Rising temperature may negate the stimulatory effect of rising CO2 on growth and physiology of Wollemi pine (Wollemia nobilis)
James D. Lewis A B , Nathan G. Phillips A C , Barry A. Logan A D , Renee A. Smith A , Iker Aranjuelo E , Steve Clarke F , Catherine A. Offord G , Allison Frith G H , Margaret Barbour H , Travis Huxman I and David T. Tissue A JA University of Western Sydney, Hawkesbury Institute for the Environment, Richmond, NSW 2753, Australia.
B Fordham University, Louis Calder Center – Biological Field Station, Center for Urban Ecology and Department of Biological Sciences, Armonk, NY 10504, USA.
C Department of Geography and Environment, Boston University, Boston, MA 02215, USA.
D Department of Biology, Bowdoin College, Brunswick, ME 04011, USA.
E Plant Biology and Ecology Department, Science and Technology Faculty, University of the Basque Country, Barrio Sarriena, 48940 Leioa, Spain.
F University of Western Sydney, Capital Works and Facilities, Richmond, NSW 2753, Australia.
G The Royal Botanic Gardens and Domain Trust, The Australian PlantBank, The Australian Botanic Garden, Mount Annan, NSW 2567, Australia.
H Faculty of Agriculture and Environment, The University of Sydney, NSW 2006, Australia.
I Ecology and Evolutionary Biology, University of California, Irvine, CA 92697, USA.
J Corresponding author. Email: d.tissue@uws.edu.au
Functional Plant Biology 42(9) 836-850 https://doi.org/10.1071/FP14256
Submitted: 18 September 2014 Accepted: 4 May 2015 Published: 24 June 2015
Abstract
Rising atmospheric [CO2] is associated with increased air temperature, and this warming may drive many rare plant species to extinction. However, to date, studies on the interactive effects of rising [CO2] and warming have focussed on just a few widely distributed plant species. Wollemi pine (Wollemia nobilis W.G.Jones, K.D.Hill, & J.M.Allen), formerly widespread in Australia, was reduced to a remnant population of fewer than 100 genetically indistinguishable individuals. Here, we examined the interactive effects of three [CO2] (290, 400 and 650 ppm) and two temperature (ambient, ambient + 4°C) treatments on clonally-propagated Wollemi pine grown for 17 months in glasshouses under well-watered and fertilised conditions. In general, the effects of rising [CO2] and temperature on growth and physiology were not interactive. Rising [CO2] increased shoot growth, light-saturated net photosynthetic rates (Asat) and net carbon gain. Higher net carbon gain was due to increased maximum apparent quantum yield and reduced non-photorespiratory respiration in the light, which also reduced the light compensation point. In contrast, increasing temperature reduced stem growth and Asat. Compensatory changes in mesophyll conductance and stomatal regulation suggest a narrow functional range of optimal water and CO2 flux co-regulation. These results suggest Asat and growth of the surviving genotype of Wollemi pine may continue to increase with rising [CO2], but increasing temperatures may offset these effects, and challenges to physiological and morphological controls over water and carbon trade-offs may push the remnant wild population of Wollemi pine towards extinction.
Additional keywords: elevated [CO2], growth, photosynthesis, photosynthetic capacity, photosynthetic light response, pre-industrial [CO2], stomatal conductance.
References
Ainsworth EA, Long SP (2005) What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytologist 165, 351–372.| What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2.Crossref | GoogleScholarGoogle Scholar | 15720649PubMed |
Ainsworth EA, Rogers AL (2007) The response of photosynthesis and stomatal conductance to rising CO2: mechanisms and environmental interactions. Plant, Cell & Environment 30, 258–270.
| The response of photosynthesis and stomatal conductance to rising CO2: mechanisms and environmental interactions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjtlemu78%3D&md5=325a57fef90ea2716d3a761aa7efcd6aCAS |
Allen LH, Vu JCV (2009) Carbon dioxide and high temperature effects on growth of young orange trees in a humid, subtropical environment. Agricultural and Forest Meteorology 149, 820–830.
| Carbon dioxide and high temperature effects on growth of young orange trees in a humid, subtropical environment.Crossref | GoogleScholarGoogle Scholar |
Aranjuelo I, Ebbets AL, Evans RD, Tissue DT, Nogués S, van Gestel N, Payton P, Ebbert V, Adams III WW, Nowak RS, Smith SD (2011) Maintenance of C sinks sustains enhanced C assimilation during long-term exposure to elevated [CO2] in Mojave Desert shrubs. Oecologia 167, 339–354.
| Maintenance of C sinks sustains enhanced C assimilation during long-term exposure to elevated [CO2] in Mojave Desert shrubs.Crossref | GoogleScholarGoogle Scholar | 21516309PubMed |
Aranjuelo I, Sanz-Sáez Á, Jauregui I, Irigoyen JJ, Araus JL, Sánchez-Díaz M, Erice G (2013) Harvest index, a parameter conditioning responsiveness of wheat plants to elevated CO2. Journal of Experimental Botany 64, 1879–1892.
| Harvest index, a parameter conditioning responsiveness of wheat plants to elevated CO2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmslSltLc%3D&md5=43830cc96665b83c4fba9e9f99f6d343CAS | 23564953PubMed |
Atkin OK, Bruhn D, Hurry VM, Tjoelker MG (2005) Evans Review No. 2: The hot and the cold: unravelling the variable response of plant respiration to temperature. Functional Plant Biology 32, 87–105.
| Evans Review No. 2: The hot and the cold: unravelling the variable response of plant respiration to temperature.Crossref | GoogleScholarGoogle Scholar |
Baker JT, Allen LH, Boote KJ (1990) Growth and yield responses of rice to carbon dioxide concentration. The Journal of Agricultural Science 115, 313–320.
| Growth and yield responses of rice to carbon dioxide concentration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXhtFylt7c%3D&md5=06186ac126afe9a9bcbc8da89bd38ee1CAS |
Banks JCG (2002) Wollemi pine: tree find of the 20th Century. In ‘Australia’s ever-changing forests. Proceedings of the fifth national conference on Australian forest history’. (Eds JG Dargavel, B Libbis) pp. 85–89. (CRES: Canberra)
Barbour MM, Farquhar GD, Hanson DT, Bickford CP, Powers H, McDowell NG (2007) A new measurement technique reveals temporal variation in δ18O of leaf-respired CO2. Plant, Cell & Environment 30, 456–468.
| A new measurement technique reveals temporal variation in δ18O of leaf-respired CO2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXksVemu7w%3D&md5=b9937980ec990db603a5291abbe0b209CAS |
Bernacchi CJ, Pimentel C, Long SP (2003) In vivo temperature response functions of parameters required to model RuBP-limited photosynthesis. Plant, Cell & Environment 26, 1419–1430.
| In vivo temperature response functions of parameters required to model RuBP-limited photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXotFyru7o%3D&md5=69c4d76494e42bdd235db63eef3343a0CAS |
Bunce JA (2014) Limitations to soybean photosynthesis at elevated carbon dioxide in free-air enrichment and open top chamber systems. Plant Science 226, 131–135.
| Limitations to soybean photosynthesis at elevated carbon dioxide in free-air enrichment and open top chamber systems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXjsVWnur4%3D&md5=ebdd86caf864ebb99910ec5251bb894bCAS | 25113458PubMed |
Cowling SA, Sage RF (1998) Interactive effects of low atmospheric CO2 and elevated temperature on growth, photosynthesis and respiration in Phaseolus vulgaris. Plant, Cell & Environment 21, 427–435.
| Interactive effects of low atmospheric CO2 and elevated temperature on growth, photosynthesis and respiration in Phaseolus vulgaris.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXksFKku74%3D&md5=8b170b16fdbf7b212ae1f6ef5c023bb2CAS |
Delieu T, Walker DA (1981) Polarographic measurement of photosynthetic oxygen evolution by leaf discs. New Phytologist 89, 165–178.
| Polarographic measurement of photosynthetic oxygen evolution by leaf discs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XjtV2ltA%3D%3D&md5=74380977b490417e9bb154a2040de1a6CAS |
Dippery JK, Tissue DT, Thomas RB, Strain BR (1995) Effects of low and elevated CO2 on C3 and C4 annuals. I. Growth and biomass allocation. Oecologia 101, 13–20.
| Effects of low and elevated CO2 on C3 and C4 annuals. I. Growth and biomass allocation.Crossref | GoogleScholarGoogle Scholar |
Ellsworth DS, Reich PB, Naumburg ES, Koch GW, Kubiske ME, Smith SD (2004) Photosynthesis, carboxylation and leaf nitrogen responses of 16 species to elevated pCO2 across four free-air CO2 enrichment experiments in forest, grassland and desert. Global Change Biology 10, 2121–2138.
| Photosynthesis, carboxylation and leaf nitrogen responses of 16 species to elevated pCO2 across four free-air CO2 enrichment experiments in forest, grassland and desert.Crossref | GoogleScholarGoogle Scholar |
Evans JR, Schortemeyer M, McFarlane N, Atkin OK (2000) Photosynthetic characteristics of 10 Acacia species grown under ambient and elevated atmospheric CO2. Australian Journal of Plant Physiology 27, 13–25.
Farquhar GD, Sharkey TD (1982) Stomatal conductance and photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 33, 317–345.
| Stomatal conductance and photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XktlKjs7o%3D&md5=6ce628bdcc867afe7bef5e721d61fd5cCAS |
Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149, 78–90.
| A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXksVWrt7w%3D&md5=580ad8465ff46edd49bd8f41674c5486CAS | 24306196PubMed |
Farquhar GD, O’Leary MH, Berry JA (1982) On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Australian Journal of Plant Physiology 9, 121–137.
| On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XhsF2ms70%3D&md5=db544bd1d696e70c100aef500258c036CAS |
Franks PJ, Adams MA, Amthor JS, Barbour MM, Berry JA, Ellsworth DS, Farquhar GD, Ghannoum O, Lloyd J, McDowell N, Norby RJ, Tissue DT, von Caemmerer S (2013) Sensitivity of plants to changing atmospheric CO2 concentration: from the geological past to the next century. New Phytologist 197, 1077–1094.
| Sensitivity of plants to changing atmospheric CO2 concentration: from the geological past to the next century.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXitVOjtbc%3D&md5=c7801b33c01337184a9ecb8b5fbcc7c9CAS | 23346950PubMed |
Gallagher SJ, Greenwood DR, Taylor D, Smith AJ, Wallace MW, Holdgate GR (2003) The Pliocene climatic and environmental evolution of southeastern Australia: evidence from the marine and terrestrial realm. Palaeogeography, Palaeoclimatology, Palaeoecology 193, 349–382.
| The Pliocene climatic and environmental evolution of southeastern Australia: evidence from the marine and terrestrial realm.Crossref | GoogleScholarGoogle Scholar |
Gerhart LM, Ward JK (2010) Plant responses to low [CO2] of the past. New Phytologist 188, 674–695.
| Plant responses to low [CO2] of the past.Crossref | GoogleScholarGoogle Scholar | 20840509PubMed |
Gerhart LM, Harris JM, Nippert JB, Sandquist DR, Ward JK (2012) Glacial trees from the La Brea tar pits show physiological constraints of low CO2. New Phytologist 194, 63–69.
| Glacial trees from the La Brea tar pits show physiological constraints of low CO2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XltlGiurc%3D&md5=72e828f0cc95287ce26e3fecf93edcb6CAS | 22187970PubMed |
Ghannoum O, Phillips NG, Conroy JP, Smith RA, Attard RD, Woodfield R, Logan BA, Lewis JD, Tissue DT (2010a) Exposure to preindustrial, current and future atmospheric CO2 and temperature differentially affects growth and photosynthesis in Eucalyptus. Global Change Biology 16, 303–319.
| Exposure to preindustrial, current and future atmospheric CO2 and temperature differentially affects growth and photosynthesis in Eucalyptus.Crossref | GoogleScholarGoogle Scholar |
Ghannoum O, Phillips NG, Sears MA, Logan BA, Lewis JD, Conroy JP, Tissue DT (2010b) 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=87a6802999146e8c1e4cea98b2543406CAS |
Gill RA, Polley HW, Johnson HB, Anderson LJ, Maherali H, Jackson RB (2002) Nonlinear grassland responses to past and future atmospheric CO2. Nature 417, 279–282.
| Nonlinear grassland responses to past and future atmospheric CO2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xjs1agt7o%3D&md5=47865c81035f509c28db222f38feae6bCAS | 12015601PubMed |
Griffin KL, Tissue DT, Turnbull MH, Whitehead D (2000) The onset of photosynthetic acclimation to elevated CO2 partial pressure in field-grown Pinus radiata D.Don. after 4 years. Plant, Cell & Environment 23, 1089–1098.
| The onset of photosynthetic acclimation to elevated CO2 partial pressure in field-grown Pinus radiata D.Don. after 4 years.Crossref | GoogleScholarGoogle Scholar |
Grulke NE, Hom JL, Roberts SW (1993) Physiological adjustment of two full-sib families of ponderosa pine to elevated CO2. Tree Physiology 12, 391–401.
| Physiological adjustment of two full-sib families of ponderosa pine to elevated CO2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXlvF2ls74%3D&md5=05080ae115ebb14995645d206285c2e8CAS | 14969909PubMed |
Haworth M, Elliott-Kingston C, McElwain JC (2011) The stomatal CO2 proxy does not saturate at high atmospheric CO2 concentrations: evidence from stomatal index responses of Araucariaceae conifers. Oecologia 167, 11–19.
| The stomatal CO2 proxy does not saturate at high atmospheric CO2 concentrations: evidence from stomatal index responses of Araucariaceae conifers.Crossref | GoogleScholarGoogle Scholar | 21461935PubMed |
Huxman TE, Monson RK (2003) Stomatal responses of C3, C3-C4 and C4 Flaveria species to light and intercellular CO2 concentration: implications for the evolution of stomatal behaviour. Plant, Cell & Environment 26, 313–322.
| Stomatal responses of C3, C3-C4 and C4 Flaveria species to light and intercellular CO2 concentration: implications for the evolution of stomatal behaviour.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhslOgur0%3D&md5=ab7c06bf079d53296c9fa544e1e615b8CAS |
Jahan E, Amthor J, Farquhar G, Trethowan R, Barbour MM (2014) Variation in mesophyll conductance among Australian wheat genotypes. Functional Plant Biology 41, 568–580.
| Variation in mesophyll conductance among Australian wheat genotypes.Crossref | GoogleScholarGoogle Scholar |
Kellomäki S, Wang K (1996) Photosynthetic response to needle water potentials in Scots pine after a four-year exposure to elevated CO2 and temperature. Tree Physiology 16, 765–772.
| Photosynthetic response to needle water potentials in Scots pine after a four-year exposure to elevated CO2 and temperature.Crossref | GoogleScholarGoogle Scholar | 14871683PubMed |
Kershaw AP (1994) Pleistocene vegetation of the humid tropics of northeastern Queensland, Australia. Palaeogeography, Palaeoclimatology, Palaeoecology 109, 399–412.
| Pleistocene vegetation of the humid tropics of northeastern Queensland, Australia.Crossref | GoogleScholarGoogle Scholar |
Kirschbaum MUF (1994) The sensitivity of C3 photosynthesis to increasing CO2 concentration: a theoretical analysis of its dependence on temperature and background CO2 concentration. Plant, Cell & Environment 17, 747–754.
| The sensitivity of C3 photosynthesis to increasing CO2 concentration: a theoretical analysis of its dependence on temperature and background CO2 concentration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXlslGns70%3D&md5=7ebbf457415b0ffee6ec7d9ddfa7df1eCAS |
Körner C (2006) Plant CO2 responses: an issue of definition, time and resource supply. New Phytologist 172, 393–411.
| Plant CO2 responses: an issue of definition, time and resource supply.Crossref | GoogleScholarGoogle Scholar | 17083672PubMed |
Leverenz JW, Jarvis PG (1979) Photosynthesis in Sitka spruce. VIII. The effects of light flux density and direction on the rate of net photosynthesis and the stomatal conductance of needles. Journal of Applied Ecology 16, 919–932.
| Photosynthesis in Sitka spruce. VIII. The effects of light flux density and direction on the rate of net photosynthesis and the stomatal conductance of needles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXks1Kns70%3D&md5=396a829997e88fee6e807cf6236d7eceCAS |
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 Biology 2, 103–114.
| Seasonal response of photosynthesis to elevated CO2 in loblolly pine (Pinus taeda L) over two growing seasons.Crossref | GoogleScholarGoogle Scholar |
Lewis JD, Olszyk D, Tingey DT (1999) Seasonal patterns of photosynthetic light response in Douglas-fir seedlings subjected to elevated atmospheric CO2 and temperature. Tree Physiology 19, 243–252.
| Seasonal patterns of photosynthetic light response in Douglas-fir seedlings subjected to elevated atmospheric CO2 and temperature.Crossref | GoogleScholarGoogle Scholar | 12651567PubMed |
Lewis JD, McKane RB, Tingey DT, Beedlow PA (2000) Vertical gradients in photosynthetic light response within an old-growth Douglas-fir and western hemlock canopy. Tree Physiology 20, 447–456.
| Vertical gradients in photosynthetic light response within an old-growth Douglas-fir and western hemlock canopy.Crossref | GoogleScholarGoogle Scholar | 12651440PubMed |
Lewis JD, Lucash M, Olszyk D, Tingey DT (2001) Seasonal patterns of photosynthesis in Douglas fir seedlings during the third and fourth year of exposure to elevated CO2 and temperature. Plant, Cell & Environment 24, 539–548.
| Seasonal patterns of photosynthesis in Douglas fir seedlings during the third and fourth year of exposure to elevated CO2 and temperature.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkt1OitL4%3D&md5=91cf80d1ef5e917657018aec40fbfdc7CAS |
Lewis JD, Lucash M, Olszyk DM, Tingey DT (2002a) Stomatal responses of Douglas-fir seedlings to elevated carbon dioxide and temperature during the third and fourth years of exposure. Plant, Cell & Environment 25, 1411–1421.
| Stomatal responses of Douglas-fir seedlings to elevated carbon dioxide and temperature during the third and fourth years of exposure.Crossref | GoogleScholarGoogle Scholar |
Lewis JD, Wang XZ, Griffin KL, Tissue DT (2002b) Effects of age and ontogeny on photosynthetic responses of a determinate annual plant to elevated CO2 concentrations. Plant, Cell & Environment 25, 359–368.
| Effects of age and ontogeny on photosynthetic responses of a determinate annual plant to elevated CO2 concentrations.Crossref | GoogleScholarGoogle Scholar |
Lewis JD, Lucash M, Olszyk DM, Tingey DT (2004) Relationships between needle nitrogen concentration and photosynthetic responses of Douglas-fir seedlings to elevated CO2 and temperature. New Phytologist 162, 355–364.
| Relationships between needle nitrogen concentration and photosynthetic responses of Douglas-fir seedlings to elevated CO2 and temperature.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXksVWjur8%3D&md5=75e7784a30e8f71ec9ac643d50ffddb8CAS |
Lewis JD, Ward JK, Tissue DT (2010) Phosphorus supply drives nonlinear responses of cottonwood (Populus deltoides) to increases in CO2 concentration from glacial to future concentrations. New Phytologist 187, 438–448.
| Phosphorus supply drives nonlinear responses of cottonwood (Populus deltoides) to increases in CO2 concentration from glacial to future concentrations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVSks7rM&md5=d40ccf596bd2732bedc2958463cdf669CAS | 20524990PubMed |
Lewis JD, Smith RA, Ghannoum O, Logan BA, Phillips NG, Tissue DT (2013) Industrial-age changes in atmospheric [CO2] and temperature differentially alter responses of faster- and slower-growing Eucalyptus seedlings to short-term drought. Tree Physiology 33, 475–488.
| Industrial-age changes in atmospheric [CO2] and temperature differentially alter responses of faster- and slower-growing Eucalyptus seedlings to short-term drought.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXosVehsbw%3D&md5=7695817dd990ead2f51a2e0cc00959adCAS | 23677118PubMed |
Li X-P, Bjorkman O, Shih C, Grossman AR, Rosenquist M, Jansson S, Niyogi KK (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403, 391–395.
| A pigment-binding protein essential for regulation of photosynthetic light harvesting.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXps1ehsQ%3D%3D&md5=96d1bdbed363f9d260cf9bc85801ab3aCAS | 10667783PubMed |
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=24c93dc088facc1516395ae0be304202CAS | 19364706PubMed |
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 |
Long SP (1991) Modification of the response of photosynthetic productivity to rising temperature by atmospheric CO2 concentrations: has its importance been underestimated? Plant, Cell & Environment 14, 729–739.
| Modification of the response of photosynthetic productivity to rising temperature by atmospheric CO2 concentrations: has its importance been underestimated?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XhsVyns7s%3D&md5=b240011b9a2f37daa5b5a34d097c0a31CAS |
Long SP, Drake BG (1991) Effect of the long-term elevation of CO2 concentration in the field on the quantum yield of photosynthesis of the C3 sedge, Scirpus olneyi. Plant Physiology 96, 221–226.
| Effect of the long-term elevation of CO2 concentration in the field on the quantum yield of photosynthesis of the C3 sedge, Scirpus olneyi.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXks1ylu7c%3D&md5=ac567e1b353adf0d96869cd87e146b86CAS | 16668155PubMed |
MacPhail MK, Hill K, Partridge AD, Truswell EM (1995) ‘Wollemi Pine’ - old pollen records for a newly discovered genus of gymnosperms. Geology Today 11, 48–50.
Marshall B, Biscoe PV (1980) A model for C3 leaves describing the dependence of net photosynthesis on irradiance: II. Application to the analysis of flag leaf photosynthesis. Journal of Experimental Botany 31, 41–48.
| A model for C3 leaves describing the dependence of net photosynthesis on irradiance: II. Application to the analysis of flag leaf photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXksVWkurY%3D&md5=dd66cecd8edd1b038ab3532453379843CAS |
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 |
Moore BD, Cheng SH, Sims D, Seemann JR (1999) The biochemical and molecular basis for photosynthetic acclimation to elevated atmospheric CO2. Plant, Cell & Environment 22, 567–582.
| The biochemical and molecular basis for photosynthetic acclimation to elevated atmospheric CO2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXksVartL0%3D&md5=4de2add07fd4c9ae159f4484ac659f27CAS |
Morison JIL, Lawlor DW (1999) Interactions between increasing CO2 concentration and temperature on plant growth. Plant, Cell & Environment 22, 659–682.
| Interactions between increasing CO2 concentration and temperature on plant growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXksVartLc%3D&md5=87153b6c1d0f15ba5ff96edf915b9062CAS |
Norby RJ, DeLucia EH, Gielen B, Calfapietra C, Giardina CP, King JS, Ledford J, McCarthy HR, Moore DJP, Ceulemans R, De Angelis P, Finzi AC, Karnosky DF, Kubiske ME, Lukac M, Pregitzer KS, Scarascia-Mugnozza GE, Schlesinger WH, Oren R (2005) Forest response to elevated CO2 is conserved across a broad range of productivity. Proceedings of the National Academy of Sciences of the United States of America 102, 18052–18056.
| Forest response to elevated CO2 is conserved across a broad range of productivity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlersr3N&md5=257c3663c637660204f2e3199e474ca4CAS | 16330779PubMed |
Offord CA (2011) Pushed to the limit: consequences of climate change for the Araucariaceae: a relictual rain forest family. Annals of Botany 108, 347–357.
| Pushed to the limit: consequences of climate change for the Araucariaceae: a relictual rain forest family.Crossref | GoogleScholarGoogle Scholar | 21727080PubMed |
Offord CA, Meagher PF, Zimmer HC (2014) Growing up or growing out? How soil pH and light affect seedling growth of a relictual rainforest tree. AoB Plants 6, plu011
| Growing up or growing out? How soil pH and light affect seedling growth of a relictual rainforest tree.Crossref | GoogleScholarGoogle Scholar | 24790132PubMed |
Ögren E, Evans JR (1993) Photosynthetic light response curves. I. The influence of CO2 partial pressure and leaf inversion. Planta 189, 182–190.
| Photosynthetic light response curves. I. The influence of CO2 partial pressure and leaf inversion.Crossref | GoogleScholarGoogle Scholar |
Peakall R, Ebert D, Scott LJ, Meagher PF, Offord CA (2003) Comparative genetic study confirms exceptionally low genetic variation in the ancient and endangered relictual conifer, Wollemia nobilis (Araucariaceae). Molecular Ecology 12, 2331–2343.
| Comparative genetic study confirms exceptionally low genetic variation in the ancient and endangered relictual conifer, Wollemia nobilis (Araucariaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXnvVSgt7w%3D&md5=eceb8b86b11f975f0c73f09c0350bf88CAS | 12919472PubMed |
Pohio KE, Wallace HM, Peters RF, Smith TE, Trueman SJ (2005) Cuttings of Wollemi pine tolerate moderate photoinhibition and remain highly capable of root formation. Trees 19, 587–595.
| Cuttings of Wollemi pine tolerate moderate photoinhibition and remain highly capable of root formation.Crossref | GoogleScholarGoogle Scholar |
Prioul JL, Chartier P (1977) Partitioning of transfer and carboxylation components of intracellular resistance to photosynthetic CO2 fixation: a critical analysis of the methods used. Annals of Botany 41, 789–800.
Robinson JM (1994) Speculations on carbon dioxide starvation, late tertiary evolution of stomatal regulation and floristic modernization. Plant, Cell & Environment 17, 345–354.
| Speculations on carbon dioxide starvation, late tertiary evolution of stomatal regulation and floristic modernization.Crossref | GoogleScholarGoogle Scholar |
Saxe H, Ellsworth DS, Heath J (1998) Tree and forest functioning in an enriched CO2 atmosphere. New Phytologist 139, 395–436.
| Tree and forest functioning in an enriched CO2 atmosphere.Crossref | GoogleScholarGoogle Scholar |
Setoguchi H, Asakawa Osawa T, Pintaud J-C, Jaffré T, Veillon J-M (1998) Phylogenetic relationships within Araucariaceae based on rbcL gene sequences. American Journal of Botany 85, 1507–1516.
| Phylogenetic relationships within Araucariaceae based on rbcL gene sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXkvVSr&md5=14590b2d044bc1254bd4ea906d24c637CAS | 21680310PubMed |
Shapiro JB, Griffin KL, Lewis JD, Tissue DT (2004) Response of Xanthium strumarium leaf respiration in the light to elevated CO2 concentration, nitrogen availability and temperature. New Phytologist 162, 377–386.
| Response of Xanthium strumarium leaf respiration in the light to elevated CO2 concentration, nitrogen availability and temperature.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXksVWjur0%3D&md5=6348981f16bca5f179933ccf518ae123CAS |
Sharkey TD, Bernacchi CJ, Farquhar GD, Singsaas EL (2007) Fitting photosynthetic carbon dioxide response curves for C3 leaves. Plant, Cell & Environment 30, 1035–1040.
| Fitting photosynthetic carbon dioxide response curves for C3 leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVeiur3F&md5=82578db68694d79cb87c996f505523e8CAS |
Smith RA, Lewis JD, Ghannoum O, Tissue DT (2012) Leaf structural responses to pre-industrial, current and elevated atmospheric [CO2] and temperature affect leaf function in Eucalyptus sideroxylon. Functional Plant Biology 39, 285–296.
| Leaf structural responses to pre-industrial, current and elevated atmospheric [CO2] and temperature affect leaf function in Eucalyptus sideroxylon.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XmtVGkt7s%3D&md5=150990a70da7068b69278e4703e87702CAS |
Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (2007) ‘Climate change 2007. The physical science basis. Contribution of Working Group I to the fourth assessment report of the Intergovernmental Panel on Climate Change’. (Cambridge University Press: Cambridge, UK)
Stinziano JR, Way DA (2014) Combined effects of rising [CO2] and temperature on boreal forests: growth, physiology and limitations. Botany 92, 425–436.
| Combined effects of rising [CO2] and temperature on boreal forests: growth, physiology and limitations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXotFWktrs%3D&md5=db034cdd51079cf3914afe77e6be9598CAS |
Tissue DT, Lewis JD (2012) Learning from the past: how low [CO2] studies inform plant and ecosystem response to future climate change. New Phytologist 194, 4–6.
| Learning from the past: how low [CO2] studies inform plant and ecosystem response to future climate change.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XltlGiur4%3D&md5=90587acd5d7dc50070c46f1937901bf8CAS | 22364117PubMed |
Tissue DT, Griffin KL, Ball JT (1999) Photosynthetic adjustment in field-grown ponderosa pine trees after six years of exposure to elevated CO2. Tree Physiology 19, 221–228.
| Photosynthetic adjustment in field-grown ponderosa pine trees after six years of exposure to elevated CO2.Crossref | GoogleScholarGoogle Scholar | 12651564PubMed |
Tjoelker MG, Oleksyn J, Reich PB (1998) Seedlings of five boreal tree species differ in acclimation of net photosynthesis to elevated CO2 and temperature. Tree Physiology 18, 715–726.
| Seedlings of five boreal tree species differ in acclimation of net photosynthesis to elevated CO2 and temperature.Crossref | GoogleScholarGoogle Scholar | 12651406PubMed |
Tjoelker MG, Oleksyn J, Reich PB, Zytkowiak R (2008) Coupling of respiration, nitrogen, and sugars underlies convergent temperature acclimation in Pinus banksiana across wide-ranging sites and populations. Global Change Biology 14, 782–797.
| Coupling of respiration, nitrogen, and sugars underlies convergent temperature acclimation in Pinus banksiana across wide-ranging sites and populations.Crossref | GoogleScholarGoogle Scholar |
Turnbull MH, Tissue DT, Griffin KL, Rogers GND, Whitehead D (1998) Photosynthetic acclimation to long-term exposure to elevated CO2 concentration in Pinus radiata D.Don. is related to age of needles. Plant, Cell & Environment 21, 1019–1028.
| Photosynthetic acclimation to long-term exposure to elevated CO2 concentration in Pinus radiata D.Don. is related to age of needles.Crossref | GoogleScholarGoogle Scholar |
von Felten S, Hattenschwiler S, Saurer M, Siegwolf R (2007) Carbon allocation in shoots of alpine treeline conifers in a CO2 enriched environment. Trees – Structure and Function 21, 283–294.
| Carbon allocation in shoots of alpine treeline conifers in a CO2 enriched environment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXkvVOnur0%3D&md5=7640c1a51adf6ca192e76152fbf8320bCAS |
Wang KY, Kellomäki S, Zha T (2003) Modifications in photosynthetic pigments and chlorophyll fluorescence in 20-year-old pine trees after a four-year exposure to carbon dioxide and temperature elevation. Photosynthetica 41, 167–175.
| Modifications in photosynthetic pigments and chlorophyll fluorescence in 20-year-old pine trees after a four-year exposure to carbon dioxide and temperature elevation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtVSqtrnK&md5=446c5668a45537da6381d29b0d6272c3CAS |
Ward JK, Tissue DT, Thomas RB, Strain BR (1999) Comparative responses of model C3 and C4 plants to drought in low and elevated CO2. Global Change Biology 5, 857–867.
| Comparative responses of model C3 and C4 plants to drought in low and elevated CO2.Crossref | GoogleScholarGoogle 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 Physiology 30, 669–688.
| Differential responses to changes in growth temperature between trees from different functional groups and biomes: a review and synthesis of data.Crossref | GoogleScholarGoogle Scholar | 20368338PubMed |
Way DA, Sage RF (2008) Thermal acclimation of photosynthesis in black spruce (Picea mariana (Mill.) B.S.P.). Plant, Cell & Environment 31, 1250–1262.
| Thermal acclimation of photosynthesis in black spruce (Picea mariana (Mill.) B.S.P.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1SqsbrO&md5=96114d8ac3fbdaba0bf9abd6a3cd3be0CAS |
Wheelwright NT, Logan BA (2004) Previous-year reproduction reduces photosynthetic capacity and slows lifetime growth in females of a neotropical tree. Proceedings of the National Academy of Sciences of the United States of America 101, 8051–8055.
| Previous-year reproduction reduces photosynthetic capacity and slows lifetime growth in females of a neotropical tree.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXkslCisbY%3D&md5=9467e275577f3076f46eba777f645963CAS | 15148383PubMed |
Wong SC, Cowan IR, Farquhar GD (1978) Leaf conductance in relation to assimilation in Eucalyptus pauciflora Sieb. Ex Spenge. Influence of irradiance and partial pressure of carbon dioxide. Plant Physiology 62, 670–674.
| Leaf conductance in relation to assimilation in Eucalyptus pauciflora Sieb. Ex Spenge. Influence of irradiance and partial pressure of carbon dioxide.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXhvFaltA%3D%3D&md5=0c30870aeb27bf23cf2d7c60ca84fbc6CAS | 16660580PubMed |
Wong SC, Kriedemann PE, Farquhar GD (1992) CO2 x nitrogen interaction on seedling growth of four species of Eucalypt. Australian Journal of Botany 40, 457–472.
| CO2 x nitrogen interaction on seedling growth of four species of Eucalypt.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXht1elt7o%3D&md5=338778e4c2d862229fdb69d9a13ff538CAS |
Zieger E (1983) The biology of stomatal guard cells. Annual Review of Plant Physiology 34, 441–474.
| The biology of stomatal guard cells.Crossref | GoogleScholarGoogle Scholar |
Zimmer HC, Auld TD, Benson J, Baker PJ (2014) Recruitment bottlenecks in the rare Australian conifer Wollemia nobilis. Biodiversity and Conservation 23, 203–215.
| Recruitment bottlenecks in the rare Australian conifer Wollemia nobilis.Crossref | GoogleScholarGoogle Scholar |
Zonneveld BJM (2012) Genome sizes of all 19 Araucaria species are correlated with their geographical distribution. Plant Systematics and Evolution 298, 1249–1255.
| Genome sizes of all 19 Araucaria species are correlated with their geographical distribution.Crossref | GoogleScholarGoogle Scholar |