Photosynthetica 2013, 51(1):75-84 | DOI: 10.1007/s11099-012-0080-0

Photosynthesis, energy partitioning, and metabolic adjustments of the endangered Cistaceae species Tuberaria major under high temperature and drought

M. L. Osório1,2,*, J. Osório1,2, A. Romano1,2
1 Institute for Biotechnology and Bioengineering, Centre of Genomics and Biotechnology IBB/CGB, Faculty of Sciences and Technology, Ed. 8, University of Algarve, Campus de Gambelas, Faro, Portugal
2 Institute of Mediterranean Agricultural and Environment Sciences ICAAM, Faculty of Sciences and Technology, Ed. 8, University of Algarve, Campus de Gambelas, Faro, Portugal

In view of predicted climatic changes for the Mediterranean region, study of high temperature and drought impacts on physiological responses of endangered species regains relevance. In this context, micropropagated plants of Tuberaria major, a critically endangered species, endemic of Algarve, were transferred to a controlled-environment cabinet with day/night temperatures set at 25/18°C (Reference) or 32/21°C (HT). After 15 days of HT acclimation, some plants were subjected to progressive drought followed by rewatering. The enhancement of temperature alone did not affect water relations and photosynthetic rates (P N) but the stomatal conductance (g s) exhibited a 3-fold increase in comparison with reference plants. The maximum quantum yield of photosystem (PS) II (Fv/Fm), the effective quantum yield of PSII photochemistry (ΦPSII), carotenoid (Car) and anthocyanin content enhanced, whereas the quantum yields of regulated (ΦNPQ) and nonregulated (ΦNO) energy dissipation decreased. Drought combined with HT reduced predawn leaf water potential to values of about -1.3 MPa, which had adverse effects on gas exchange and PSII activity. Values of P N and g s were 71 and 79% lower than those of HT plants. An impairment of photochemical activity was also observed: the decrease in ΦPSII and the increase of ΦNPQ. However, an irreversible photoinhibitory damage had not occurred. Carotenoid and anthocyanin content remained elevated and soluble sugars (SS) increased twice, whereas proline and MDA accumulation was not detected. On the first 24 h after water-stress relief, g s, P N, ΦPSII, and ΦNPQ did not recover, but SS returned to the reference level. Overall, T. major acquired an adequate capacity for a protection against the development of oxidative stress during drought and water recovery under HT. These findings suggest that T. major is prepared to deal with predicted climate changes.

Additional key words: anthocyanins; chlorophyll fluorescence imaging; energy partitioning; malondialdehyde; proline; soluble sugars

Received: June 25, 2012; Accepted: November 6, 2012; Published: March 1, 2013  Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Osório, M.L., Osório, J., & Romano, A. (2013). Photosynthesis, energy partitioning, and metabolic adjustments of the endangered Cistaceae species Tuberaria major under high temperature and drought. Photosynthetica51(1), 75-84. doi: 10.1007/s11099-012-0080-0
Download citation

References

  1. Ashraf, M., Foolad, M.R.: Roles of glycine betaine and proline in improving plant abiotic stress resistance. - Environ. Exp. Bot. 59: 206-216, 2007. Go to original source...
  2. Bates, L.S., Waldren, R.P., Tear, I.D.: Rapid determination of free proline for water stress studies. - Plant Soil 156: 205-207, 1973. Go to original source...
  3. Biehler, K., Fock, H.: Evidence for the contribution of the Mehler-peroxidase reaction in dissipating excess electrons in drought-stressed wheat. - Plant Physiol. 112: 265-272, 1996. Go to original source...
  4. Chalker-Scott, L.: Environmental significance of anthocyanins in plant stress responses. - Photochem. Photobiol. 70: 1-9, 1999. Go to original source...
  5. Chaves, M.M., Flexas, J., Pinheiro, C.: Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. - Ann. Bot. 103: 551-560, 2009. Go to original source...
  6. Chaves, M.M., Osório, M.L., Osório, J., Pereira, J.S.: Nonstomatal limitation of photosynthesis under high temperature and water deficits in Lupinus albus. - Photosynthetica 27: 521-528, 1992.
  7. 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. Go to original source...
  8. Cushman, J.C., Bohnert, H.J.: Genomic approaches to plant stress tolerance. - Curr. Opin. Plant Biol. 3: 117-124, 2000. Go to original source...
  9. David, M.M., Coelho, D., Barrote, I., Correia, M.J.: Leaf age effects on photosynthetic activity and sugar accumulation in droughted and rewatered Lupinus albus plants. - Aust. J. Plant Physiol. 25: 299-306, 1998. Go to original source...
  10. Demmig-Adams, B., Adams, W.W., III: Xanthophyll cycle and light stress in nature: uniform response to excess direct sunlight among higher plant species. - Planta 198: 460-470, 1996. Go to original source...
  11. Epron, D., Dreyer, E.: Effects of severe dehydration on leaf photosynthesis in Quercus petraea (Matt.) Liebl.: photosystem II efficiency, photochemical and nonphotochemical fluorescence quenching and electrolyte leakage. - Tree Physiol. 10: 273-284, 1992. Go to original source...
  12. Ensminger, I., Busch, F., Huner, N.P.A.: Photostasis and cold acclimation: sensing low temperature through photosynthesis. - Physiol. Plant. 126: 28-44, 2006. Go to original source...
  13. Feller, U.: Stomatal open at elevated temperature: an underestimated regulatory mechanism? - Gen. Appl. Plant Physiol. Special Issue: 19-31, 2006.
  14. Frackowiak, D., Smyk, B.: Interactions between photosynthetic pigments in organisms and in model systems. - Photosynthetica 45: 1-8, 2007. Go to original source...
  15. Galmés, J., Abadia, A., Cifre, J., Medrano, H., Flexas, J.: Photoprotection processes under water stress and recovery in Mediterranean plants with different growth forms and leaf habits. - Physiol. Plant. 130: 495-510, 2007. Go to original source...
  16. García-Plazaola, J.I., Olano, J.M., Hernández, A., Becerril, J.M.: Photoprotection in evergreen Mediterranean plants during sudden periods of intense cold weather. - Trees 17: 285-291, 2003. Go to original source...
  17. Genty, B., Harbinson, J., Baker, N.R.: Relative quantum efficiencies of the two photosystems of leaves in photorespiratory and non-photorespiratory conditions. - Plant Physiol. Biochem. 28: 1-10, 1990.
  18. Gonçalves. S., Fernandes, L., Pérez-García, F. et al.: Germination requirements and cryopreservation tolerance of seeds of the endangered species Tuberaria major. - Seed Sci. Technol. 37: 480-484, 2009. Go to original source...
  19. Gonçalves, S., Fernandes, L., Romano A.: High frequency in vitro propagation of the endangered species Tuberaria major. - Plant Cell Tissue Organ Cult. 101: 359-363, 2010. Go to original source...
  20. Gould, K.S., Mckelvie, J., Markham, K.R.: Do anthocyanins function as antioxidants in leaves? Imaging of H2O2 in red and green leaves after mechanical injury. - Plant Cell Environ. 25: 1261-1269, 2002. Go to original source...
  21. Gulías, J., Flexas, J., Abadía, A., Medrano, H.: Photosynthetic responses to water deficit in six Mediterranean sclerophyll species: possible factors explaining the declining distribution of Rhamnus ludovici-salvatoris, an endemic Balearic species. - Tree Physiol. 2: 687-697, 2002. Go to original source...
  22. Hodges, D., DeLong, J.M., Forney, C.F., Prange, R.K.: Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. - Planta 207: 604-611, 1999. Go to original source...
  23. Hormaetxe. K., Esteban, R., Becerril, J.M., García-Plazaola, J.I.: Dynamics of the a-tocopherol pool as affected by external (environmental) and internal (leaf age) factors in Buxus sempervirens leaves. - Physiol. Plant. 125: 333-344, 2005. Go to original source...
  24. Kyparissis, A., Drilias, P., Manetas, Y.: Seasonal fluctuations in photoprotective (xanthophyll cycle) and photoselective (chlorophylls) capacity in eight Mediterranean plant species belonging to two different growth forms. - Aust. J. Plant Physiol. 27: 265-272, 2000. Go to original source...
  25. 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. Go to original source...
  26. Lichtenthaler, H.K.: Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. - Methods Enzymol. 148: 350-382, 1987. Go to original source...
  27. Lu, Z., Chen, J., Percy R.G., Zeiger, E.: Photosynthetic rate, stomatal conductance and leaf area in two cotton species (Gossypium barbadense and Gossypium hirsutum) and their relation with heat resistance and yield. - Aust. J. Plant Physiol. 24: 693-700, 1997. Go to original source...
  28. 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. Go to original source...
  29. Mancinelli, A.L.: Photoregulation of anthocyanin synthesis: VIII. Effects of light pretreatments. - Plant Physiol. 75: 447-453, 1984. Go to original source...
  30. Mittler, R.: Abiotic stress, the field environment and stress combination. - Trends Plant Sci. 11: 15-19, 2006. Go to original source...
  31. Munné-Bosch, S., Jubany-Marí, T., Alegre, L.: Enhanced photo- and antioxidative protection, and hydrogen peroxide accumulation in drought-stressed Cistus clusii and Cistus albidus plants. - Tree Physiol. 23: 1-12, 2003. Go to original source...
  32. Ort, D.R.: When there is too much light. - Plant Physiol. 125: 29-32, 2001. Go to original source...
  33. Osborne, C.P., Mitchell, O.L., Sheehy, J.E., Woodward, F.I.: Modelling the recent historical impacts of atmospheric CO2 climate change on Mediterranean vegetation. - Global Change Biol. 6: 445-458, 2000. Go to original source...
  34. Osório, M.L., Osório, J., Vieira, A.C., Gonçalves, S., Romano, A.: 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. Go to original source...
  35. 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. Go to original source...
  36. 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. Go to original source...
  37. Rizhsky, L., Liang, H., Shumanm, J., Shulaev, V., Davletova, S., Mittler, R.: When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. - Plant Physiol. 134: 1683-1696, 2004. Go to original source...
  38. Shulaev, V., Cortes, D., Miller, G., Mittler, R.: Metabolomics for plant stress response. - Physiol. Plant. 32: 199-208, 2008. Go to original source...
  39. Sperdouli, I., Moustakas, M.: Interaction of proline, sugars, and anthocyanins during photosynthetic acclimation of Arabidopsis thaliana to drought stress. - J. Plant Physiol. 169: 577-585, 2012. Go to original source...
  40. Szabados, L., Savouré, A.: Proline: a multifunctional amino acid. - Trends Plant Sci. 15: 89-97, 2010. Go to original source...
  41. Wahid, A.: Physiological implications of metabolite biosynthesis for net assimilation and heat-stress tolerance of sugarcane (Saccharum officinarum) sprouts. - J. Plant Res. 120: 219-228, 2007. Go to original source...
  42. Wang, Z., Huang, B.: Physiological recovery of Kentucky bluegrass from simultaneous drought and heat stress. - Crop Sci. 44: 1729-1736, 2004. Go to original source...
  43. Weber, H., Chételat, A., Reymond, P., Farmer, E.E.: Selective and powerful stress gene expression in Arabidopsis in response to malondialdehyde. - Plant J. 37: 877-888, 2004. Go to original source...
  44. Wingler, A., Quick, W.P., Bungard, R.A. et al.: The role of photorespiration during drought stress: an analysis utilizing barley mutants with reduced activities of photorespiratory enzymes. - Plant Cell Environ. 22: 361-373, 1999. Go to original source...
  45. Yamamoto, Y., Aminaka, R., Yoshioka, M., Khatoon, M., Komayama, K., Takenaka, D., et al.: Quality control of photosystem II: impact of light and heat stresses. - Photosynth. Res. 98: 589-608, 2008. Go to original source...