Becana M 1995 Activated oxygen and antioxidant defences in iron-deficient pea plants. Plant Cell Environ. 18, 421-429.

    Article  CAS  Google Scholar 

  • Krause G H 1988 Photoinhibition of photosynthesis. An evaluation of damaging and protective mechanisms. Physiol. Plant. 74, 566-574.

    Article  CAS  Google Scholar 

  • Krause G H and Weis E 1991 Chlorophyll fluorescence and photosynthesis: The basics. Ann. Rev. Plant Physiol. Plant Mol. Biol. 42, 313-349.

    Article  CAS  Google Scholar 

  • Laisk A, Oja V, Rasulov B, Eichelmann H and Sumberg A 1997 Quantum yields and rate constants of photochemical and nonphotochemical excitation quenching-Experimental and model. Plant Physiol. 115, 803-815.

    PubMed  CAS  Google Scholar 

  • Lindsay W L 1995 Chemical reactions in soils that affect iron availability to plants. A quantitative approach. In Iron Nutrition in Soils and Plants. Ed. J Abadía. pp 7-14. Kluwer Academic Publishers, Dordrecht.

    Google Scholar 

  • Marschner H 1986 Mineral nutrition of higher plants. Academic Press, London.

    Google Scholar 

  • Masoni A, Ercoli L and Mariotti M 1996 Spectral properties of leaves deficient in iron, sulfur, magnesium and manganese. Agron. J. 88, 937-943.

    Article  CAS  Google Scholar 

  • Miller G W, Jen Huang I, Welkie G W and Pushnik J C 1995 Function of iron in plants with special emphasis on chloroplasts and photosynthetic activity. In Iron Nutrition in Soils and Plants. Ed. J Abadía. pp 19-28. Kluwer Academic Publishers, Dordrecht.

    Google Scholar 

  • Moog P R and Brüggemann W 1995 Iron reductase systems on the plant plasma membrane. A review. Plant Soil 165, 241-260.

    Article  Google Scholar 

  • 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, 607-613.

    PubMed  CAS  Google Scholar 

  • 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, 886-893.

    PubMed  CAS  Google Scholar 

  • 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, 403-412.

    Article  CAS  Google Scholar 

  • Morales F, Belkhodja R, Abadía A 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, 1153-1160.

    Article  CAS  Google Scholar 

  • Morales F, Belkhodja R, Abadía A and Abadía J 1998b Energy dissipation in iron-chlorotic field-grown pear. Submitted.

  • Morales F, Belkhodja R, Abadía A and Abadía J 1998c Photosystem II efficiency and mechanisms of energy dissipation in iron-deficient, field-grown pear trees (Pyrus communis L.). Submitted.

  • Morales F, Grasa R, Abadía A and Abadía J 1998d The iron chlorosis paradox in fruit trees. J. Plant Nutr. 21, 815-825.

    CAS  Google Scholar 

  • 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, 1783-1790.

    CAS  Google Scholar 

  • Pérez C, Val J and Monge E 1995 Effects of iron deficiency on photosynthetic structures in peach (Prunus persica L. Batsch) leaves. In Iron Nutrition in Soils and Plants. Ed. J Abadía. pp 183-189. Kluwer Academic Publishers, Dordrecht.

    Google Scholar 

  • Pushnik J and Miller G 1989 Iron regulation of chloroplast photosynthetic function: mediation of PS I development. J. Plant Nutr. 12, 407-421.

    CAS  Google Scholar 

  • Römheld V 1997 The chlorosis paradox: Fe inactivation in leaves as a secondary event in Fe deficiency chlorosis. In Abstracts 9th International Symposium on Iron Nutrition and Interactions in Plants. pp 10. Hohenheim, Stuttgart.

    Google Scholar 

  • Sanz M, Cavero J and Abadía J 1992 Iron chlorosis in the Ebro river basin, Spain. J. Plant Nutr. 15, 1971-1981.

    CAS  Google Scholar 

  • Schreiber U, Bilger W and Neubauer C 1995 Chlorophyll fluorescence as a nonintrusive indicator for rapid assessment of in vivo photosynthesis. In Ecophysiology of Photosynthesis. Eds. E-D Schulze, M M Caldwell. pp 49-70. Springer-Verlag, Berlin.

    Google Scholar 

  • 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, 121-125.

    PubMed  CAS  Google Scholar 

  • Taylor S E and Terry N 1986 Variation in photosynthetic electron transport capacity and its effect on the light modulation of ribulose bisphosphate carboxilase. Photosynth. Res. 8, 249-256.

    Article  CAS  Google Scholar 

  • Terry N 1980 Limiting factors in photosynthesis. I. Use of iron stress to control photochemical capacity in vivo. Plant Physiol. 65, 114-120.

    PubMed  CAS  Google Scholar 

  • Terry N 1983 Limiting factors in photosynthesis. IV. Iron stress mediated changes in light-harvesting and electron transport capacity and its effects on photosynthesis in vivo. Plant Physiol. 71, 855-860.

    CAS  Google Scholar 

  • Terry N and Abadía J 1986 Function of iron in chloroplasts. J. Plant Nutr. 9, 609-646.

    CAS  Google Scholar 

  • Verhoeven A S, 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, 567-576.

    Article  CAS  Google Scholar 

  • Verhoeven A S, Demmig-Adams B and Adams III W W 1997 Enhanced employment of the xanthophyll cycle and thermal energy dissipation in spinach exposed to high light and N stress. Plant Physiol. 113, 817-824.

    PubMed  CAS  Google Scholar 

  • Welkie G W and Miller G W 1993 Plant iron uptake physiology by nonsiderophore systems. In Iron Chelation in Plants and Soil Microorganisms. Eds L L Barton, B C Hemming. pp 345-370. Academic Press Inc, New York.

    Google Scholar 

  • Winder T L and Nishio J 1995 Early iron deficiency stress response in leaves of sugar beet. Plant Physiol. 108, 1487-1494.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Abadía, J., Morales, F. & Abadía, A. Photosystem II efficiency in low chlorophyll, iron-deficient leaves. Plant and Soil 215, 183–192 (1999). https://doi.org/10.1023/A:1004451728237

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1004451728237

Navigation