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Plant function and evolutionary biology
RESEARCH ARTICLE

Relationships between climate of origin and photosynthetic responses to an episodic heatwave depend on growth CO2 concentration for Eucalyptus camaldulensis var. camaldulensis

Michael E. Loik A D , Víctor Resco de Dios B C , Renee Smith C and David T. Tissue C
+ Author Affiliations
- Author Affiliations

A Department of Environmental Studies, University of California, Santa Cruz, CA 95064, USA.

B Department of Crop and Forest Sciences, Universitat de Lleida, 25198 Lleida, Spain.

C Hawkesbury Institute for the Environment, Western Sydney University, Richmond, NSW 2753, Australia.

D Corresponding author. Email: mloik@ucsc.edu

Functional Plant Biology 44(11) 1053-1062 https://doi.org/10.1071/FP17077
Submitted: 21 March 2017  Accepted: 28 June 2017   Published: 18 August 2017

Abstract

Stressful episodic weather is likely to affect the C balance of trees as the climate changes, potentially altering survival. However, the role of elevated CO2 concentration ([CO2]) in tolerating off-season episodic extremes is not clear. We tested for interactive effects of elevated CO2 and springtime heat stress on photosynthesis for seven genotypes of Eucalyptus camaldulensis Dehnh. var. camaldulensis, representing its widespread distribution across south-eastern Australia. We grew clonal material under glasshouse conditions of ambient (aCO2; 400 parts per million (ppm)) or elevated (eCO2; 640 ppm) [CO2], and air temperatures of 25 : 17°C (day : night), and measured the electron transport rate in PSII (ETR), stomatal conductance to water vapour (gs) and net CO2 assimilation (A). Measurements were made before, during and after a four-day temperature excursion of 35 : 27°C. ETR and A were ~17% higher for plants grown in eCO2 than in aCO2. Photosynthesis remained stable for plants in eCO2 during the heatwave. Based on the effect size ratio (eCO2 : aCO2), gs and ETR were temporarily affected more by the heatwave than A. A reduction in ETR in eCO2 was the only lasting effect of the heatwave. There were no significant differences among genotypes. Correlations between photosynthesis and climate of origin differed for plants grown in aCO2 compared with eCO2, suggesting potential complex and multiple control points on photosynthesis.

Additional keywords: chlorophyll fluorescence, electron transport, seedling growth, stomatal conductance, temperature stress.


References

Adams WW, Watson AM, Mueh KE, Amiard V, Turgeon R, Ebbert V, Logan BA, Combs AF, Demmig-Adams B (2007) Photosynthetic acclimation in the context of structural constraints to carbon export from leaves. Photosynthesis Research 94, 455–466.
Photosynthetic acclimation in the context of structural constraints to carbon export from leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtl2ks7bE&md5=199d73878d8033e7c4327336016d8bebCAS |

Adams WW, Cohu CM, Muller O, Demmig-Adams B (2013) Foliar phloem infrastructure in support of photosynthesis. Frontiers in Plant Science 4, 194
Foliar phloem infrastructure in support of photosynthesis.Crossref | GoogleScholarGoogle Scholar |

Ainsworth EA, Davey PA, Bernacchi CJ, Dermody OC, Heaton EA, Moore DJ, Morgan PB, Naidu SL, Ra HSY, Zhu XG, Curtis PS, Long SP (2002) A meta-analysis of elevated [CO2] effects on soybean (Glycine max) physiology, growth and yield. Global Change Biology 8, 695–709.
A meta-analysis of elevated [CO2] effects on soybean (Glycine max) physiology, growth and yield.Crossref | GoogleScholarGoogle Scholar |

Allakhverdiev SI, Murata N (2004) Environmental stress inhibits the synthesis de novo of proteins involved in the photodamage–repair cycle of Photosystem II in Synechocystis sp. PCC 6803. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1657, 23–32.
Environmental stress inhibits the synthesis de novo of proteins involved in the photodamage–repair cycle of Photosystem II in Synechocystis sp. PCC 6803.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlt1Wgu7o%3D&md5=9f8db8ff59ef318af55099bbe090e23cCAS |

Allakhverdiev SI, Kreslavski VD, Klimov VV, Los DA, Carpentier R, Mohanty P (2008) Heat stress: an overview of molecular responses in photosynthesis. Photosynthesis Research 98, 541
Heat stress: an overview of molecular responses in photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVOgt7bF&md5=6ec334cbccda4dc96390c894fa94b19bCAS |

Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Kitzberger T, Rigling A, Breshears DD, Hogg ET (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. Forest Ecology and Management 259, 660–684.
A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests.Crossref | GoogleScholarGoogle Scholar |

Arp W (1991) Effects of source–sink relations on photosynthetic acclimation to elevated CO2. Plant, Cell & Environment 14, 869–875.
Effects of source–sink relations on photosynthetic acclimation to elevated CO2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XhsVyns7g%3D&md5=5b6e314332623dd72297f24a0e875c4aCAS |

Ashton DH (1958) The ecology of Eucalyptus regnans F. Muell.: the species and its frost resistance. Australian Journal of Botany 6, 154–176.
The ecology of Eucalyptus regnans F. Muell.: the species and its frost resistance.Crossref | GoogleScholarGoogle Scholar |

Aspinwall MJ, Loik ME, Resco de Dios V, Tjoelker MG, Payton PR, Tissue DT (2014) Utilizing intraspecific variation in phenotypic plasticity to bolster agricultural and forest productivity under climate change. Plant, Cell & Environment 38, 1752–1764.
Utilizing intraspecific variation in phenotypic plasticity to bolster agricultural and forest productivity under climate change.Crossref | GoogleScholarGoogle Scholar |

Asshoff R, Zotz G, Korner C (2006) Growth and phenology of mature temperate forest trees in elevated CO2. Global Change Biology 12, 848–861.
Growth and phenology of mature temperate forest trees in elevated CO2.Crossref | GoogleScholarGoogle Scholar |

Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48.
Fitting linear mixed-effects models using lme4.Crossref | GoogleScholarGoogle Scholar |

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 Ecology 215, 733–746.
Acclimation effects of heat waves and elevated CO2 on gas exchange and chlorophyll fluorescence of northern red oak (Quercus rubra L.) seedlings.Crossref | GoogleScholarGoogle Scholar |

Blackman CJ, Aspinwall MJ, de Dios VR, Smith RA, Tissue DT (2016) Leaf photosynthetic, economics and hydraulic traits are decoupled among genotypes of a widespread species of eucalypt grown under ambient and elevated CO2. Functional Ecology 30, 1491–1500.
Leaf photosynthetic, economics and hydraulic traits are decoupled among genotypes of a widespread species of eucalypt grown under ambient and elevated CO2.Crossref | GoogleScholarGoogle Scholar |

Bowes G (1991) Growth at elevated CO2: photosynthetic responses mediated through Rubisco. Plant, Cell & Environment 14, 795–806.
Growth at elevated CO2: photosynthetic responses mediated through Rubisco.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XhsVyitr4%3D&md5=3fa179a349ad29c6ae73c37c3103b2a4CAS |

Canadell JG, Raupach MR (2008) Managing forests for climate change mitigation. Science 320, 1456–1457.
Managing forests for climate change mitigation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntVWrtbg%3D&md5=70af13bf4f7138b4dff031f21c6409a1CAS |

Cowan T, Purich A, Perkins S, Pezza A, Boschat G, Sadler K (2014) More frequent, longer, and hotter heat waves for Australia in the twenty-first century. Journal of Climate 27, 5851–5871.
More frequent, longer, and hotter heat waves for Australia in the twenty-first century.Crossref | GoogleScholarGoogle Scholar |

Crous KY, Quentin AG, Lin YS, Medlyn BE, Williams DG, Barton CVM, Ellsworth DS (2013) Photosynthesis of temperate Eucalyptus globulus trees outside their native range has limited adjustment to elevated CO2 and climate warming. Global Change Biology 19, 3790–3807.
Photosynthesis of temperate Eucalyptus globulus trees outside their native range has limited adjustment to elevated CO2 and climate warming.Crossref | GoogleScholarGoogle Scholar |

Dillon S, McEvoy R, Baldwin DS, Southerton S, Campbell C, Parsons Y, Rees GN (2015) Genetic diversity of Eucalyptus camaldulensis Dehnh. following population decline in response to drought and altered hydrological regime. Austral Ecology 40, 558–572.
Genetic diversity of Eucalyptus camaldulensis Dehnh. following population decline in response to drought and altered hydrological regime.Crossref | GoogleScholarGoogle Scholar |

Drake JE, Aspinwall MJ, Pfautsch S, Rymer PD, Reich PB, Smith RA, Crous KY, Tissue DT, Ghannoum O, Tjoelker MG (2015) The capacity to cope with climate warming declines from temperate to tropical latitudes in two widely distributed Eucalyptus species. Global Change Biology 21, 459–472.
The capacity to cope with climate warming declines from temperate to tropical latitudes in two widely distributed Eucalyptus species.Crossref | GoogleScholarGoogle Scholar |

Duan HL, Amthor JS, Duursma RA, O’Grady AP, Choat B, Tissue DT (2013) Carbon dynamics of eucalypt seedlings exposed to progressive drought in elevated CO2 and elevated temperature. Tree Physiology 33, 779–792.
Carbon dynamics of eucalypt seedlings exposed to progressive drought in elevated CO2 and elevated temperature.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvVyks7jM&md5=a23daf91a3d1d8b7cd48ebb5029ff18aCAS |

Duan HL, Duursma RA, Huang GM, Smith RA, Choat B, O’Grady AP, Tissue DT (2014) Elevated CO2 does not ameliorate the negative effects of elevated temperature on drought-induced mortality in Eucalyptus radiata seedlings. Plant, Cell & Environment 37, 1598–1613.
Elevated CO2 does not ameliorate the negative effects of elevated temperature on drought-induced mortality in Eucalyptus radiata seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXptlamsLw%3D&md5=a48887b1648ff14380e552cffe13a98eCAS |

Ekman A, Bulow L, Stymne S (2007) Elevated atmospheric CO2 concentration and diurnal cycle induce changes in lipid composition in Arabidopsis thaliana. New Phytologist 174, 591–599.
Elevated atmospheric CO2 concentration and diurnal cycle induce changes in lipid composition in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmsFOktb8%3D&md5=37ddf9d8ee1ebfd07ad24fb92e2f62b2CAS |

Feller U (2016) Drought stress and carbon assimilation in a warming climate: reversible and irreversible impacts. Journal of Plant Physiology 203, 84–94.
Drought stress and carbon assimilation in a warming climate: reversible and irreversible impacts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xls1Gjurs%3D&md5=c91817da838c434d2a3f53b4edcea7eaCAS |

Gauthier PPG, Crous KY, Ayub G, Duan HL, Weerasinghe LK, Ellsworth DS, Tjoelker MG, Evans JR, Tissue DT, Atkin OK (2014) Drought increases heat tolerance of leaf respiration in Eucalyptus globulus saplings grown under both ambient and elevated atmospheric CO2 and temperature. Journal of Experimental Botany 65, 6471–6485.
Drought increases heat tolerance of leaf respiration in Eucalyptus globulus saplings grown under both ambient and elevated atmospheric CO2 and temperature.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xhs1Ont7vF&md5=937b84c872facea47c7802654bb0e99eCAS |

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 & Environment 33, 1671–1681.
Photosynthetic responses of two eucalypts to industrial-age changes in atmospheric CO2 and temperature.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlemsbbL&md5=51dab43bab0b267c7e574ef22e356092CAS |

Gombos Z, Wada H, Hideg E, Murata N (1994) The unsaturation of membrane lipids stabilizes photosynthesis against heat stress. Plant Physiology 104, 563–567.
The unsaturation of membrane lipids stabilizes photosynthesis against heat stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXhvVOgu7c%3D&md5=7ce2dd9c436efba9367c2e55996dc04dCAS |

Gunderson CA, Sholtis JD, Wullschleger SD, Tissue DT, Hanson PJ, Norby RJ (2002) Environmental and stomatal control of photosynthetic enhancement in the canopy of a sweetgum (Liquidambar styraciflua L.) plantation during 3 years of CO2 enrichment. Plant, Cell & Environment 25, 379–393.
Environmental and stomatal control of photosynthetic enhancement in the canopy of a sweetgum (Liquidambar styraciflua L.) plantation during 3 years of CO2 enrichment.Crossref | GoogleScholarGoogle 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 Ecology 148, 183–193.
Effects of extreme high temperature, drought and elevated CO2 on photosynthesis of the Mojave Desert evergreen shrub, Larrea tridentata.Crossref | GoogleScholarGoogle Scholar |

Hamilton EW, 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. Journal of Integrative Plant Biology 50, 1375–1387.
Interactive effects of elevated CO2 and growth temperature on the tolerance of photosynthesis to acute heat stress in C3 and C4 species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVyltb7N&md5=afcf7f20831eb20a9d6300c42f1d8f95CAS |

Hughes L (2003) Climate change and Australia: trends, projections and impacts. Austral Ecology 28, 423–443.
Climate change and Australia: trends, projections and impacts.Crossref | GoogleScholarGoogle Scholar |

Intergovernmental Panel on Climate Change (IPCC) 2014 ‘Synthesis report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change.’ (IPCC, Geneva, Switzerland).

Karschon R, Pinchas L (1971) Variations in heat resistance of ecotypes of Eucalyptus camaldulensis Dehn. and their significance. Australian Journal of Botany 19, 261–272.
Variations in heat resistance of ecotypes of Eucalyptus camaldulensis Dehn. and their significance.Crossref | GoogleScholarGoogle Scholar |

Krall JP, Edwards GE (1992) Relationship between photosystem II activity and CO2 fixation in leaves. Physiologia Plantarum 86, 180–187.
Relationship between photosystem II activity and CO2 fixation in leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XmtlSgsbg%3D&md5=f84c9f939ea416f78c23d59d63f7d203CAS |

Law RD, Crafts-Brandner SJ (1999) Inhibition and acclimation of photosynthesis to heat stress is closely correlated with activation of ribulose-1,5-bisphosphate carboxylase/oxygenase. Plant Physiology 120, 173–182.
Inhibition and acclimation of photosynthesis to heat stress is closely correlated with activation of ribulose-1,5-bisphosphate carboxylase/oxygenase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjt1Sqsrk%3D&md5=8490917571128a5fcdf4a68897eeeb08CAS |

Lewis JD, Phillips NG, Logan BA, Hricko CR, Tissue DT (2011) Leaf photosynthesis, respiration and stomatal conductance in six Eucalyptus species native to mesic and xeric environments growing in a common garden. Tree Physiology 31, 997–1006.
Leaf photosynthesis, respiration and stomatal conductance in six Eucalyptus species native to mesic and xeric environments growing in a common garden.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVCls7jP&md5=c4ea4d3380eb56db47f6cb5937b9cdf9CAS |

Lewis JD, Phillips NG, Logan BA, Smith RA, Aranjuelo I, Clarke S, Offord CA, Frith A, Barbour M, Huxman T, Tissue DT (2015) Rising temperature may negate the stimulatory effect of rising CO2 on growth and physiology of Wollemi pine (Wollemia nobilis). Functional Plant Biology 42, 836–850.
Rising temperature may negate the stimulatory effect of rising CO2 on growth and physiology of Wollemi pine (Wollemia nobilis).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtlajtbvN&md5=03b210f97930f8ac59c6ad242c851767CAS |

Logan BA, Combs A, Myers K, Kent R, Stanley L, Tissue DT (2009) Seasonal response of photosynthetic electron transport and energy dissipation in the eighth year of exposure to elevated atmospheric CO2 (FACE) in Pinus taeda (loblolly pine). Tree Physiology 29, 789–797.
Seasonal response of photosynthetic electron transport and energy dissipation in the eighth year of exposure to elevated atmospheric CO2 (FACE) in Pinus taeda (loblolly pine).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXms1Kgsbk%3D&md5=a93772c5de7a70ca8476e51667fef072CAS |

Logan BA, Hricko CR, Lewis JD, Ghannoum O, Phillips NG, Smith R, Conroy JP, Tissue DT (2010) Examination of pre-industrial and future CO2 reveals the temperature-dependent CO2 sensitivity of light energy partitioning at PSII in eucalypts. Functional Plant Biology 37, 1041–1049.
Examination of pre-industrial and future CO2 reveals the temperature-dependent CO2 sensitivity of light energy partitioning at PSII in eucalypts.Crossref | GoogleScholarGoogle Scholar |

Medlyn BE, Barton CVM, Broadmeadow MSJ, Ceulemans R, De Angelis P, Forstreuter M, Freeman M, Jackson SB, Kellomaki S, Laitat E, Rey A, Roberntz P, Sigurdsson BD, Strassemeyer J, Wang K, Curtis PS, Jarvis PG (2001) Stomatal conductance of forest species after long-term exposure to elevated CO2 concentration: a synthesis. New Phytologist 149, 247–264.
Stomatal conductance of forest species after long-term exposure to elevated CO2 concentration: a synthesis.Crossref | GoogleScholarGoogle Scholar |

Meehl GA, Tebaldi C (2004) More intense, more frequent, and longer lasting heat waves in the 21st century. Science 305, 994–997.
More intense, more frequent, and longer lasting heat waves in the 21st century.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmsVGmtrc%3D&md5=59f0fafb27a0f5227a1d7bd97ffdc0a9CAS |

Meehl GA, Karl T, Easterling DR, Changnon S, Pielke R, Changnon D, Evans J, Groisman PY, Knutson TR, Kunkel KE, Mearns LO, Parmesan C, Pulwarty R, Root T, Sylves RT, Whetton P, Zwiers F (2000) An introduction to trends in extreme weather and climate events: observations, socioeconomic impacts, terrestrial ecological impacts, and model projections. Bulletin of the American Meteorological Society 81, 413–416.
An introduction to trends in extreme weather and climate events: observations, socioeconomic impacts, terrestrial ecological impacts, and model projections.Crossref | GoogleScholarGoogle Scholar |

Moore G, Rowan K, Blake T (1977) Effects of heat on the physiology of seedlings of Eucalyptus obliqua. Functional Plant Biology 4, 283–288.

Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1767, 414–421.
Photoinhibition of photosystem II under environmental stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmt1ygsLw%3D&md5=92714112509f50441fc04f006ffa4bcdCAS |

Nishiyama Y, Allakhverdiev SI, Murata N (2006) A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1757, 742–749.
A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XotVCrsb4%3D&md5=0cf0ac489a9d1bf87b4a834e22161d84CAS |

O’Sullivan OS, Heskel MA, Reich PB, Tjoelker MG, Weerasinghe LK, Penillard A, Zhu LL, Egerton JJG, Bloomfield KJ, Creek D, Bahar NHA, Griffin KL, Hurry V, Meir P, Turnbull MH, Atkin OK (2017) Thermal limits of leaf metabolism across biomes. Global Change Biology 23, 209–223.
Thermal limits of leaf metabolism across biomes.Crossref | GoogleScholarGoogle Scholar |

Oberhuber W, Edwards GE (1993) Temperature dependence of the linkage of quantum yield of photosystem II to CO2 fixation in C4 and C3 plants. Plant Physiology 101, 507–512.
Temperature dependence of the linkage of quantum yield of photosystem II to CO2 fixation in C4 and C3 plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXhs1Gnsrk%3D&md5=05c94e753373f70acd2f7c1720aa5283CAS |

Osmond CB, Austin MP, Berry JA, Billings WD, Boyer JS, Dacey JWH, Nobel PS, Smith SD, Winner WE (1987) Stress physiology and the distribution of plants. Bioscience 37, 38–48.
Stress physiology and the distribution of plants.Crossref | GoogleScholarGoogle Scholar |

Paton D (1980) Eucalyptus physiology. II. Temperature responses. Australian Journal of Botany 28, 555–566.
Eucalyptus physiology. II. Temperature responses.Crossref | GoogleScholarGoogle Scholar |

Polley HW, Tischler CR, Jobnson HB (2006) Elevated atmospheric CO2 magnifies intra-specific variation in seedling growth of honey mesquite: an assessment of relative growth rates. Rangeland Ecology and Management 59, 128–134.
Elevated atmospheric CO2 magnifies intra-specific variation in seedling growth of honey mesquite: an assessment of relative growth rates.Crossref | GoogleScholarGoogle Scholar |

Pryor L (1959) Species distribution and association in Eucalyptus. In ‘Biogeography and ecology in Australia’. (Ed. A Keast) pp. 461–471 (Springer: Dordrecht)

Purich A, Cowan T, Cai WJ, van Rensch P, Uotila P, Pezza A, Boschat G, Perkins S (2014) Atmospheric and oceanic conditions associated with southern Australian heat waves: a CMIP5 analysis. Journal of Climate 27, 7807–7829.
Atmospheric and oceanic conditions associated with southern Australian heat waves: a CMIP5 analysis.Crossref | GoogleScholarGoogle Scholar |

Reddy AR, Rasineni GK, Raghavendra AS (2010) The impact of global elevated CO2 concentration on photosynthesis and plant productivity. Current Science 99, 46–57.

Resco de Dios VR, Loik ME, Smith R, Aspinwall MJ, Tissue DT (2016a) Genetic variation in circadian regulation of nocturnal stomatal conductance enhances carbon assimilation and growth. Plant, Cell & Environment 39, 3–11.
Genetic variation in circadian regulation of nocturnal stomatal conductance enhances carbon assimilation and growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXitVeqtL3L&md5=362393fc98b425b99f99cfc37b324750CAS |

Resco de Dios VR, Mereed TE, Ferrio JP, Tissue DT, Voltas J (2016b) Intraspecific variation in juvenile tree growth under elevated CO2 alone and with O3: a meta-analysis. Tree Physiology 36, 682–693.
Intraspecific variation in juvenile tree growth under elevated CO2 alone and with O3: a meta-analysis.Crossref | GoogleScholarGoogle Scholar |

Roden JS, Ball MC (1996a) The effect of elevated [CO2] on growth and photosynthesis of two Eucalyptus species exposed to high temperatures and water deficits. Plant Physiology 111, 909–919.
The effect of elevated [CO2] on growth and photosynthesis of two Eucalyptus species exposed to high temperatures and water deficits.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XktlKksb4%3D&md5=22542f98d6937abd4d08b0e5bd8b6fc2CAS |

Roden JS, Ball MC (1996b) Growth and photosynthesis of two eucalypt species during high temperature stress under ambient and elevated [CO2]. Global Change Biology 2, 115–128.
Growth and photosynthesis of two eucalypt species during high temperature stress under ambient and elevated [CO2].Crossref | GoogleScholarGoogle Scholar |

Roden JS, Egerton JJG, Ball MC (1999) Effect of elevated [CO2] on photosynthesis and growth of snow gum (Eucalyptus pauciflora) seedlings during winter and spring. Australian Journal of Plant Physiology 26, 37–46.
Effect of elevated [CO2] on photosynthesis and growth of snow gum (Eucalyptus pauciflora) seedlings during winter and spring.Crossref | GoogleScholarGoogle Scholar |

Rollins JA, Habte E, Templer SE, Colby T, Schmidt J, von Korff M (2013) Leaf proteome alterations in the context of physiological and morphological responses to drought and heat stress in barley (Hordeum vulgare L.). Journal of Experimental Botany 64, 3201–3212.
Leaf proteome alterations in the context of physiological and morphological responses to drought and heat stress in barley (Hordeum vulgare L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1CktL%2FF&md5=7a4b0ec8c89874c5d7293d403843afa9CAS |

Sage RF, Sharkey TD, Seemann JR (1989) Acclimation of photosynthesis to elevated CO2 in five C3 species. Plant Physiology 89, 590–596.
Acclimation of photosynthesis to elevated CO2 in five C3 species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXktVCntr0%3D&md5=a294c15cd8237e629c48ced253891e47CAS |

Salvucci ME, Crafts‐Brandner SJ (2004) Inhibition of photosynthesis by heat stress: the activation state of Rubisco as a limiting factor in photosynthesis. Physiologia Plantarum 120, 179–186.
Inhibition of photosynthesis by heat stress: the activation state of Rubisco as a limiting factor in photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtFSltr8%3D&md5=6f2eabed1354f6ce92dfe760b8cb164eCAS |

Shanmugam S, Kjaer KH, Ottosen CO, Rosenqvist E, Sharma DK, Wollenweber B (2013) The alleviating effect of elevated CO2 on heat stress susceptibility of two wheat (Triticum aestivum L.) cultivars. Journal Agronomy & Crop Science 199, 340–350.
The alleviating effect of elevated CO2 on heat stress susceptibility of two wheat (Triticum aestivum L.) cultivars.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsVShsrnP&md5=0b67be160ccf5d17e5cad87f80d23333CAS |

Sharkey TD (1985) Photosynthesis in intact leaves of C3 plants: physics, physiology and rate limitations. Botanical Review 51, 53–105.
Photosynthesis in intact leaves of C3 plants: physics, physiology and rate limitations.Crossref | GoogleScholarGoogle Scholar |

Shaw MR, Zavaleta ES, Chiariello NR, Cleland EE, Mooney HA, Field CB (2002) Grassland responses to global environmental changes suppressed by elevated CO2. Science 298, 1987–1990.
Grassland responses to global environmental changes suppressed by elevated CO2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xpt1WisLo%3D&md5=faa693f5ed667d559ae2964ce2ea9a79CAS |

Slatyer R (1977) Altitudinal variation in the photosynthetic characteristics of snow gum, Eucalyptus pauciflora Sieb. ex Spreng. III. Temperature response of material grown in contrasting thermal environments. Functional Plant Biology 4, 301–312.

Slatyer R, Ferrar P (1977) Altitudinal variation in the photosynthetic characteristics of snow gum, Eucalyptus pauciflora Sieb. ex Spreng. II. Effects of growth temperature under controlled conditions. Functional Plant Biology 4, 289–299.

Sun ZH, Hve K, Vislap V, Niinemets U (2013) Elevated CO2 magnifies isoprene emissions under heat and improves thermal resistance in hybrid aspen. Journal of Experimental Botany 64, 5509–5523.
Elevated CO2 magnifies isoprene emissions under heat and improves thermal resistance in hybrid aspen.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXotlCh&md5=d361d23e70e3daad34037d777f256b23CAS |

Tissue DT, Oechel WC (1987) Response of Eriophorum vaginatum to elevated CO2 and temperature in the Alaskan tussock tundra. Ecology 68, 401–410.
Response of Eriophorum vaginatum to elevated CO2 and temperature in the Alaskan tussock tundra.Crossref | GoogleScholarGoogle 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 & Environment 20, 1123–1134.
Atmospheric CO2 enrichment increases growth and photosynthesis of Pinus taeda: a 4 year experiment in the field.Crossref | GoogleScholarGoogle 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. American Journal of Botany 95, 165–176.
Effects of elevated CO2 on the tolerance of photosynthesis to acute heat stress in C3, C4, and CAM species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXis1Wiurc%3D&md5=3838f7dec1e3745166fcb007af04c28eCAS |

Wang D, Heckathorn SA, Wang XZ, Philpott SM (2012) A meta-analysis of plant physiological and growth responses to temperature and elevated CO2. Oecologia 169, 1–13.
A meta-analysis of plant physiological and growth responses to temperature and elevated CO2.Crossref | GoogleScholarGoogle Scholar |

Wang D, Fan JZ, Heckathorn SA (2014) Acclimation of photosynthetic tolerance to acute heat stress at elevated CO2 and N. Plant Science 226, 162–171.
Acclimation of photosynthetic tolerance to acute heat stress at elevated CO2 and N.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXpvVarsbc%3D&md5=8da38aabb7cb69cdd4a6b1a12ea4124aCAS |

Weis E, Berry JA (1988) Plants and high temperature stress. In: ‘Symposia of the Society for Experimental Biology Number XLII’ (Eds SP Long, FI Woodward) pp. 329–346. (The Company of Biologist: Cambridge, UK)

Zeppel MJB, Lewis JD, Chaszar B, Smith RA, Medlyn BE, Huxman TE, Tissue DT (2012) Nocturnal stomatal conductance responses to rising CO2, temperature and drought. New Phytologist 193, 929–938.
Nocturnal stomatal conductance responses to rising CO2, temperature and drought.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XivVyhtLo%3D&md5=6b5200bb3ce8bbbb2f5cd078df14bb65CAS |