Photosynthetica 2005, 43(1):65-74 | DOI: 10.1007/s11099-005-5074-8

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

M. C. Antolín1,*, M. Hekneby1, M. Sánchez-Díaz1
1 Departamento de Fisiología Vegetal, Universidad de Navarra, Pamplona, Spain

Growth, net photosynthetic rate (PN), 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 PN 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 PN 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.

Additional key words: chlorophyll fluorescence; cold acclimation; dry matter accumulation; leaf area ratio; net photosynthetic rate; photosystem 2; specific leaf area; ribulose-1,5-bisphosphate carboxylase, oxygenase; stromal fructose-1,6-bisphosphatase

Received: June 7, 2004; Accepted: August 23, 2004; Published: March 1, 2005  Show citation

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Antolín, M.C., Hekneby, M., & Sánchez-Díaz, M. (2005). Contrasting responses of photosynthesis at low temperatures in different annual legume species. Photosynthetica, 43(1), 65-74. doi: 10.1007/s11099-005-5074-8
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    References

    1. Antolín, M.C., Sánchez-Díaz, M.: Effects of temporary droughts on photosynthesis of alfalfa plants. - J. exp. Bot. 44: 1341-1349, 1993. Go to original source...
    2. 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. Go to original source...
    3. 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. Go to original source...
    4. 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. Go to original source...
    5. 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. Go to original source...
    6. Germino, M.J., Smith, W.K.: High resistance to low-temperature photoinhibition in two alpine snowbank species. - Physiol. Plant. 110: 89-95, 2000. Go to original source...
    7. Griffith, M., McIntyre, H.C.H.: The interrelationship of growth and frost tolerance in winter rye. - Physiol. Plant. 87: 335-344, 1993. Go to original source...
    8. 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. Go to original source...
    9. 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. Go to original source...
    10. 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. Go to original source...
    11. 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. Go to original source...
    12. 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.
    13. 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. Go to original source...
    14. 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. Go to original source...
    15. 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. Go to original source...
    16. 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. Go to original source...
    17. Larcher, W.: Physiological Plant Ecology. - Springer-Verlag, Berlin 2003. Go to original source...
    18. 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. Go to original source...
    19. 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. Go to original source...
    20. 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. Go to original source...
    21. Maxwell, K., Johnson, G.N.: Chlorophyll fluorescence - a practical guide. - J. exp. Bot. 51: 659-668, 2000. Go to original source...
    22. 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.
    23. 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. Go to original source...
    24. Roháçek, K., Barták, M.: Technique of the modulated chlorophyll fluorescence: basic concepts, useful parameters, and some applications. - Photosynthetica 37: 339-363, 1999. Go to original source...
    25. 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. Go to original source...
    26. 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. Go to original source...
    27. 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. Go to original source...
    28. 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. Go to original source...
    29. 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. Go to original source...
    30. 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. Go to original source...
    31. 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. Go to original source...
    32. Streb, P., Shang, W., Feierabend, J., Bligny, R.: Divergent strategies of photoprotection in high-mountain plants. - Planta 207: 313-324, 1998. Go to original source...
    33. 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. Go to original source...
    34. van Kooten, O., Snel, J.F.H.: The use of chlorophyll fluorescence nomenclature in plant stress physiology. - Photosynth.. Res. 25: 147-150, 1990. Go to original source...
    35. 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. Go to original source...

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