Skip to main content
Log in

Contrasting responses of photosynthesis at low temperatures in different annual legume species

  • Published:
Photosynthetica

Abstract

Growth, net photosynthetic rate (P N), chlorophyll fluorescence induction kinetics, and stromal fructose-1,6-bisphosphatase (sFBPase) in annual legumes native to the Mediterranean region, two clovers (Trifolium subterraneum L. ssp. oxaloides Nyman cv. Clare and T. michelianum Savi cv. Giorgia) and two Medicago species (M. polymorpha L. cv. Anglona and M. truncatula Gaertn. cv. Paraggio), shifted from 20 to 10 °C for 1 d or developed at 10 °C were compared with controls kept at 20 °C. Cold development produced a larger stimulation of growth in the clover cv. Giorgia and the Medicago cv. Paraggio. Transferring plants to low temperatures affected P N relatively less in clovers than in Medicago plants. Development at 10 °C relieved the inhibition of photosynthesis in Giorgia and Paraggio, but not in Clare and Anglona, which correlated with increases in the maximum rate of carboxylation by ribulose-1,5-bisphosphate carboxylase/oxygenase, RuBPCO (Vcmax), and the photon-saturated rate of electron transport (Jmax). In Medicago, transfer from high to low temperature inhibited photosynthesis in a lesser extent in Anglona than in Paraggio, which showed severe limitations at level of Vcmax and Jmax. Development at 10 °C in Paraggio produced an efficient photosynthetic cold acclimation, this being associated with a two-fold increase of quantum yield of photosystem 2 electron transport (ΔF/F'm) and with the activity of sFBPase. By contrast, Anglona showed an irreversible inhibition of P N coupled with the reduction of carbon metabolism by impairment of Calvin cycle enzyme activities such as RuBPCO and sFBPase, resulting in a poor cold acclimation of photosynthesis in this cultivar.

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

  • Antolín, M.C., Sánchez-Díaz, M.: Effects of temporary droughts on photosynthesis of alfalfa plants. — J. exp. Bot. 44: 1341–1349, 1993.

    Google Scholar 

  • Boese, S.R., Huner, N.P.A.: Effect of growth temperature and temperature shifts on spinach leaf morphology and photosynthesis. — Plant Physiol. 94: 1830–1836, 1990.

    Google Scholar 

  • Bradford, M.M.: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. — Anal. Biochem. 72: 248–254, 1976.

    Google Scholar 

  • García-Plazaola, J.I., Artetxe, U., Becerril, J.M.: Diurnal changes in antioxidant and carotenoid composition in the Mediterranean sclerophyll tree Quercus ilex (L.) during winter. — Plant Sci. 143: 125–133, 1999.

    Google Scholar 

  • Genty, B., Briantais, J.-M., Baker, N.R.: The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. — Biochim. biophys. Acta 99: 87–92, 1989.

    Google Scholar 

  • Germino, M.J., Smith, W.K.: High resistance to low-temperature photoinhibition in two alpine snowbank species. — Physiol. Plant. 110: 89–95, 2000.

    Google Scholar 

  • Griffith, M., McIntyre, H.C.H.: The interrelationship of growth and frost tolerance in winter rye. — Physiol. Plant. 87: 335–344, 1993.

    Google Scholar 

  • Guy, C.L., Huber, J.L.A., Huber, S.C.: Sucrose phosphate synthase and sucrose accumulation at low temperature. — Plant Physiol. 100: 502–508, 1992.

    Google Scholar 

  • Holaday, A.S., Martindale, W., Alred, R., Brooks, A.L., Leegood, R.C.: Changes in activities of enzymes of carbon metabolism in leaves during exposure of plants to low temperature. — Plant Physiol. 98: 1105–1114, 1992.

    Google Scholar 

  • Huner, N.P.A., Elfman, B., Krol, M., McIntosh, A.: Growth and development at cold-hardening temperatures. Chloroplast ultrastructure, pigment content, and composition. — Can. J. Bot. 62: 53–60, 1984.

    Google Scholar 

  • Huner, N.P.A., Öquist, G., Hurry, V.M., Krol, M., Falk, S., Griffith, M.: Photosynthesis, photoinhibition and low temperature acclimation in cold tolerant plants. — Photosynth. Res. 37: 19–39, 1993.

    Google Scholar 

  • Hurry, V., Huner, N., Selstam, E., Gardeström, P., Öquist, G.: Photosynthesis at low growth temperatures. — In: Raghavendra, A.S. (ed.): Photosynthesis. A Comprehensive Treatise. Pp. 238–249. Cambridge University Press, Cambridge 1998.

    Google Scholar 

  • Hurry, V., Strand, Å., Furbank, R., Stitt, M.: The role of inorganic phosphate in the development of freezing tolerance and the acclimatization of photosynthesis to low temperature is revealed by the pho mutants of Arabidopsis thaliana. — Plant J. 24: 383–396, 2000.

    Google Scholar 

  • Hurry, V.M., Gardeström, P., Öquist, G.: Reduced sensitivity to photoinhibition following frost-hardening of winter rye is due to increased phosphate availability. — Planta 190: 484–490, 1993.

    Google Scholar 

  • Hurry, V.M., Keerberg, O., Pärnik, T., Gardeström, P., Öquist, G.: Cold-hardening results in increased activity of enzymes involved in carbon metabolism in leaves of winter rye (Secale cereale L.). — Planta 195: 554–562, 1995a.

    Google Scholar 

  • Hurry, V.M., Strand, A., Tobiaeson, M., Gardeström, P., Öquist, G.: Cold hardening of spring and winter wheat and rape results in differential effects on growth, carbon metabolism, and carbohydrate content. — Plant Physiol. 109: 697–706, 1995b.

    Google Scholar 

  • Larcher, W.: Physiological Plant Ecology. — Springer-Verlag, Berlin 2003.

    Google Scholar 

  • Leonardos, E.D., Savitch, L.V., Huner, N.P.A., Öquist, G., Grodzinski, B.: Daily photosynthetic and C-export patterns in winter wheat leaves during cold stress and acclimation. — Physiol. Plant. 117: 521–531, 2003.

    Google Scholar 

  • Lichtenthaler, H.K.: Chlorophylls and carotenoids — pigments of photosynthetic biomembranes. — In: Colowick, S.P., Kaplan, N.O. (ed.): Methods in Enzymology. Vol. 148. Pp. 350–382. Academic Press, San Diego — New York — Berkeley — Boston — London — Sydney — Tokyo — Toronto 1987.

    Google Scholar 

  • Lichtenthaler, H.K., Bu schmann, C.: Chlorophylls and carotenoids: Measurement and characterization by UV-VIS spectroscopy. — In: Current Protocols in Food Analytical Chemistry (CPFA) (Supplement 1) unit F4.3.1–F4.3.8. John Willey, New York 2001.

    Google Scholar 

  • Maxwell, K., Johnson, G.N.: Chlorophyll fluorescence — a practical guide. — J. exp. Bot. 51: 659–668, 2000.

    Google Scholar 

  • Oliveira, G., Peñuelas, J.: Allocation of absorbed light energy into photochemistry and dissipation in a semi-decidous and an evergreen Mediterranean woody species during winter. — Aust. J. Plant Physiol. 28: 471–480, 2001.

    Google Scholar 

  • Pérez, P., Morcuende, R., Martín del Molino, I., Sánchez de la Puente, L., Martí nez-Carrasco, R.: Contrasting responses of photosynthesis and carbon metabolism to low temperatures in tall fescue and clovers. — Physiol. Plant. 112: 478–486, 2001.

    Google Scholar 

  • Roháçek, K., Barták, M.: Technique of the modulated chlorophyll fluorescence: basic concepts, useful parameters, and some applications. — Photosynthetica 37: 339–363, 1999.

    Google Scholar 

  • Savitch, L.V., Barker-Astrom, J., Ivanov, A.G., Hurry, V., Öquist, G., Huner, N.P.A., Gardeström, P.: Cold acclimation of Arabidopsis thaliana results in incomplete recovery of photosynthetic capacity, associated with an increased reduction of the chloroplast stroma. — Planta 214: 295–303, 2001.

    Google Scholar 

  • Savitch, L.V., Harney, T., Huner, N.P.A.: Sucrose metabolism in spring and winter wheat in response to high irradiance, cold stress and cold acclimation. — Physiol. Plant. 108: 270–278, 2000a.

    Google Scholar 

  • Savitch, L.V., Massacci, A., Gray, G.R., Huner, N.P.A.: Acclimation to low temperature or high light mitigates sensitivity to photoinhibition: roles of the Calvin cycle and the Mehler reaction. — Aust. J. Plant Physiol. 27: 253–264, 2000b.

    Google Scholar 

  • Stitt, M., Grosse, H.: Interactions between sucrose synthesis and CO2 fixation. IV. Temperature-dependent adjustment of the relation between sucrose synthesis and CO2 fixation. — J. Plant Physiol. 133: 392–400, 1988.

    Google Scholar 

  • Stitt, M., Hurry, V.: A plant for all seasons: alterations in photosynthetic carbon metabolism during cold acclimation in Arabidopsis. — Curr. Opin. Plant Biol. 5: 199–206, 2002.

    Google Scholar 

  • Strand, Å., Foyer, C.H., Gustafsson, P., Gardeström, P., Hurry, V.: Altering flux through the sucrose biosynthesis pathway in transgenic Arabidopsis thaliana modifies photosynthetic acclimation at low temperatures and the development of freezing tolerance. — Plant Cell Environ. 26: 523–535, 2003.

    Google Scholar 

  • Strand, Å., Hurry, V., Henkes, S., Huner, N., Gustafsson, P., Gardeström, P., Stitt, M.: Acclimation of Arabidopsis leaves developing at low temperatures. Increasing cytoplasmic volume accompanies increased activities of enzymes in the Calvin cycle and in the sucrose-biosynthesis pathway. — Plant Physiol. 119: 1387–1397, 1999.

    Google Scholar 

  • Streb, P., Shang, W., Feierabend, J., Bligny, R.: Divergent strategies of photoprotection in high-mountain plants. — Planta 207: 313–324, 1998.

    Google Scholar 

  • Sultan, K., Gintzburger, G., Obaton, M., Robin, C., Touchane, H., Guckert, A.: Growth and nitrogen fixation of annual Medicago-Rhizobium associations during winter in Mediterranean region. — Eur. J. Agron. 15: 221–229, 2001.

    Google Scholar 

  • van Kooten, O., Snel, J.F.H.: The use of chlorophyll fluorescence nomenclature in plant stress physiology. — Photosynth.. Res. 25: 147–150, 1990.

    Google Scholar 

  • Verhoeven, A.S., Adams, W.W., III, Demmig-Adams, B.: Close relationship between the state of the xanthophyll cycle pigments and photosystem II efficiency during recovery from winter stress. — Physiol. Plant. 96: 567–576, 1996.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to M. C. Antolín.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Antolín, M.C., Hekneby, M. & Sánchez-Díaz, M. Contrasting responses of photosynthesis at low temperatures in different annual legume species. Photosynthetica 43, 65–74 (2005). https://doi.org/10.1007/s11099-005-5074-8

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11099-005-5074-8

Additional key words

Navigation