Abstract
The share of overall photosynthetic limitation due to stomatal conductance (gs), mesophyll conductance (gm) and biochemistry depends on environmental conditions, but there is limited information on how the environmental responsiveness of photosynthesis varies among species with different heat thresholds. The study examined the photosynthetic responses of two tree species, Inga edulis, and Populus tremula, to increasing temperature and CO2. In P. tremula, higher temperature reduced gs, gm, CO2 assimilation (A), and electron transport rate (ETR). Despite these reductions, the relative share of photosynthetic limitations was minimally affected, except for reduced stomatal limitations at the highest CO2. In contrast, I. edulis increased mesophyll limitation at low CO2 but decreased at high CO2, with increased stomatal limitation under high CO2. Vcmax increased with temperature, along with A and electron flux for carboxylation. I. edulis and P. tremula exhibited distinct photosynthetic responses, indicating that temperature thresholds might influence how they respond to changes in [CO2]. These insights enhance our understanding of the complex interactions between temperature, CO2, and photosynthesis, providing valuable information for predicting species–specific adaptations and their implications for leaf carbon fluxes under varying environmental conditions.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The data associated with a paper is available at Theoretical and Experimental Plant Physiology.
References
Bellasio C, Beerling DJ, Griffiths H (2016) An Excel tool for deriving key photosynthetic parameters from combined gas exchange and chlorophyll fluorescence: theory and practice. Plant Cell Environ 39:1180–1197. https://doi.org/10.1071/FP08117
Bernacchi CJ, Singsaas EL, Pimentel C et al (2001) Improved temperature response functions for models of Rubisco-limited photosynthesis. Plant Cell Environ 24:253–259. https://doi.org/10.1046/j.1365-3040.2001.00668.x
Bonal D, Burban B, Stahl C et al (2016) The response of tropical rainforests to drought—lessons from recent research and future prospects. Ann for Sci 73:27–44. https://doi.org/10.1007/s13595-015-0522-5
Brodribb T (1996) Dynamics of changing intercellular CO2 concentration (Ci) during drought and determination of minimum functional Ci. Plant Physiol 111:179–185. https://doi.org/10.1104/pp.111.1.179
Cardoso D, Särkinen T, Alexander S et al (2017) Amazon plant diversity revealed by a taxonomically verified species list. Proc Natl Acad Sci 114:201706756. https://doi.org/10.1073/pnas.1706756114
Cavaleri MA, Reed SC, Smith WK, Wood TE (2015) Urgent need for warming experiments in tropical forests. Glob Chang Biol 21:2111–2121. https://doi.org/10.1111/gcb.12860
Cen Y, Sage R (2005) The regulation of Rubisco activity in response to variation in temperature and atmospheric CO2 partial pressure in sweet potato. Plant Physiol 139:979–990. https://doi.org/10.1104/pp.105.066233.1981
Cernusak LA, Winter K, Dalling JW et al (2013) Tropical forest responses to increasing atmospheric CO2: current knowledge and opportunities for future research. Funct Plant Biol 40:531–551. https://doi.org/10.1071/FP12309
Costa DF, Gomes HB, Cristina M, Liming LS (2022) The most extreme heat waves in Amazonia happened under extreme dryness. Clim Dyn 59:281–295. https://doi.org/10.1007/s00382-021-06134-8
Crous KY, Uddling J, De Kauwe MG (2022) Temperature responses of photosynthesis and respiration in evergreen trees from boreal to tropical latitudes. New Phytol 234:353–374. https://doi.org/10.1111/nph.17951
De Kauwe MG, Lin YS, Wright IJ et al (2016) A test of the one-point method for estimating maximum carboxylation capacity from field-measured, light-saturated photosynthesis. New Phytol 210:1130–1144. https://doi.org/10.1111/nph.13815
dos Santos VAHF, Ferreira MJ, Rodrigues JVFC et al (2018) Causes of reduced leaf-level photosynthesis during strong El Niño drought in a Central Amazon forest. Glob Chang Biol 24:4266–4279. https://doi.org/10.1111/gcb.14293
Doughty CE, Keany JM, Wiebe BC et al (2023) Tropical forests are approaching critical temperature thresholds. Nature. https://doi.org/10.1038/s41586-023-06391-z
Drake JE, Aspinwall MJ, Pfautsch S et al (2015) The capacity to cope with climate warming declines from temperate to tropical latitudes in two widely distributed Eucalyptus species. Glob Chang Biol 21:459–472. https://doi.org/10.1111/gcb.12729
Dusenge ME, Duarte AG, Way DA (2019) Plant carbon metabolism and climate change: elevated CO2 and temperature impacts on photosynthesis, photorespiration and respiration. New Phytol 221:32–49. https://doi.org/10.1111/nph.15283
Faria T, Schwanz P, Polle A et al (1999) Responses of photosynthetic and defense systems to high temperature stress in Quercus suber L. seedlings grown under elevated CO2. Plant Biol 1:365–371
Fauset S, Oliveira L, Buckeridge MS et al (2019) Contrasting responses of stomatal conductance and photosynthetic capacity to warming and elevated CO2 in the tropical tree species Alchornea glandulosa under heatwave conditions. Environ Exp Bot 158:28–39. https://doi.org/10.1016/j.envexpbot.2018.10.030
Flexas J, Diaz-Espejo A, Berry JA et al (2007) Analysis of leakage in IRGA’s leaf chambers of open gas exchange systems: quantification and its effects in photosynthesis parameterization. J Exp Bot 58:1533–1543. https://doi.org/10.1093/jxb/erm027
Flexas J, Niinemets Ü, Gallé A et al (2013a) Diffusional conductances to CO2 as a target for increasing photosynthesis and photosynthetic water-use efficiency. Photosynth Res 117:45–59
Flexas J, Scoffoni C, Gago J, Sack L (2013b) Leaf mesophyll conductance and leaf hydraulic conductance: an introduction to their measurement and coordination. J Exp Bot 64:3965–3981. https://doi.org/10.1093/jxb/ert319
Galmés J, Flexas J, Keys AJ et al (2005) Rubisco specificity factor tends to be larger in plant species from drier habitats and in species with persistent leaves. Plant Cell Environ 28:571–579. https://doi.org/10.1111/j.1365-3040.2005.01300.x
Galmés J, Kapralov MV, Copolovici LO et al (2015) Temperature responses of the Rubisco maximum carboxylase activity across domains of life: phylogenetic signals, trade-offs, and importance for carbon gain. Photosynth Res 123:183–201. https://doi.org/10.1007/s11120-014-0067-8
Galmés J, Hermida-carrera C, Laanisto L, Niinemets Ü (2016) A compendium of temperature responses of Rubisco kinetic traits: variability among and within photosynthetic groups and impacts on photosynthesis modeling. J Exp Bot 67:5067–5091. https://doi.org/10.1093/jxb/erw267
Galmés J, Molins A, Flexas J, Conesa M (2017) Coordination between leaf CO2 diffusion and Rubisco properties allows maximizing photosynthetic efficiency in Limonium species. Plant Cell Environ 40:2081–2094. https://doi.org/10.1111/pce.13004
Galmés J, Capó-Bauçà S, Niinemets Ü, Iñiguez C (2019) Potential improvement of photosynthetic CO2 assimilation in crops by exploiting the natural variation in the temperature response of Rubisco catalytic traits. Curr Opin Plant Biol 49:60–67. https://doi.org/10.1016/j.pbi.2019.05.002
Genty B, Briantais J-M, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92. https://doi.org/10.1016/S0304-4165(89)80016-9
Grassi G, Magnani F (2005) Stomatal, mesophyll conductance and biochemical limitations to photosynthesis as affected by drought and leaf ontogeny in ash and oak trees. Plant Cell Environ 28:834–849. https://doi.org/10.1111/j.1365-3040.2005.01333.x
Harley PC, Loreto F, Di Marco G, Sharkey TD (1992) Theoretical considerations when estimating the mesophyll conductance to CO2 flux by analysis of the response of photosynthesis to CO2. Plant Physiol 98:1429–1436. https://doi.org/10.1104/pp.98.4.1429
Hasper TB, Dusenge ME, Breuer F et al (2017) Stomatal CO2 responsiveness and photosynthetic capacity of tropical woody species in relation to taxonomy and functional traits. Oecologia 184:43–57. https://doi.org/10.1007/s00442-017-3829-0
Hozain MI, Salvucci ME, Fokar M, Holaday AS (2010) The differential response of photosynthesis to high temperature for a boreal and temperate Populus species relates to differences in Rubisco activation and Rubisco activase properties. Tree Physiol 30:32–44. https://doi.org/10.1093/treephys/tpp091
Huang M, Piao S, Ciais P et al (2019) Air temperature optima of vegetation productivity across global biomes. Nat Ecol Evol. https://doi.org/10.1038/s41559-019-0838-x
Hüve K, Bichele I, Kaldmäe H et al (2019) Responses of Aspen leaves to Heatflecks: both damaging and non-damaging rapid temperature excursions reduce photosynthesis. Plants 8:145. https://doi.org/10.3390/plants8060145
Iñiguez C, Capó-Bauçà S, Niinemets Ü et al (2020) Evolutionary trends in RuBisCO kinetics and their co-evolution with CO2 concentrating mechanisms. Plant J 101:897–918. https://doi.org/10.1111/tpj.14643
Kurepin LV, Stangl ZR, Ivanov AG et al (2018) Contrasting acclimation abilities of two dominant boreal conifers to elevated CO2 and temperature. Plant Cell Environ 41:1331–1345. https://doi.org/10.1111/pce.13158
Laisk A, Oja V, Rasulov B et al (2002) A computer-operated routine of gas exchange and optical measurements to diagnose photosynthetic apparatus in leaves. Plant Cell Environ 25:923–943. https://doi.org/10.1046/j.1365-3040.2002.00873.x
Leuning R (1995) A critical appraisal of a combined stomatal-photosynthesis model for C3 plants. Plant Cell Physiol 18:339–355
Lewis JD, Phillips NG, Logan BA et al (2015) Rising temperature may negate the stimulatory effect of rising CO2 on growth and physiology of Wollemi pine (Wollemia Nobilis). Funct Plant Biol 42:836–850. https://doi.org/10.1071/FP14256
Lloyd J, Farquhar GD (2008) Effects of rising temperatures and [CO2] on the physiology of tropical forest trees. Philos Trans R Soc Lond B Biol Sci 363:1811–1817. https://doi.org/10.1098/rstb.2007.0032
Loftus GR, Masson MEJ (1994) Using confidence intervals in within-subject designs. Psychon Bull Rev 1:476–490. https://doi.org/10.3758/BF03210951
Lojka B, Dumas L, Preininger D et al (2010) The use and integration of Inga edulis en agroforestry systems in the amazon. Agric Trop Subtrop 43:352–359
Martins SCV, Galmés J, Cavatte PC et al (2014) Understanding the low photosynthetic rates of sun and shade coffee leaves: bridging the gap on the relative roles of hydraulic, diffusive and biochemical constraints to photosynthesis. PLoS One 9:e95571. https://doi.org/10.1371/journal.pone.0095571
Martins MQ, Rodrigues WP, Fortunato AS et al (2016) Protective response mechanisms to heat stress in interaction with high [CO2] conditions in Coffea spp. Front Plant Sci. https://doi.org/10.3389/fpls.2016.00947
Moore CE, Meacham-Hensold K, Lemonnier P et al (2021) The effect of increasing temperature on crop photosynthesis: from enzymes to ecosystems. J Exp Bot 72:2822–2844. https://doi.org/10.1093/jxb/erab090
Morfopoulos C, Sperlich D, Peñuelas J et al (2014) A model of plant isoprene emission based on available reducing power captures responses to atmospheric CO2. New Phytol 203:125–139. https://doi.org/10.1111/nph.12770
Niinemets Ü (2018) When leaves go over the thermal edge. Plant Cell Environ 41:1247–1250. https://doi.org/10.1111/pce.13184
Niinemets U, Díaz-Espejo A, Flexas J et al (2009) Role of mesophyll diffusion conductance in constraining potential photosynthetic productivity in the field. J Exp Bot 60:2249–2270. https://doi.org/10.1093/jxb/erp036
Nijs I, Impens I (1996) Effects of elevated CO2 concentration and climate-warming on photosynthesis during winter in Lolium perenne. J Exp Bot 47:915–924. https://doi.org/10.1093/jxb/47.7.915
Ouyang W, Struik PC, Yin X, Yang J (2017) Stomatal conductance, mesophyll conductance, and trans piration efficiency in relation to leaf anatomy in rice and wheat genotypes under drought. J Exp Bot 68:5191–5205. https://doi.org/10.1093/jxb/erx314
Pan C, Ahammed GJ, Li X, Shi K (2018) Elevated CO2 improves photosynthesis under high temperature by attenuating the functional limitations to energy fluxes, electron transport and redox homeostasis in tomato leaves. Front Plant Sci 871:1–11. https://doi.org/10.3389/fpls.2018.01739
Pimentel C, Bernacchi C, Long S (2007) Limitations to photosynthesis at different temperatures in the leaves of Citrus limon. Braz J Plant Physiol 19:141–147. https://doi.org/10.1590/S1677-04202007000200006
Pinto SS, Martins AO, Fontes LFP et al (2022) Elevated [CO2] mitigates the impacts of heat stress in eucalyptus seedlings. Theor Exp Plant Physiol 34:447–462. https://doi.org/10.1007/s40626-022-00257-x
Rodeghiero M, Niinemets Ü, Cescatti A (2007) Major diffusion leaks of clamp-on leaf cuvettes still unaccounted: how erroneous are the estimates of Farquhar model parameters? Plant Cell Environ 30:1006–1022. https://doi.org/10.1111/j.1365-3040.2007.001689.x
Rodrigues WP, Martins MQ, Fortunato AS et al (2016) Long-term elevated air [CO2] strengthens photosynthetic functioning and mitigates the impact of supra-optimal temperatures in tropical Coffea arabica and C. Canephora species. Glob Chang Biol 22:415–431. https://doi.org/10.1111/gcb.13088
Sage RF (2002) Variation in the kcat of Rubisco in C3 and C4 plants and some implications for photosynthetic performance at high and low temperature. J Exp Bot 53:609–620. https://doi.org/10.1093/jexbot/53.369.609
Silim SN, Ryan N, Kubien DS (2010) Temperature responses of photosynthesis and respiration in Populus balsamifera L.: acclimation versus adaptation. Photosynth Res 104:19–30. https://doi.org/10.1007/s11120-010-9527-y
Slot M, Winter K (2017a) Photosynthetic acclimation to warming in tropical forest tree seedlings. J Exp Bot 68:2275–2284. https://doi.org/10.1093/jxb/erx071
Slot M, Winter K (2017b) In situ temperature relationships of biochemical and stomatal controls of photosynthesis in four lowland tropical tree species. Plant Cell Environ 40:3055–3068. https://doi.org/10.1111/pce.13071
Slot M, Garcia MN, Winter K (2016) Temperature response of CO2 exchange in three tropical tree species. Funct Plant Biol 43:468–478. https://doi.org/10.1071/FP15320
Smith MN, Taylor TC, van Haren J et al (2020) Empirical evidence for resilience of tropical forest photosynthesis in a warmer world. Nat Plants 6:1225–1230. https://doi.org/10.1038/s41477-020-00780-2
Soh WK, Yiotis C, Murray M et al (2019) Rising CO2 drives divergence in water use efficiency of evergreen and deciduous plants. Sci Adv 5:1–12. https://doi.org/10.1126/sciadv.aax7906
Steege H, Pitman NC, Sabatier D et al (2013) Hyperdominance in the Amazonian tree flora. Science 342:1243092.-=. https://doi.org/10.1126/science.1243092
Stefanski A, Butler EE, Bermudez R et al (2023) Stomatal behavior moderates water cost of CO2 acquisition for 21 boreal and temperate species under experimental climate change. Plant Cell Environ. https://doi.org/10.1111/pce.14559
von Caemmerer S, Evans JR (2015) Temperature responses of mesophyll conductance differ greatly between species. Plant Cell Environ 38:629–637. https://doi.org/10.1111/pce.12449
Way DA, Oren R (2010) Differential responses to changes in growth temperature between trees from different functional groups and biomes: a review and synthesis of data. Tree Physiol 30:669–688. https://doi.org/10.1093/treephys/tpq015
Worrell R (1995) European aspen (Populus tremula L.): a review with particular reference to Scotland I. distribution, ecology and genetic variation. Forestry 68:93–105. https://doi.org/10.1093/forestry/68.2.93
Ye ZP, Yu Q, Kang HJ (2012) Evaluation of photosynthetic electron flow using simultaneous measurements of gas exchange and chlorophyll fluorescence under photorespiratory conditions. Photosynthetica 50:472–476. https://doi.org/10.1007/s11099-012-0051-5
Zhu L, Bloomfield KJ, Hocart CH et al (2018) Plasticity of photosynthetic heat tolerance in plants adapted to thermally contrasting biomes. Plant Cell Environ 41:1251–1262. https://doi.org/10.1111/pce.13133
Zhu L, Li H, Thorpe MR et al (2021) Stomatal and mesophyll conductance are dominant limitations to photosynthesis in response to heat stress during severe drought in a temperate and a tropical tree species. Trees 35:1613–1626. https://doi.org/10.1007/s00468-021-02140-9
Acknowledgements
We acknowledge the National Institute for Amazonian Research (MCTIC-INPA) and the National Council for Scientific and Technological Development (CNPq, Brazil) for financially supporting our work. This work was also supported by funding from Coordination for the Improvement of Higher Level Personnel (CAPES, Brazil), Amazonas State Research Support Foundation (FAPEAM, Brazil) and DoRa T5 program (European Regional Development Fund) and CNPq-Brazil research fellowships granted to J.F.C.G. are also gratefully acknowledged. Ü.N., B.R., and E.T. were supported by the European Commission through the European Research Council (advanced grant 322603, SIP VOL+), the European Regional Development Fund (Center of Excellence EcolChange), the Estonian Ministry of Science and Education (institutional grant IUT-8-3), and Mobilitas Pluss (MOBJD696).
Author information
Authors and Affiliations
Contributions
VFS, BR, ET, ÜN, and JFCG. discussed the original idea; VFS., and ET, carried out the experiments and analyzed the data; VFS. conceived the study and wrote the article with contributions of all authors; CM research plans and complemented the writing; PMA, and SDJ provided technical assistance to VFS; BR, ÜN, JFCG supervised the experiments; JFCG agrees to serve as the author responsible for contact and ensures communication.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
de Souza, V.F., Rasulov, B., Talts, E. et al. Thermal sensitivity determines the effect of high CO2 on carbon uptake in Populus tremula and Inga edulis. Theor. Exp. Plant Physiol. 36, 199–213 (2024). https://doi.org/10.1007/s40626-024-00312-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40626-024-00312-9