Abstract
Predicted future climatic changes for the Mediterranean region give additional importance to the study of photooxidative stress in local economic species subjected to combined drought and high-temperature conditions. Under this context, the impact of these stresses on photosynthesis, energy partitioning, and membrane lipids, as well as the potential ability to attenuate oxidative damage, were investigated in Ceratonia siliqua L. Two thermal regimes (LT: 25/18°C; HT: 32/21°C) and three soil water conditions (control, water stress, and rewetting) were considered. HT exacerbated the adverse effects of water shortage on photosynthetic rates (P N) and PSII function. The decrease in P N was 33% at LT whereas at HT it was 84%. In spite of this, the electron transport rate (ETR) was not affected, which points to an increased allocation of reductants to sinks other than CO2 assimilation. Under LT conditions, water stress had no significant effects on yield of PSII photochemistry (ΦPSII) and yields of regulated (ΦNPQ) and nonregulated (ΦNO) energy dissipation. Conversely, drought induced a significant decrease of ΦPSII and a concomitant increase of ΦNO in HT plants, thereby favouring the overproduction of reactive oxygen species (ROS). Moreover, signs of lipid peroxidation damage were detected in HT plants, in which drought caused an increase of 40% in malondialdehyde (MDA) content. Concurrently, a marked increase in proline content was observed, while the activities of catalase (CAT) and ascorbate peroxidase (APX) were unaffected. Despite the generation of a moderate oxidative stress response, C. siliqua revealed a great capability for photosynthetic recovery 36 h after rewatering, which suggests that the species can cope with predicted climate change.
Similar content being viewed by others
Abbreviations
- APX:
-
ascorbate peroxidase
- C i :
-
substomatal CO2 concentration
- Cars:
-
carotenoids
- CAT:
-
catalase
- Chl:
-
chlorophyll
- ETR:
-
apparent linear electron transport rate
- Fv/Fm :
-
maximum PSII photochemical efficiency
- g s :
-
stomatal conductance
- HT:
-
32/21°C
- LT:
-
25/18°C
- MDA:
-
malondialdehyde
- NPQ:
-
nonphotochemical quenching
- P N :
-
net photosynthetic rate
- PPFD:
-
photosynthetic photon flux density
- PSII:
-
photosystem II
- ROS:
-
reactive oxygen species
- RWC:
-
relative water content
- WS:
-
water-stressed plants
- WW:
-
well watered plants
- Ψw :
-
leaf water potential
- ΦNO :
-
quantum yield of nonregulated energy dissipation of PSII
- ΦNPQ :
-
quantum yield of regulated energy dissipation of PSII
- ΦPSII :
-
actual PSII quantum yield
References
Aebi, H.: Catalase in vitro: — In: H. Bergmeyer (ed.): Methods of Enzymatic Analysis. Pp. 273–277. Verlag Chemie, Weinheim 1983.
Ashraf, M., Foolad M.R.: Roles of glycine betaine and praline in improving plant abiotic stress resistance. — Environ. Exp. Bot. 59: 206–216, 2007.
Baker, N.R.: A possible role for photosystem II in environmental perturbations of photosynthesis. — Physiol. Plant. 81: 563–570, 1991.
Bates, L.S., Waldren, R.P., Tear, I.D.: Rapid determination of free proline for water stress studies. — Plant Soil 39: 205–207, 1973.
Berry, J., Björkman, O.: Photosynthetic response and adaptation to temperature in higher plants. — Annu. Rev. Plant Physiol. 31: 491–543, 1980.
Boyer, J.S.: Plant productivity and environment. — Science 218: 443–448, 1982.
Bradford, M.M.: A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. — Anal. Biochem. 72: 248–254, 1976.
Cechin, I., Rossi, S.C., Oliveira, V.C., Fumis, T.F.: Photosynthetic responses and proline content of mature and young leaves of sunflower plants under water deficit. — Photosynthetica 44: 143–146, 2006.
Chartzoulakis, K., Psarras, G.: Global change effects on crop photosynthesis and production in Mediterranean: the case of Crete, Greece. — Agr. Ecosyst. Environ. 106: 147–157, 2005.
Chaves, M.M., Pereira, J.S., Maroco, J., Rodrigues, M.L., Ricardo, C.P.P., Osório, M.L., Carvalho, I., Faria, T., Pinheiro, C.: How plants cope with water stress in the field: photosynthesis and growth. — Ann. Bot. 89: 907–916, 2002.
Cornic, G.: Drought stress inhibits photosynthesis by decreasing stomatal aperture — not by affecting ATP synthesis. — Trends Plant Sci. 5: 187–188, 2000.
Correia, M.J., Osório M.L., Osório J., Barrote I., Martins M., David M.M.: Influence of transient shade periods on the effects of drought on photosynthesis, carbohydrate accumulation and lipid peroxidation in sunflower leaves. — Environ. Exp. Bot. 58: 75–84, 2006.
Costa, A.C., Pinheiro, B.G, Cordeiro, E.S., Shimizu, F.T., Santos-Filho, B.,G., Moraes, F.K.C., Figueiredo, D.M.: Lipid peroxidation, chloroplastic pigments and antioxidant strategies in Carapa guianensis (Aubl.) subjected to waterdeficit and short-term rewetting. — Trees 24: 275–283, 2010.
Downton, W.J.S., Loveys, B.R., Grant, W.J.R.: Non-uniform stomatal closure induced by water stress causes putative nonstomatal inhibition of photosynthesis. — New Phytol. 110: 503–509, 1988.
Feng, Z., Jin-Kui, G., Ying-Li, Y., Wen-Liang, H., Li-Xin, Z.: Changes in the pattern of antioxidant enzymes in wheat exposed to water deficit and rewatering. — Acta Physiol. Plant. 26: 345–352, 2004.
Flexas, J., Escalona, J.M., Medrano, H.: Down-regulation of photosynthesis by drought under field conditions in grapevine leaves. — Aust. J. Plant Physiol. 25: 893–900, 1998.
Flexas, J., Medrano, H.: Drought-inhibition of photosynthesis in C3 plants: stomatal and non-stomatal limitations revisited. — Ann. Bot. 89: 183–189, 2002.
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 990: 87–92, 1989.
Guo, Z., Ou, W., Lu, S., Zhong, Q.: Differential responses of antioxidative system to chilling and drought in four rice cultivars differing in sensitivity. — Plant Physiol. Biochem. 44: 828–836, 2006.
Hare, P.D., Cress, W.A.: Metabolic implications of stress induced proline accumulation in plants. — Plant Growth Regul. 21: 79–102, 1997.
Hodges, D., DeLong, J.M., Forney, C.F., Prange, R.K.: Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidationin plant tissues containing anthocyanin and other interfering compounds. — Planta 207: 604–611, 1999.
Houghton, J.T, Ding, Y., Griggs, D.J, Noguer, M., van der Linden, P.J., Dai, X., Maskell, K., Johnson, C.A.: IPCC Report on Climate Change 2001: The Scientific Basis. — Cambridge University Press, New York 2001.
Mc Arthy, J.J., Canziani, O.F., Leary, N.A., Dokken, D.J., White, K.S. (ed.): IPCC: Climate Change 2001: Impacts, Adaptation and Vulnerability. — Cambridge University Press, Cambridge 2001.
Jiang, M.Y., Zhang, J.H.: Water stress-induced abscisic acid accumulation triggers the increased generation of reactiveoxygen species and up-regulates the activities of antioxidant enzymes in maize leaves. — J. Exp. Bot. 53: 2401–2410, 2002.
Kramer, D.M., Johnson, G., Kiirats, O., Edwards, G.E.: New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. — Photosynth. Res. 79: 209–218, 2004.
Lawlor, D.W.: The effects of water deficit on photosynthesis. — In: Smirnoff, N. (ed.): Environment and Plant Metabolism, Flexibility and Acclimation. Pp. 129–160. BIOS Scientific Publishers, Oxford 1995.
Lichtenthaler, H.K.: Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. — Meth. Enzymol. 148: 350–382, 1987.
Lo Gullo, M.A., Salleo, S.: Different strategies of drought resistance in three Mediterranean sclerophyllous trees growing in the same environmental conditions. — New Phytol. 108: 267–276, 1988.
Machado, S., Paulsen, G.M.: Combined effects of drought and high temperature on water relations of wheat and sorghum. — Plant Soil 233: 179–187, 2001.
Magné, C., Larher, F.: Higher sugar content of extracts interferes with the colorimetric determination of amino acids and free proline. — Anal. Biochem. 200: 115–118, 1992.
Massacci, A., Nabiev, S.M., Pietrosanti, L., Nematov, S.K., Chernikova, T.N., Thor, K., Leipner, J.: Response of the photosynthetic apparatus of cotton (Gossypium hirsutum) to the onset of drought stress under field conditions studied by gas-exchange analysis and chlorophyll fluorescence imaging. — Plant Physiol. Biochem. 46: 189–195, 2008.
Mott, K.A., Buckley, T.N.: Patchy stomatal conductance: emergent collective behaviour of stomata. — Trends Plant Sci. 5: 258–262, 2000.
Nakano, Y., Asada, K.: Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. — Plant Cell Physiol. 22: 867–880, 1981.
Nunes, M.A., Ramalho, J.D.C., Rijo, P.S.: Seasonal changes in some photosynthetic properties of Ceratonia siliqua (carob tree) leaves under natural conditions. — Physiol. Plant. 86: 381–387, 1992.
Osório, M.L., Breia, E., Rodrigues, A., Osório, J., Le Roux, X., Daudet, F.A., Ferreira, I., Chaves, M.M.: Limitations to carbon assimilation by mild drought in nectarine trees growing under field conditions. — Environ. Exp. Bot. 55: 235–247, 2006.
Oxborough, K., Baker, N.R.: Resolving chlorophyll a fluorescence images of photosynthetic efficiency into photochemical and non-photochemical components — calculation of qP and Fv’/Fm’ without measuring Fo’. — Photosynth. Res. 54: 135–142, 1997.
Petsas, A., Grammatikopoulos, G.: Drought resistance and recovery of photosystem II activity in a Mediterranean semideciduous shrub at the seedling stage. — Photosynthetica 47: 284–292, 2009.
Ramalho, J.C., Lauriano, J.A., Nunes, M.A.: Changes in photosynthetic performance of Ceratonia siliqua in summer. — Photosynthetica 38: 393–396, 2000.
Savitch, L.V., Ivanov, A.G., Gudynaite-Savitch, L., Huner, N.P.A., Simmonds, J.: Effect of low temperature stress on excitation energy partitioning and photoprotection in Zea Mays. — Funct. Plant Biol. 36: 37–49, 2009.
Smirnoff, N.: Tansley review.52. The role of active oxygen in the response of plants to water deficit and desiccation. — New Phytol. 125: 27–58, 1993.
Szabados, L., Savouré, A.: Proline: a multifunctional amino acid. — Trends Plant Sci. 15: 89–97, 2010.
Szyszka, B., Ivanov, A.G., Huner, N.P.A.: Psychrophily is associated with differential energy partitioning, photosystem stoichiometry and polypeptide phosphorylation in Chlamydomonas raudensis. — Biochim. Biophys. Acta — Bioenergetics 1767: 789–800, 2007.
Wang, L-J., Loescher, W., Duan, W., Li, W-D., Yang, S-H., Li, S-H.: Heat acclimation induced acquired heat tolerance and cross adaptation in different grape cultivars: relationships to photosynthetic energy partitioning. — Funct. Plant Biol. 36: 516–526, 2009.
Wilson, K.E., Ivanov, A.G., Öquist, G., Grodzinski, B., Sarhan, F., Huner, N.P.A: Energy balance, organellar redox status and acclimation to environmental stress. — Can. J. Bot. 84: 1355–1370, 2006.
Yordanov, I., Velikova, V., Tsonev, T.: Plant responses to drought, acclimation, and stress tolerance. — Photosynthetica 38: 171–186, 2000.
Acknowledgements
This work was supported by a grant from Portuguese Foundation for Science and Technology (FCT) to MLO: SFRH/BPD/35410/2007.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Osório, M.L., Osório, J., Vieira, A.C. et al. Influence of enhanced temperature on photosynthesis, photooxidative damage, and antioxidant strategies in Ceratonia siliqua L. seedlings subjected to water deficit and rewatering. Photosynthetica 49, 3–12 (2011). https://doi.org/10.1007/s11099-011-0001-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11099-011-0001-7