Abstract
Key message
Two species from warmer climates, but not the corresponding congeneric species from relatively cooler ones, decreased stomatal conductance upon heatwaves, and one of them showed significant decrease in the efficiency of open reaction centres of PSII in the light. In contrast, responses of major antioxidants ascorbic acid and glutathione to heatwaves were more similar between congeneric species than between species from similar climates.
Abstract
According to climate change predictions, heatwaves will increase in frequency and intensity. This can threaten survival of sensitive tree species. Heatwaves affect photosynthetic capacity and cause an imbalance between light driven electron transport and carbon fixation. This can increase the concentration of reactive oxygen species, and can cause photo-oxidative stress. Heat dissipation and antioxidants are crucial in plant defence against photo-oxidative stress. We hypothesised that stomatal regulations, heat dissipation as measured by chlorophyll fluorescence and responses of major antioxidants ascorbic acid and glutathione to heatwaves will vary according to the climate at the site of origin of tree species. Tree seedlings from warmer (Eucalyptus grandis, Acacia aneura) and cooler climates (Eucalyptus tricarpa, Acacia melanoxylon) were exposed to air temperatures about 5 °C above control levels for 5 days. The two species from warmer climates responded to heatwaves with stomatal closure restricting transpiration and carbon fixation, and E. grandis also significantly increased heat dissipation (as judged by decreased efficiency of open reaction centres of PSII in the light). Species from cooler climates kept stomata open allowing continuing carbon assimilation and transpirational cooling. Heatwaves did not reduce maximum quantum efficiency of PSII in Acacia species, with insignificant decreases in Eucalyptus species. Glutathione concentrations increased significantly upon heatwave in E. tricarpa (from cooler climates), showed a time-dependent response to heatwave in E. grandis (from warmer climates) with an increase at later stages, and showed a tendency to decrease upon heatwave in both Acacia species (non-significant only for A. melanoxylon). Ascorbic acid concentrations increased significantly in E. tricarpa (cooler climates), and did not change significantly in other species. The redox state of ascorbic acid or glutathione only changed significantly and transiently in response to heatwave in A. aneura (warmer climates; GSSG % and ASC %) and A. melanoxylon (cooler climates; GSSG %), but not Eucalyptus species. Therefore, differences in stomatal regulations upon heatwaves aligned with the origin of species in warmer or cooler climates, whereas responses of ascorbic acid and glutathione to heatwaves were more aligned with the two genera.
Similar content being viewed by others
References
Addington RN, Mitchell RJ, Oren R, Donovan LA (2004) Stomatal sensitivity to vapor pressure deficit and its relationship to hydraulic conductance in Pinus palustris. Tree Physiol 24:561–569
Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Kitzberger T, Rigling A, Breshears DD, Hogg EHT, Gonzalez P, Fensham R, Zhang Z, Castro J, Demidova N, Lim J-H, Allard G, Running SW, Semerci A, Cobb N (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For Ecol Manag 259:660–684
Ameye M, Wertin TM, Bauweraerts I, McGuire MA, Teskey RO, Steppe K (2012) The effect of induced heat waves on Pinus taeda and Quercus rubra seedlings in ambient and elevated CO2 atmospheres. New Phytol 196(2):448–461
Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141(2):391–396
Bauweraerts I, Ameye M, Wertin TM, McGuire MA, Teskey RO, Steppe K (2014) Acclimation effects of heat waves and elevated [CO2] on gas exchange and chlorophyll fluorescence of northern red oak (Quercus rubra L.) seedlings. Plant Ecol 215(7):733–746
Berry J, Björkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Ann Rev Plant Physiol 31:491–543
Bussotti F, Ferrini F, Pollastrini M, Fini A (2014) The challenge of Mediterranean sclerophyllous vegetation under climate change: from acclimation to adaptation. Environ Exp Bot 103:80–98
Contran N, Gunthardt-Goerg MS, Kuster TM, Cerana R, Crosti P, Paoletti E (2013) Physiological and biochemical responses of Quercus pubescens to air warming and drought on acidic and calcareous soils. Plant Biol (Stuttg) 15(Suppl 1):157–168
Cunningham SC, Read J (2003) Do temperate rainforest trees have a greater ability to acclimate to changing temperatures than tropical rainforest trees. New Phytol 157:55–64
Cunningham SC, Read J (2006) Foliar temperature tolerance of temperate and tropical evergreen rain forest trees of Australia. Tree Physiol 26:1435–1443
De Micco V, Aronne G, Baas P (2008) Wood anatomy and hydraulic architecture of stems and twigs of some Mediterranean trees and shrubs along a mesic-xeric gradient. Trees 22(5):643–655
Demmig-Adams B, Cohu CM, Muller O, Adams WW (2012) Modulation of photosynthetic energy conversion efficiency in nature: from seconds to seasons. Photosynth Res 113(1–3):75–88
Dreyer E, Roux XL, Montpied P, Alain F, Daudet, Masson F (2001) Temperature response of leaf photosynthetic capacity in seedlings from seven temperate tree species. Tree Physiol 21:223–232
Duan B, Dong T, Zhang X, Zhang Y, Chen J (2014) Ecophysiological responses of two dominant subalpine tree species Betula albo-sinensis and Abies faxoniana to intra- and interspecific competition under elevated temperature. For Ecol Manag 323:20–27
Duursma RA, Barton CVM, Lin Y-S, Medlyn BE, Eamus D, Tissue DT, Ellsworth DS, McMurtrie RE (2014) The peaked response of transpiration rate to vapour pressure deficit in field conditions can be explained by the temperature optimum of photosynthesis. Agric For Meteorol 189–190:2–10
Faria T, Vaz M, Schwanz P, Polle A, Pereira JS, Chaves MM (1999) Responses of photosynthetic and defence systems to high temperature stress in Quercus suber L. seedlings grown under elevated CO2. Plant Biol 1:365–371
Feller U (2006) Stomatal opening at elevated temperature: an underestimated regulatory mechanim? Gen Appl Plant Physiol 32(Special issue):19–31
FloraBank (2014) Greening Australia, http://www.florabank.org.au. Accessed 07 Jan 2015
Foyer CH, Noctor G (2009) Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid Redox Signal 11(4):861–905
Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155(1):2–18
Foyer CH, Shigeoka S (2011) Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiol 155(1):93–100
Foyer CH, Neukermans J, Queval G, Noctor G, Harbinson J (2012) Photosynthetic control of electron transport and the regulation of gene expression. J Exp Bot 63(4):1637–1661
Frich P, Alexander LV, Della-Marta P, Gleason B, Haylock M, Tank AMGK, Peterson T (2002) Observed coherent changes in climatic extremes during the second half of the twentieth century. Clim Res 19:193–212
García-Plazaola JI, Esteban R, Hormaetxe K, Fernández-Marín B, Becerril JM (2008) Photoprotective responses of Mediterranean and Atlantic trees to the extreme heat-wave of summer 2003 in Southwestern Europe. Trees 22(3):385–392
Ghannoum O, Phillips NG, Sears MA, Logan BA, Lewis JD, Conroy JP, Tissue DT (2010) Photosynthetic responses of two eucalypts to industrial-age changes in atmospheric [CO2] and temperature. Plant Cell Environ 33(10):1671–1681
Gunderson CA, O’Hara KH, Campion CM, Walker AV, Edwards NT (2010) Thermal plasticity of photosynthesis: the role of acclimation in forest responses to a warming climate. Glob Change Biol 16(8):2272–2286
Hu B, Simon J, Rennenberg H (2013) Drought and air warming affect the species-specific levels of stress-related foliar metabolites of three oak species on acidic and calcareous soil. Tree Physiol 33(5):489–504
Hüve K, Bichele I, Rasulov B, Niinemets Ü (2011) When it is too hot for photosynthesis: heat-induced instability of photosynthesis in relation to respiratory burst, cell permeability changes and H2O2 formation. Plant Cell Environ 34(1):113–126
IPCC (2014) Climate Change: impacts, adaptation, and vulnerability. Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. In: Field CB, Barros VR, Dokken DJ, Mach KJ, Mastrandrea MD, Bilir TE, Chatterjee M, Ebi KL, Estrada YO, Genova RC, Girma B, Kissel ES, Levy AN, MacCracken S, Mastrandrea PR, White LL (eds) Intergovernmental Panel on Climate Change. Part A, Cambridge, New York
Johnson DM, McCulloh KA, Reinhardt K (2011) The earliest stages of tree growth: development, physiology and impacts of microclimate. In: Meinzer FC, Lachenbruch B, Dawson TE (eds) Size- and age-related changes in tree structure and function. Springer, Netherlands
Knight C, Ackerly D (2002) An ecological and evolutionary analysis of photosynthetic thermotolerance using the temperature-dependent increase in fluorescence. Oecologia 130(4):505–514
Knörzer OC, Burner J, Boger P (1996) Alterations in the antioxidative system of suspension-cultured soybean cells (Glycine max) induced by oxidative stress. Physiol Plant 97:388–396
Lin YS, Medlyn BE, De Kauwe MG, Ellsworth DS (2013) Biochemical photosynthetic responses to temperature: how do interspecific differences compare with seasonal shifts? Tree Physiol 33(8):793–806
Ma Y-H, Ma F-W, Zhang J-K, Li M-J, Wang Y-H, Liang D (2008) Effects of high temperature on activities and gene expression of enzymes involved in ascorbate–glutathione cycle in apple leaves. Plant Sci 175(6):761–766
Maxwell K, Johnson GN (2000) Chlorophyll fluorescence-a practical guide. J Exp Bot 51(345):659–668
McDowell N, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T, Plaut J, Sperry J, West A, Williams DG, Yepez EA (2008) Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytol 178(4):719–739
Mittler R, Finka A, Goloubinoff P (2012) How do plants feel the heat? Trends Biochem Sci 37(3):118–125
Monteith JL, Unsworth MH (eds) (2008) Principles of environmental physics. Elsevier, Amsterdam, Boston
Munné-Bosch S, Alegre L (2002) The function of tocopherols and tocotrienols in plants. Crit Rev Plant Sci 21(1):31–57
Munné-Bosch S, Peñuelas J, Asensio D, Llusiá J (2004) Airborne ethylene may alter antioxidant protection and reduce tolerance of holm Oak to heat and drought stress. Plant Physiol 136(2):2937–2947
Munné-Bosch S, Queval G, Foyer CH (2012) The impact of global change factors on redox signaling underpinning stress tolerance. Plant Physiol 161(1):5–19
Niinemets Ü (2010) Responses of forest trees to single and multiple environmental stresses from seedlings to mature plants: past stress history, stress interactions, tolerance and acclimation. For Ecol Manag 260(10):1623–1639
Orsenigo S, Mondoni A, Rossi G, Abeli T (2014) Some like it hot and some like it cold, but not too much: plant responses to climate extremes. Plant Ecol 215(7):677–688
Peltzer D, Dreyer E, Polle A (2002) Differential temperature dependencies of antioxidative enzymes in two contrasting species: Fagus sylvatica and Coleus blumei. Plant Physiol Biochem 40:141–150
Rennenberg H, Loreto F, Polle A, Brilli F, Fares S, Beniwal RS, Gessler A (2006) Physiological responses of forest trees to heat and drought. Plant Biol 8(5):556–571
Roden JS, Ball MC (1996) Growth and photosynthesis of two eucalypt species during high temperature stress under ambient and elevated [CO2]. Glob Change Biol 2(2):115–128
Sage RF, Way DA, Kubien DS (2008) Rubisco, rubisco activase, and global climate change. J Exp Bot 59(7):1581–1595
Schymanski SJ, Or D, Zwieniecki M (2013) Stomatal control and leaf thermal and hydraulic capacitances under rapid environmental fluctuations. PLoS One 8(1):e54231
Sgherri CLM, Loggini B, Puligaa S, Navari-Izzo F (1994) Antioxidant system in Sporobolus stapfianus: changes in response to desiccation and rehydration. Phytochemistry 35(3):561–565
Sharkey TD (2005) 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
Sharkey TD, Zhang R (2010) High temperature effects on electron and proton circuits of photosynthesis. J Integr Plant Biol 52(8):712–722
Silva EN, Ferreira-Silva SL, de Vasconcelos Fontenele A, Ribeiro RV, Viégas RA, Silveira JAG (2010) Photosynthetic changes and protective mechanisms against oxidative damage subjected to isolated and combined drought and heat stresses in Jatropha curcas plants. J Plant Physiol 167(14):1157–1164
Silva EN, Vieira SA, Ribeiro RV, Ponte LFA, Ferreira-Silva SL, Silveira JAG (2012) Contrasting physiological responses of Jatropha curcas plants to single and combined stresses of salinity and heat. J Plant Growth Regul 32(1):159–169
Smirnoff N (2011) Vitamin C: the metabolism and functions of ascorbic acid in plants. Adv Bot Res 59:107–177
SpeciesBank (2014) Australian Biological Resources Study, Canberra. http://www.environment.gov.au/biodiversity/abrs/online-resources/species-bank/index.html. Accessed 03 April 2014
Suzuki N, Mittler R (2006) Reactive oxygen species and temperature stresses: a delicate balance between signaling and destruction. Physiol Plant 126:45–51
Tausz M, Šircelj H, Grill D (2004) The glutathione system as a stress marker in plant ecophysiology: is a stress-response concept valid? J Exp Bot 55(404):1955–1962
Teskey R, Wertin T, Bauweraerts I, Ameye M, McGuire MA, Steppe K (2014) Responses of tree species to heat waves and extreme heat events. Plant Cell Environ. doi:10.1111/pce.12417
Thomas DS, Eamus D (1999) The influence of predawn leaf water potential on stomatal responses to atmospheric water content at constant Ci and on stem hydraulic conductance and foliar ABA concentrations. J Exp Bot 50:243–251
Tissier J, Lambs L, Peltier JP, Marigo G (2004) Relationships between hydraulic traits and habitat preference for six Acer species occurring in the French Alps. Ann For Sci 61(1):81–86
Vargas GG, Roberto A, Cordero S (2013) Photosynthetic responses to temperature of two tropical rainforest tree species from Costa Rica. Trees 27(5):1261–1270
Venegas-González A, von Arx G, Chagas MP, Filho MT (2014) Plasticity in xylem anatomical traits of two tropical species in response to intra-seasonal climate variability. Trees 29(2):423–435
Weston DJ, Bauerle WL (2007) Inhibition and acclimation of C3 photosynthesis to moderate heat: a perspective from thermally contrasting genotypes of Acer rubrum (red maple). Tree Physiol 27:1083–1092
Will RE, Wilson SM, Zou CB, Hennessey TC (2013) Increased vapor pressure deficit due to higher temperature leads to greater transpiration and faster mortality during drought for tree seedlings common to the forest-grassland ecotone. New Phytol 200(2):366–374
Wujeska A, Bossinger G, Tausz M (2013) Responses of foliar antioxidative and photoprotective defence systems of trees to drought: a meta-analysis. Tree Physiol 33(10):1018–1029
Wujeska-Klause A, Bossinger G, Tausz M (2015) Seedlings of two Acacia species from contrasting habitats show different photoprotective and antioxidative responses to drought and heatwaves. Ann For Sci 72(4):403–414
Acknowledgments
A. W-K would like to acknowledge staff and students at Department of Forest and Ecosystem Science of the University of Melbourne. Special thanks to Markus Loew for advice with R, free software environment for statistical computing and graphics. We thank reviewers for many constructive suggestions that improved the manuscript.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Funding
A. W-K is supported by a Melbourne International Research Scholarship and a Melbourne International Fee Remission Scholarship.
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by W. Bilger.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Wujeska-Klause, A., Bossinger, G. & Tausz, M. Responses to heatwaves of gas exchange, chlorophyll fluorescence and antioxidants ascorbic acid and glutathione in congeneric pairs of Acacia and Eucalyptus species from relatively cooler and warmer climates. Trees 29, 1929–1941 (2015). https://doi.org/10.1007/s00468-015-1274-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00468-015-1274-4