Photosynthetica 2019, 57(3):875-889 | DOI: 10.32615/ps.2019.090

Carbon assimilation in oak (Quercus spp.) populations under acute and chronic high-temperature stress

R. HORAK1,†, M. ŽUPUNSKI2,†, S. PAJEVIĆ2, M. BORIŠEV2, D. ARSENOV2, N. NIKOLIĆ2, S. ORLOVIĆ3
1 University of Novi Sad, Hungarian Language Teacher Training Faculty in Subotica, Serbia
2 University of Novi Sad, Faculty of Sciences, Department of Biology and Ecology, Serbia
3 University of Novi Sad, Institute of Lowland Forestry and Environment, Novi Sad, Serbia

This study tried to evaluate the influence of high temperatures (HT) on carbon assimilation of two oak species (Quercus cerris and Quercus robur). The screening of their populations, which are assumed to have a different resistance and acclimatization potential to adverse environmental conditions, can provide essential information for its implementation in reforestation strategies. By employing principal component analysis, the aim was to determine the most variable physiological characteristics of plants exposed to extremely HT during vegetation periods. After 2 d of HT treatment, a significant decline of photosynthetic and transpiration rates, and stomatal conductance were observed in plants of all investigated populations. The decrease of photosynthetic parameters after 2 d of HT treatment was regulated by the stomatal closure which caused the limitation of CO2 assimilation. Contrary, a chronic HT stress led to an increase in gs and inhibition of photosynthesis at the level of carboxylation.

Keywords: fluorescence; gas exchange; heat stress; Random Forest analysis; water-use efficiency.

Received: September 12, 2018; Accepted: April 23, 2019; Prepublished online: July 12, 2019; Published: July 23, 2019Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
HORAK, R., ŽUPUNSKI, M., PAJEVIĆ, S., BORIŠEV, M., ARSENOV, D., NIKOLIĆ, N., & ORLOVIĆ, S. (2019). Carbon assimilation in oak (Quercus spp.) populations under acute and chronic high-temperature stress. Photosynthetica, 57(3), 875-889. doi: 10.32615/ps.2019.090.
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)

    • Open full article

    Supplementary files

    Download file2041fig 8 S.pdf

    File size: 196.47 kB

    Download file2041fig 6 S.pdf

    File size: 317.83 kB

    Download file2041fig 7 S.pdf

    File size: 301.63 kB

    Download file2041Table S.pdf

    File size: 857.91 kB

    Download file2041 supplementary material.pdf

    File size: 1.45 MB

    References

    1. Anjum S.A., Wang L., Farooq M. et al.: Methyl jasmonate-induced alteration in lipid peroxidation, antioxidative defence system and yield in soybean under drought. - J. Agron. Crop Sci. 197: 296-301, 2011. Go to original source...
    2. Arena C., Vitale L., Virzo de Santo A.: Photosynthesis and photoprotective strategies in Laurus nobilis L. and Quercus ilex L. under summer drought and winter cold. - Plant Biosyst. 142: 472-479, 2008. Go to original source...
    3. Asada K.: Production and scavenging of reactive oxygen species in chloroplasts and their functions. - Plant Physiol. 141: 391-396, 2006. Go to original source...
    4. Avola G., Cavallaro V., Patanè C., Riggi E.: Gas exchange and photosynthetic water use efficiency in response to light, CO2 concentration and temperature in Vicia faba. - J. Plant Physiol. 165: 796-804, 2008. Go to original source...
    5. Balouchi H.R.: Screening wheat parents of mapping population for heat and drought tolerance, detection of wheat genetic variation. - Int. J. Biol. Life Sci. 6: 56-66, 2010.
    6. Banković S., Medarević M., Pantić D. et al.: [National Inventory of Republic of Serbia Forests - Forest Fond of Republic of Serbia.] Ministry of Agriculture, Forestry and Water Management of Republic of Serbia, Belgrade 2009. [In Serbian]
    7. Barr D.J., Levy R., Scheepers C., Tily H.J.: Random effects structure for confirmatory hypothesis testing: Keep it maximal. - J. Mem. Lang. 68: 255-278, 2013. Go to original source...
    8. Bates L.S.: Rapid determination of free proline for water stress studies. - Plant Soil 39: 205-207, 1973. Go to original source...
    9. Battipaglia G., De Micco V., Brand W.A. et al.: Drought impact on water use efficiency and intra-annual density fluctuations in Erica arborea on Elba (Italy). - Plant Cell Environ. 37: 382-391, 2014. Go to original source...
    10. Benavides R., Escudero A., Coll L. et al.: Recruitment patterns of four tree species along elevation gradients in Mediterranean mountains: not only climate matters. - Forest Ecol. Manag. 360: 287-296, 2016. Go to original source...
    11. Ben-Rouina B., Ben-Ahmed C., Athar H.U.R., Boukhriss M.: Water relations, proline accumulation and photosynthetic activity in olive tree (Olea europaea L. cv "Chemlali") in response to salt stress. - Pak. J. Bot. 38: 1397-1406, 2006.
    12. Berry J., Björkman O.: Photosynthetic response and adaptation to temperature in higher plants. - Annu. Rev. Plant Phys. 31: 491-543, 1980. Go to original source...
    13. Borišev M., Horak R., Pajević S. et al.: Daily dynamics of photo-synthetic parameters in beech population under periodical drought conditions. - Open Life Sci. 10: 165-174, 2015.
    14. Breiman L., Friedman J.H., Olshen R.A., Stone C.J.: Classification and Regression Trees. The Wadsworth and Brooks-Cole Statistics-Probability Series. Pp. 368. CRC Press, Boca Raton 1984.
    15. Breiman L.: Random forests. - Mach. Learn. 45: 5-32, 2001. Go to original source...
    16. Brestič M., Živčák M.: PSII fluorescence techniques for measure-ment of drought and high temperature stress signal in plants: protocols and applications. - In: Rout G.R., Das A.B. (ed.): Molecular Stress Physiology of Plants. Pp. 87-131. Springer, Dordrecht 2013. Go to original source...
    17. Camejo D., Jiménez A., Alarcón J.J. et al.: Changes in photosynthetic parameters and antioxidant activities following heat-shock treatment in tomato plants. - Funct. Plant Biol. 33: 177-187, 2006. Go to original source...
    18. Camejo D., Rodríguez P., Morales M.A. et al.: High temperature effects on photosynthetic activity of two tomato cultivars with different heat susceptibility. - J. Plant Physiol. 162: 281-289, 2005. Go to original source...
    19. Canavar Ö., Götz K.P., Ellmer F. et al.: Determination of the relationship between water use efficiency, carbon isotope discrimination and proline in sunflower genotypes under drought stress. - Aust. J. Crop Sci. 8: 232-242, 2014.
    20. Chai Y., Zhang W., Yue M. et al.: Leaf traits suggest different ecological strategies for two Quercus species along an altitu-dinal gradient in the Qinling Mountains. - J. For. Res.-Jpn. 20: 501-513, 2015.
    21. Challinor A.J., Wheeler T.R., Craufurd P.Q., Slingo J.M.: Simula-tion of the impact of high temperature stress on annual crop yields. - Agr. Forest Meteorol. 135: 180-189, 2005. Go to original source...
    22. Condon A.G., Richards R.A., Rebetzke G.J., Farquhar G.D.: Improving intrinsic water-use-efficiency and crop yield. - Crop Sci. 42: 122-131, 2002. Go to original source...
    23. Correia B., Rodriguez J.L., Valledor L. et al.: Analysis of the expression of putative heat-stress related genes in relation to thermotolerance of cork oak. - J. Plant Physiol. 171: 399-406, 2014. Go to original source...
    24. Crafts-Brandner S.J., Salvucci M.E.: Rubisco activase constrains the photosynthetic potential of leaves at high temperature and CO2. - P. Natl. Acad. Sci. USA 97: 13430-13435, 2000. Go to original source...
    25. Crafts-Brandner S.J., Salvucci M.E.: Sensitivity of photosynthesis in a C4 plant, maize, to heat stress. - Plant Physiol. 129: 1773-1780, 2002. Go to original source...
    26. Craufurd P.Q., Wheeler T.R., Ellis R.H. et al.: Effect of temperature and water deficit on water-use efficiency, carbon isotope discrimination, and specific leaf area in peanut. - Crop Sci. 39: 136-142, 1999. Go to original source...
    27. Cui L., Li J., Fan Y. et al.: High temperature effects on photosynthesis, PSII functionality and antioxidant activity of two Festuca arundinacea cultivars with different heat susceptibility. - Bot. Stud. 47: 61-69, 2006.
    28. Daas C., Montpied P., Hanchi B., Dreyer E.: Responses of photosynthesis to high temperatures in oak saplings assessed by chlorophyll-a fluorescence: inter-specific diversity and temperature-induced plasticity. - Ann. For. Sci. 65: 305, 2008. Go to original source...
    29. Dhyani K., Ansari M.W., Rao Y.R. et al.: Comparative physio-logical response of wheat genotypes under terminal heat stress. - Plant Signal. Behav. 8: e24564, 2013. Go to original source...
    30. Di Filipo A., Alessandrini A., Biondi F. et al.: Climate change and oak growth decline: Dendroecology and stand productivity of Turkey oak (Quercus cerris L.) old stored coppice in Central Italy. - Ann. For. Sci. 67: 706, 2010. Go to original source...
    31. Dickson R.E., Tomlinson P.T.: Oak growth, development and carbon metabolism in response to water stress. - Ann. For. Sci. 53: 181-196, 1996. Go to original source...
    32. Epron D., Dreyer E.: Long-term effects of drought on photo-synthesis of adult oak trees [Quercus petraea (Matt.) Liebl. and Quercus robur L.] in a natural stand - New Phytol. 125: 381-389, 1993. Go to original source...
    33. Farhad M., Babak A.M., Reza Z.M. et al.: Response of proline, soluble sugars, photosynthetic pigments and antioxidant enzymes in potato (Solanum tuberosum L.) to different irriga-tion regimes in greenhouse condition. - Aust. J.Crop Sci. 5: 55-60, 2011.
    34. Feng X.: Trends in intrinsic water-use efficiency of natural trees for the past 100-200 years: a response to atmospheric CO2 concentration. - Geochim. Cosmochim. Ac. 63: 1891-1903, 1999.
    35. Filella I., Wilkinson M.J., Llusià J. et al.: Volatile organic compounds emissions in Norway spruce (Picea abies) in response to temperature changes. - Physiol. Plantarum 130: 58-66, 2007. Go to original source...
    36. Gilbert M.E., Zwieniecki M.A., Holbrook N.M.: Independent variation in photosynthetic capacity and stomatal conductance leads to differences in intrinsic water use efficiency in 11 soybean genotypes before and during mild drought. - J. Exp. Bot. 62: 2875-2887, 2011. Go to original source...
    37. Haldimann P., Feller U.: Inhibition of photosynthesis by high temperature in oak (Quercus pubescens L.) leaves grown under natural conditions closely correlates with a reversible heat dependent reduction of the activation state of ribulose-1,5-bisphosphate carboxylase/oxygenase. - Plant Cell Envi-ron. 27: 1169-1183, 2004. Go to original source...
    38. Hanson D.T., Swanson S., Graham L.E., Sharkey T.D.: Evolu-tionary significance of isoprene emission from mosses. - Am. J. Bot. 86: 634-639, 1999. Go to original source...
    39. Hasanuzzaman M., Nahar K., Alam M.M. et al.: Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. - Int. J. Mol. Sci. 14: 9643-9684, 2013. Go to original source...
    40. Hasanuzzaman M., Nahar K., Alam M.M., Fujita M.: Exogenous nitric oxide alleviates high temperature induced oxidative stress in wheat (Triticum aestivum L.) seedlings by modulating the antioxidant defense and glyoxalase system. - Aust. J. Crop Sci. 6: 1314-1323, 2012.
    41. Hassan I.A.: Effects of water stress and high temperature on gas exchange and chlorophyll fluorescence in Triticum aestivum L. - Photosynthetica 44: 312-315, 2006. Go to original source...
    42. Horak R., Borišev M., Pilipović A. et al.: Drought impact on forest trees in four nature protected areas in Serbia. - Sumar. List 138: 301-308, 2014.
    43. Hothorn T., Bretz F., Westfall P.: Simultaneous inference in general parametric models. - Biometrical J. 50: 346-363, 2008. Go to original source...
    44. Huang W., Yang Y.J., Zhang S.B.: Specific roles of cyclic electron flow around photosystem I in photosynthetic regulation in immature and mature leaves. - J. Plant Physiol. 209: 76-83, 2017. Go to original source...
    45. IPCC 2001: Climate Change: The Scientific Basis. Contribution of Working Group I to the Third Assessment Report of the Intergovernmental Panel on Climate Change. Pp. 83. Cambridge University Press, Cambridge 2001.
    46. James G., Witten D., Hastie T., Tibshirani R.: An Introduction to Statistical Learning with Applications in R. Pp. 426. Springer, New York 2013. Go to original source...
    47. Janković M.M.: Fam. Fagaceae Dum. - In: Josifović M. (ed.): [Flora of Republic of Serbia II.] Pp. 69-98. SANU, Belgrade 1970. [In Serbian]
    48. Janković M.M.: [Phytoecology with Basics of Phytocoenology and Overview of Vegetation Types on Earth.] Naučna knjiga, Belgrade 1971. [In Serbian]
    49. Jansen K., Du B., Kayler Z. et al.: Douglas-fir seedlings exhibit metabolic responses to increased temperature and atmospheric drought. - PLoS ONE 9: e114165, 2014. Go to original source...
    50. Jedmowski C., Ashoub A., Momtaz O., Brüggemann W.: Impact of drought, heat, and their combination on chlorophyll fluorescence and yield of wild barley (Hordeum spontaneum). -J. Bot. 2015: 120868, 2015. Go to original source...
    51. Jin R., Wang Y., Liu R. et al.: Physiological and metabolic changes of purslane (Portulaca oleracea L.) in response to drought, heat, and combined stresses. - Front. Plant Sci. 6: 1123, 2016. Go to original source...
    52. Knauer J., Zaehle S., Reichstein M. et al.: The response of ecosystem water-use efficiency to rising atmospheric CO2 concentrations: sensitivity and large-scale biogeochemical implications. - New Phytol. 213: 1654-1666, 2017. Go to original source...
    53. Koyama K., Takemoto S.: Morning reduction of photosynthetic capacity before midday depression. - Sci. Rep-UK 4: 4389, 2014.
    54. Lambers H., Chapin I., Pons S. et al.: Plant Physiological Ecology. Pp. 56-57. Springer, New York 2008. Go to original source...
    55. Liang X., Zhang L., Natarajan S.K., Becker D.F.: Proline mechanisms of stress survival. - Antioxid. Redox Sign. 19: 998-1011, 2013. Go to original source...
    56. Liaw A., Wiener M.: Classification and regression by randomForest. - R News 2: 18-22, 2002. Go to original source...
    57. Lichtenthaler H.K., Wellburn A.R.: Determinations of total caro-tenoids and chlorophylls a and b of leaf extracts in different solvents. - Biochem. Soc. T. 11: 591-592, 1983. Go to original source...
    58. Lüdecke D.: sjPlot: Data Visualization for Statistics in Social Science. R Package Version 2.6.1. Available at: https://CRAN.R-project.org/package=sjPlot, 2018.
    59. Manes F., Vitale M., Donato E. et al.: Different ability of three Mediterranean oak species to tolerate progressive water stress. - Photosynthetica 44: 387-393, 2006. Go to original source...
    60. Matsui T., Omasa K., Horie T.: The difference in sterility due to high temperatures during the flowering period among japonica rice varieties. - Plant Prod. Sci. 4: 90-93, 2001. Go to original source...
    61. Munné-Bosch S., Peñuelas J., Asensio D., Llusià J.: Airborne ethylene may alter antioxidant protection and reduce tolerance of holm oak to heat and drought stress. - Plant Physiol. 136: 2937-2947, 2004. Go to original source...
    62. Nahar K., Hasanuzamman M., Ahamed K.U. et al.: Plant responses and tolerance to high temperature stress: role of exogenous phytoprotectants. - In: Hakeem K.R. (ed.): Crop Production and Global Environmental Issues. Pp. 385-436. Springer, Cham-Heidelberg-New York-Dordrecht-London 2015. Go to original source...
    63. Nardini A., Lo Gullo M., Salleo S.: Competitive strategies for water availability in two Mediterranean Quercus species. - Plant Cell Environ. 22: 109-116, 1999. Go to original source...
    64. Öquist G., Wass R.R.: Portable microprocessor operated instrument for measuring chlorophyll fluorescence kinetics in stress physiology. - Physiol. Plantarum 73: 211-217, 1988. Go to original source...
    65. Pajević S., Borišev M., Orčić D. et al.: Photosynthetic and biochemical characteristics of invasive species (Ambrosia artemisiifolia L., Ambrosia trifida L. and Iva xanthifolia Nutt.) depending on soil humidity and phenological phase. - Russ. J. Ecol+ 41: 498-505, 2010. Go to original source...
    66. Pastenes C., Horton P.: Effect of high temperature on photo-synthesis in beans. I. Oxygen evolution and chlorophyll fluorescence. - Plant Physiol. 112: 1245-1251, 1996a. Go to original source...
    67. Pastenes C., Horton P.: Effect of high temperature on photo-synthesis in beans. II. CO2 assimilation and metabolite contents. - Plant Physiol. 112: 1253-1260, 1996b. Go to original source...
    68. Pinheiro J.C., Bates D.M., DebRoy S. et al.: nlme: Linear and Nonlinear Mixed Effects Models. R Package Version 3.1-137. Available at: https://CRAN.R-project.org/package=nlme, 2018.
    69. Pinheiro J.C., Bates D.M.: Mixed-Effects Models in S and S-PLUS. Pp. 528. Springer, New York 2000. Go to original source...
    70. Pintarić K.: [Forest-growing Features and Life of the Important Forest Species.] Pp. 221. UŠIT, Sarajevo 2002. [In Serbian]
    71. Polutchko S.K., Stewart J.J., Demmig-Adams B., Adams W.W.: Evaluating the link between photosynthetic capacity and leaf vascular organization with principal component analysis. - Photosynthetica 56: 392-403, 2018. Go to original source...
    72. Prasad P.V.V., Craufurd P.Q., Summerfield R.J., Wheeler T.R.: Effects of short episodes of heat stress on flower production and fruit-set of groundnut Arachis hypogaea L. - J. Exp. Bot. 51: 777-784, 2000.
    73. Pšidová E., Živčák M., Stojnić S. et al.: Altitude of origin influences the responses of PSII photochemistry to heat waves in European beech (Fagus sylvatica L.). - Environ. Exp. Bot. 152: 97-106, 2017. Go to original source...
    74. R Core Team R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna 2016. Available at: https://www.R-project.org/, 2016.
    75. Ran F., Zhang X., Zhang Y. et al.: Altitudinal variation in growth, photosynthetic capacity and water use efficiency of Abies faxoniana Rehd. et Wils. seedlings as revealed by reciprocal transplantations. - Trees 27: 1405-1416, 2013. Go to original source...
    76. Rennenberg H., Loreto F., Polle A. et al.: Physiological responses of forest trees to heat and drought. - Plant Biol. 8: 556-571, 2006. Go to original source...
    77. Scafaro A.P., Haynes P.A., Atwell B.J.: Physiological and molecular changes in Oryza meridionalis Ng., a heat-tolerant species of wild rice. - J. Exp. Bot. 61: 191-202, 2010. Go to original source...
    78. Schrader S.M., Wise R.R., Wacholtz W.F. et al.: Thylakoid membrane responses to moderately high leaf temperature in Pima cotton. - Plant Cell Environ. 27: 725-735, 2004. Go to original source...
    79. Schulze E.D., Ciais P., Luyssaert S. et al.: The European carbon balance. Part 4: integration of carbon and other trace-gas fluxes. - Glob. Change Biol. 16: 1451-1469, 2010. Go to original source...
    80. Selvaraj M.G., Burow G., Burke J.J. et al.: Heat stress screening of peanut (Arachis hypogaea L.) seedlings for acquired thermotolerance. - Plant Growth Regul. 65: 83-91, 2011. Go to original source...
    81. Sharkey D.T.: Effects of moderate heat stress on photosynthesis: importance of thylakoid reactions, rubisco deactivation, reactive oxygen species, and thermotolerance provided by isoprene. - Plant Cell Environ. 28: 269-277, 2005. Go to original source...
    82. Sharkey T.D., Zhang R.: High temperature effects on electron and proton circuits of photosynthesis. - J. Integr. Plant Biol. 52: 712-722, 2010. Go to original source...
    83. Singsaas E.L., Laporte M.M., Shi J.Z. et al.: Leaf temperature fluctuation affects isoprene emission from red oak (Quercus rubra) leaves. - Tree Physiol. 19: 917-924, 1999. Go to original source...
    84. Song Y., Chen Q., Ci D. et al.: Effects of high temperature on photosynthesis and related gene expression in poplar. - BMC Plant Biol. 14: 111, 2014. Go to original source...
    85. Spiegelhalter, D.J., Best N.G., Carlin B.P., van der Linde A.: Bayesian measures of model complexity and fit. - J. R. Stat. Soc. B 64: 583-640, 2002. Go to original source...
    86. Stojnić S, Pekeč S, Kebert M. et al.: Drought effects on physiology and biochemistry of pedunculate oak (Quercus robur L.) and hornbeam (Carpinus betulus L.) saplings grown in urban area of Novi Sad, Serbia. - SEEFOR 7: 57-63, 2016. Go to original source...
    87. Szabados L., Savouré A.: Proline: a multifunctional amino acid. -Trends Plant Sci. 15: 89-97, 2010. Go to original source...
    88. Taub D.R., Seemann J.R., Coleman J.S.: Growth in elevated CO2 protects photosynthesis against high-temperature damage. - Plant Cell Environ. 23: 649-656, 2000. Go to original source...
    89. Vaida F., Blanchard S.: Conditional Akaike information for mixed-effects models. - Biometrika 92: 351-370, 2005. Go to original source...
    90. Valentini R., Epron D., De Angelis P. et al.: In situ estimation of net CO2 assimilation, photosynthetic electron flow and photorespiration in Turkey oak (Q. cerris L.) leaves: diurnal cycles under different levels of water supply. - Plant Cell Environ. 18: 631-640, 1995. Go to original source...
    91. Vitale L., Arena C., de Santo V., D'Ambrosio N.: Effects of heat stress on gas exchange and photosystem II (PSII) photochemical activity of Phillyrea angustifolia exposed to elevated CO2 and subsaturating irradiance. - Botany 86: 435-441, 2008. Go to original source...
    92. Vitale L., Arena C., de Santo V.: Seasonal changes in photo-synthetic activity and photochemical efficiency of the Medi-terranean shrub Phillyrea angustifolia L. - Plant Biosyst. 146: 443-450, 2012. Go to original source...
    93. Wang G.P., Zhang X.Y., Li F. et al.: Overaccumulation of glycine betaine enhances tolerance to drought and heat stress in wheat leaves in the protection of photosynthesis. - Photosynthetica 48: 117-126, 2010. Go to original source...
    94. Wang J.Z., Cui L.J., Wang Y., Li J.L.: Growth, lipid peroxidation and photosynthesis in two tall fescue cultivars differing in heat tolerance. - Biol. Plantarum 53: 237-242, 2009. Go to original source...
    95. Wang X., Xu C., Cai X. et al.: Heat-responsive photosynthetic and signaling pathways in plants: insight from proteomics. - Int. J. Mol. Sci. 18: 2191, 2017. Go to original source...
    96. Woodward F.I., Lomas M.R.: Vegetation dynamics - simulating responses to climate change. - Biol. Rev. 79: 643-670, 2004. Go to original source...
    97. Zhang S., Li Q., Ma K., Chen L..: Temperature-dependent gas exchange and stomatal/non-stomatal limitation to CO2 assimilation of Quercus liaotungensis under midday high irradiance. - Photosynthetica 39: 383-388, 2001. Go to original source...

    Return to the content