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Elevated [CO2] and growth temperature have a small positive effect on photosynthetic thermotolerance of Pinus taeda seedlings

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Growth temperature had little effect on the response of net photosynthesis to high temperatures (up to 47 °C). On the other hand, elevated [CO 2 ] increased net photosynthesis at high temperatures.

Abstract

We investigated whether Pinus taeda seedlings grown under elevated CO2-concentration ([CO2]) and temperature would be able to maintain positive net photosynthesis (A net) longer than seedlings grown under ambient conditions when exposed to temperatures up to 47 °C. Additionally, we investigated whether a locally applied temperature increase would yield the same short-term gas exchange response to temperatures up to 47 °C as a naturally occurring latitudinal temperature increase of equal magnitude. Growth conditions were applied for 7 months (February to August) in treatment chambers constructed at two sites in the native range of P. taeda in the southern US. The sites were located 300 km apart along a north–south axis with a natural temperature difference of 2.1 °C. Seedlings were grown under ambient temperature and [CO2] conditions at both sites. At the northern site, we also applied a temperature increase of 2 °C (T E), ensuring that this treatment equalled the mean temperature at the southern site. Additionally, at the northern site, we applied a treatment of elevated [CO2] (C E). Gas exchange was measured on all plants in walk-in environmentally controlled chambers. Under C E, there was no difference in A net of seedlings grown in ambient or ambient +2 °C temperatures at any measurement temperature, while differences were present under ambient [CO2]. Furthermore, A net was higher under C E than under ambient [CO2]. At 47 °C, A net was negative in all seedlings except those in the C E and ambient temperature treatment combination. Seedlings at the northern site in the T E treatment showed no significant differences in A net compared with seedlings grown at ambient temperature at the southern site, indicating that the plants responded equally to a manipulated temperature increase and a latitudinal increase in temperature. Our results suggest that elevated [CO2] increases photosynthetic thermotolerance at high temperature (>41 °C), but this effect diminishes as temperature increases further. Temperature manipulations could provide accurate information on the effect of latitudinal differences in temperature on leaf gas exchange of P. taeda.

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References

  • Ainsworth EA, Rogers A (2007) The response of photosynthesis and stomatal conductance to rising [CO2]: mechanisms and environmental interactions. Plant Cell Environ 30:258–270

    Article  PubMed  CAS  Google Scholar 

  • Al-Khatib K, Paulsen GM (1989) Enhancement of thermal injury to photosynthesis in wheat plants and thylakoids by high light intensity. Plant Physiol 90:1041–1048

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • 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 196:448–461

    Article  PubMed  Google Scholar 

  • Anderson LJ, Cipollini D (2013) Gas exchange, growth, and defense responses of invasive Alliaria petiolata (Brassicaceae) and native Geum vernum (Rosaceae) to elevated atmospheric CO2 and warm spring temperatures. Am J Bot 100:1544–1554

    Article  PubMed  CAS  Google Scholar 

  • Aspinwall MJ, King JS, Domec J-C, McKeand SE, Isik F (2011) Genetic effects on transpiration, canopy conductance, stomatal sensitivity to vapour pressure deficit, and cavitation resistance in loblolly pine. Ecohydrol 4:168–182

    Article  Google Scholar 

  • Bauweraerts I, Wertin TM, Ameye M, McGuire MA, Teskey RO, Steppe K (2013) The effect of heat waves, elevated [CO2] and low soil water availability on northern red oak (Quercus rubra L.) seedlings. Global Change Biol 19:517–528

    Article  Google Scholar 

  • Berry JA, Björkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Ann Rev Plant Biol 31:491–543

    Article  Google Scholar 

  • Bigras FJ (2000) Selection of white spruce families in the context of climate change: heat tolerance. Tree Physiol 20:1227–1234

    Article  PubMed  CAS  Google Scholar 

  • Boyette MD, Bilderback TE (1996) A small Backyard Greenhouse for the Home Gardener. North Carolina Cooperative Extension Service, Raleigh

    Google Scholar 

  • Christensen JH, Hewitson B, Busuioc A et al (2007) Climate change 2007: the regional climate projections. In: Fu C, Giorgi F (eds) IPCC 2007. Cambridge University Press, Cambridge, p 94

    Google Scholar 

  • Coumou D, Rahmstorf S (2012) A decade of weather extremes. Nat Clim Change 2:491–496

    Google Scholar 

  • Coumou D, Robinson A (2013) Historic and future increase in the global land area affected by monthly heat extremes. Environ Res Lett 8:034018

    Article  Google Scholar 

  • Diffenbaugh NS, Ashfaq M (2010) Intensification of hot extremes in the United States. Geophys Res Lett 37:1–14

    Article  Google Scholar 

  • Drake JE, Raetz LM, Davis SC, DeLucia EH (2010) Hydraulic limitation not declining nitrogen availability causes the age-related photosynthetic decline in loblolly pine (Pinus taeda L.). Plant Cell Environ 33:1756–1766

    Article  PubMed  CAS  Google Scholar 

  • Dreyer E, Le Roux X, Montpied P, Daudet FA, Masson F (2001) Temperature response of leaf photosynthetic capacity in seedlings from seven temperate tree species. Tree Physiol 21:223–232

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Ghouil H, Montpied P, Epron D, Ksontini M, Hanchi B, Dreyer E (2003) Thermal optima of photosynthetic functions and thermostability of photochemistry in cork oak seedlings. Tree Physiol 23:1031–1039

    Article  PubMed  CAS  Google Scholar 

  • Gonzalez-Benecke CA, Martin TA (2010) Water availability and genetic effects on water relations of loblolly pine (Pinus taeda) stands. Tree Physiol 30:376–392

    Article  PubMed  Google Scholar 

  • Guo Y, Zhou H, Zhang L (2006) Photosynthetic characteristics and protective mechanisms against photooxidation during high temperature stress in two citrus species. Sci Hortic 108:260–267

    Article  CAS  Google Scholar 

  • Haldimann P, Feller U (2004) 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 Environ 27:1169–1183

    Article  CAS  Google Scholar 

  • Hamerlynck EP, Knapp AK (1996) Photosynthetic and stomatal responses to high temperature and light in two oaks at the western limit of their range. Tree Physiol 16:557–565

    Article  PubMed  Google Scholar 

  • Hamerlynck EP, Huxman TE, Loik ME, Smith SD (2000) Effects of extreme high temperature, drought and elevated CO2 on photosynthesis of the Mojave Desert evergreen shrub, Larrea tridentata. Plant Ecol 148:183–193

    Article  Google Scholar 

  • Hamilton EW 3rd, Heckathorn SA, Joshi P, Wang D, Barua D (2008) Interactive effects of elevated CO2 and growth temperature on the tolerance of photosynthesis to acute heat stress in C3 and C4 species. J Integr Plant Biol 50:1375–1387

    Article  PubMed  CAS  Google Scholar 

  • Houghton JT, Ding Y, Griggs DJ, Noguer M, van der Linden PJ, Dai X, Maskell K (2001) Climate change 2001: the scientific basis. Contribution of Working Group I to the Third Assessment Report of the Intergovernmental Panel on Climate Change. In: Johnson CA (ed) IPCC 2001. Cambridge University Press, Cambridge, p 881

    Google Scholar 

  • Huerta C, Freire M, Cardemil L (2013) Expression of hsp70, hsp100 and ubiquitin in Aloe barbadensis Miller under direct heat stress and under temperature acclimation conditions. Plant Cell Rep 32:293–307

    Article  PubMed  CAS  Google Scholar 

  • Hymus GJ, Ellsworth DS, Baker NR, Long SP (1999) Does free-air carbon dioxide enrichment affect photochemical energy use by evergreen trees in different seasons? A chlorophyll fluorescence study of mature loblolly pine. Plant Physiol 120:1183–1192

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • IPCC (2013) Climate Change 2013: the physical science basis. Intergovermental panel on climate change. Cambridge University Press, Cambridge

    Google Scholar 

  • Kolb PF, Robberecht R (1996) High temperature and drought stress effects on survival of Pinus ponderosa seedlings. Tree Physiol 16:665–672

    Article  PubMed  Google Scholar 

  • Kouril R, Lazár D, Ilík P, Skotnica J, Krchnák P, Naus J (2004) High-temperature induced chlorophyll fluorescence rise in plants at 40–50 °C: experimental and theoretical approach. Photosynth Res 81:49–66

    Article  PubMed  CAS  Google Scholar 

  • Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Ann Rev Plant Physiol Mol Biol 42:313–349

    Article  CAS  Google Scholar 

  • Lau NC, Nath MJ (2012) A model study of heat waves over North America: meteorological aspects and projections for the twenty-first century. J Clim 25:4761–4784

    Article  Google Scholar 

  • Lewis JD, Tissue DT, Strain BR (1996) Seasonal response of photosynthesis to elevated CO2 in loblolly pine (Pinus taeda L.) over two growing seasons. Global Change Biol 2:103–114

    Article  Google Scholar 

  • Li H, Wang XM, Chen L et al (2013) Growth temperature-induced changes in biomass accumulation, photosynthesis and glutathione redox homeostasis as influenced by hydrogen peroxide in cucumber. Plant Physiol Biochem 71:1–10

    Article  PubMed  Google Scholar 

  • Little EL (1971) Atlas of United States trees: volume 1. Conifers and Important Hardwoods. United States Government Printing Office, Washington DC

    Google Scholar 

  • Long SP, Ainsworth EA, Rogers A, Ort DR (2004) Rising atmospheric carbon dioxide: plants FACE the future. Ann Rev Plant Biol 55:591–628

    Article  CAS  Google Scholar 

  • Lynn BH, Healy R, Druyan LM (2007) An analysis of the potential for extreme temperature change based on observations and model simulations. J Clim 20:1539–1554

    Article  Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668

    Article  PubMed  CAS  Google Scholar 

  • Mitchell JF, Lowe J, Wood RA, Vellinga M (2006) Extreme events due to human-induced climate change. Philos Transact A Math Phys Eng Sci 364:2117–2133

    Article  Google Scholar 

  • Murthy R, Zarnoch SJ, Dougherty PM (1997) Seasonal trends of light saturated net photosynthesis and stomatal conductance of loblolly pine trees grown in contrasting environments of nutrition, water and carbon dioxide. Plant Cell Environ 20:558–568

    Article  Google Scholar 

  • Norby RJ, Long TM, Hartz-Rubin JS, O’Neill EG (2000) Nitrogen resorption in senescing tree leaves in a warmer, CO2-enriched atmosphere. Plant Soil 224:15–29

    Article  CAS  Google Scholar 

  • Papageorgiou G (2004) Cholorophyll a fluorescence: a signature of photosynthesis. Springer, Dordrecht, p 820

    Book  Google Scholar 

  • Pataki DE, Oren R, Katul G, Sigmon J (1998) Canopy conductance of Pinus taeda, Liquidambar styraciflua and Quercus phellos under varying atmospheric and soil water conditions. Tree Physiol 18:307–315

    Article  PubMed  Google Scholar 

  • Rogers A, Ellsworth DS (2002) Photosynthetic acclimation of Pinus taeda (loblolly pine) to long-term growth in elevated pCO2 (FACE). Plant Cell Environ 25:851–858

    Article  CAS  Google Scholar 

  • Ruffner JA (1980) Climate of the States. Gale Research Co., Detroit, p 588

    Google Scholar 

  • Sage RF, Kubien DS (2007) The temperature response of C3 and C4 photosynthesis. Plant Cell Environ 30:1086–1106

    Article  PubMed  CAS  Google Scholar 

  • Sage RF, Sharkey TD (1987) The Effect of temperature on the occurrence of O2 and CO2 insensitive photosynthesis in field grown plants. Plant Physiol 84:658–664

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Salvucci ME, Crafts-Brandner SJ (2004) Mechanism for deactivation of Rubisco under moderate heat stress. Physiol Plant 122:513–519

    Article  CAS  Google Scholar 

  • Saxe H, Ellsworth DS, Heath J (1998) Tree and forest functioning in an enriched CO2 atmosphere. New Phytol 139:395–436

    Article  Google Scholar 

  • Schulze ED, Beck E, Müller-Hohenstein K (2005) Plant Ecol. Springer, Berlin, p 702

    Google Scholar 

  • Taub DR, Seemann JR, Coleman JS (2000) Growth in elevated CO2 protects photosynthesis against high-temperature damage. Plant Cell Environ 23:649–656

    Article  CAS  Google Scholar 

  • Teskey RO (1995) A field study of the effects of elevated CO2 on carbon assimilation, stomatal conductance and leaf and branch growth of Pinus taeda trees. Plant Cell Environ 18:565–573

    Article  Google Scholar 

  • Teskey RO (1997) Combined effects of elevated CO2 and air temperature on carbon assimilation of Pinus taeda trees. Plant Cell Environ 20:373–380

    Article  CAS  Google Scholar 

  • Teskey RO, Will RE (1999) Acclimation of loblolly pine (Pinus taeda) seedlings to high temperatures. Tree Physiol 19:519–525

    Article  PubMed  Google Scholar 

  • Teskey RO, Bongarten BC, Cregg BM, Dougherty PM, Hennessey TC (1987) Physiology and genetics of tree growth response to moisture and temperature stress: an examination of the characteristics of loblolly pine (Pinus taeda L.). Tree Physiol 3:41–61

    Article  PubMed  Google Scholar 

  • Tissue DT, Thomas RB, Strain BR (1997) Atmospheric CO2 enrichment increases growth and photosynthesis of Pinus taeda: a 4 year experiment in the field. Plant Cell Environ 20:1123–1134

    Article  Google Scholar 

  • Tranquillini W, Havranek WM, Ecker P (1986) Effects of atmospheric humidity and acclimation temperature on the temperature response of photosynthesis in young Larix decidua Mill. Tree Physiol 1:37–45

    Article  PubMed  Google Scholar 

  • Trenberth KE (1998) Atmospheric moisture residence times and cycling: implications for rainfall rates and climate change. Clim Change 39:667–694

    Article  Google Scholar 

  • Trenberth KE, Jones PD, Ambenje P et al (2007) Observations: surface and atmospheric climate change. In: Solomon S, Qin D et al (eds) IPCC 2007. Cambridge University Press, Cambridge, pp 235–336

    Google Scholar 

  • Valentini R, Epron D, Angelis PD, Matteucci G, Dreyer E (1995) 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

    Article  CAS  Google Scholar 

  • Vierling E (1991) The roles of heat shock proteins in plants. Ann Rev Plant Physiol Mol Biol 42:579–620

    Article  CAS  Google Scholar 

  • Wang D, Heckathorn SA, Barua D, Joshi P, Hamilton EW, Lacroix JJ (2008) Effects of elevated CO2 on the tolerance of photosynthesis to acute heat stress in C3, C4, and CAM species. Am J Bot 95:165–176

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Way DA, Yamori W (2014) Thermal acclimation of photosynthesis: on the importance of adjusting our definitions and accounting for thermal acclimation of respiration. Photosynth Res 119:89–100

    Article  PubMed  CAS  Google Scholar 

  • Wertin TM, McGuire MA, Teskey RO (2010) The influence of elevated temperature, elevated atmospheric CO2 concentration and water stress on net photosynthesis of loblolly pine (Pinus taeda L.) at northern, central and southern sites in its native range. Global Change Biol 16:2089–2103

    Article  Google Scholar 

  • Wertin TM, McGuire MA, Teskey RO (2011) Higher growth temperatures decreased net carbon assimilation and biomass accumulation of northern red oak seedlings near the southern limit of the species range. Tree Physiol 31:1277–1288

    Article  PubMed  CAS  Google Scholar 

  • Wertin TM, McGuire MA, Teskey RO (2012a) Effects of predicted future and current atmospheric temperature and [CO2] and high and low soil moisture on gas exchange and growth of Pinus taeda seedlings at cool and warm sites in the species range. Tree Physiol 32:847–858

    Article  PubMed  CAS  Google Scholar 

  • Wertin TM, McGuire MA, van Iersel M, Ruter JM, Teskey RO (2012b) Effects of elevated temperature and [CO2] on photosynthesis, leaf respiration, and biomass accumulation of Pinus taeda seedlings at a cool and a warm site within the species’ current range. Can J For Res 42:943–957

    Article  CAS  Google Scholar 

  • Whitehead D, Hogan KP, Rogers GND et al (1995) Performance of large open-top chambers for long-term field investigations of tree response to elevated carbon dioxide concentrations. J Biogeogr 22:307–313

    Article  Google Scholar 

  • Will RE, Teskey RO (1997) Effect of irradiance and vapour pressure deficit On stomatal response to CO2 enrichment of four tree species. J Exp Bot 48:2095–2102

    Article  CAS  Google Scholar 

  • Wolkovich EM, Cook BI, Allen JM et al (2012) Warming experiments underpredict plant phenological responses to climate change. Nature 485:494–497

    PubMed  CAS  Google Scholar 

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Author contribution statement

IB performed the analyses, created the figures and designed the manuscript. TBHLM and TMW conducted the measurements and assisted in the analyses. TMW, MAM, and ROT designed the study. MAM, ROT, and KS supervised the work. All authors discussed the results and made substantial contributions to the manuscript.

Acknowledgments

This project was supported by a grant to ROT from the United States Department of Energy NICCR Program (Grant: 07-SC-NICCR-1060). In addition, a travel grant from the CWO, Ghent University, allowing the participation of TBHLM and Lorenz Meire on the project is gratefully acknowledged. The authors appreciate LM’s help with the measuring campaign.

Conflict of interest

The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Laboratory of Plant Ecology, Faculty of Bioscience Engineering, Ghent University, Coupure Links 653, 9000, Ghent, Belgium

    Ingvar Bauweraerts, Tim B. H. L. Mannaerts & Kathy Steppe

  2. Daniel B. Warnell School of Forestry and Natural Resources, University of Georgia, Athens, GA, 30602, USA

    Timothy M. Wertin, Mary Anne McGuire & Robert O. Teskey

  3. Institute for Genomic Biology, University of Illinois, Urbana, IL, 61801, USA

    Timothy M. Wertin

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  1. Ingvar Bauweraerts
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  2. Tim B. H. L. Mannaerts
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  3. Timothy M. Wertin
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  4. Mary Anne McGuire
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  5. Robert O. Teskey
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Correspondence to Ingvar Bauweraerts.

Additional information

Communicated by M. Buckeridge.

I. Bauweraerts and T. B. H. L. Mannaerts contributed equally to this paper.

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468_2014_1057_MOESM1_ESM.tif

Fig. S1 Native distribution range of Pinus taeda L. (Little, 1971), with the locations of the two study sites. The distance between the northern (Athens) and southern (Tifton) sites is 300 km, with a difference in mean air temperature between the two sites of 2.1 °C during the growth period (15 February through 21 August). (TIFF 4273 kb)

468_2014_1057_MOESM2_ESM.tif

Fig. S2 Treatment design for the chambers at the northern site. Clear box indicates ambient temperature; grey box indicates elevated temperature; “X” indicates elevated [CO2]; no “X” indicates ambient [CO2]. Expanded view shows placement of seedling blocks within chamber. The single chamber at the southern site was maintained at ambient temperature and CO2 conditions. (TIFF 3921 kb)

468_2014_1057_MOESM3_ESM.tif

Fig. S3 Mean, maximum, and minimum daily temperature (°C) measured outdoors at 1 m above ground level during the growth period (15 February through 21 August) at the northern (Athens) and southern (Tifton) sites in Georgia, USA. (TIFF 10988 kb)

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Bauweraerts, I., Mannaerts, T.B.H.L., Wertin, T.M. et al. Elevated [CO2] and growth temperature have a small positive effect on photosynthetic thermotolerance of Pinus taeda seedlings. Trees 28, 1515–1526 (2014). https://doi.org/10.1007/s00468-014-1057-3

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