Impaired photosynthesis and increased leaf construction costs may induce floral stress during episodes of global warming over macroevolutionary timescales

Haworth, Matthew; Belcher, Claire M.; Killi, Dilek; Dewhirst, Rebecca A.; Materassi, Alessandro; Raschi, Antonio; Centritto, Mauro

doi:10.1038/s41598-018-24459-z

Title: Impaired photosynthesis and increased leaf construction costs may induce floral stress during episodes of global warming over macroevolutionary timescales

Journal Article · Thu May 31 00:00:00 EDT 2018 · Scientific Reports

DOI:https://doi.org/10.1038/s41598-018-24459-z· OSTI ID:1559790

^[1]; Belcher, Claire M. ^[2]; Killi, Dilek ^[3]; Dewhirst, Rebecca A. ^[2]; Materassi, Alessandro ^[4]; Raschi, Antonio ^[4]; Centritto, Mauro ^[1]

Italian National Research Council, Bologna (Italy). Tree and Timber Inst. (CNR-IVALSA)
Univ. of Exeter, Devon (England). wildFIRE Lab
Univ. of Florence (Italy). Dept. of Agrifood Production and Environmental Sciences (DiSPAA)
Italian National Research Council, Bologna (Italy). Inst. of Biometeorology (CNR-IBIMET)

Global warming events have coincided with turnover of plant species at intervals in Earth history. As mean global temperatures rise, the number, frequency and duration of heat-waves will increase. Ginkgo biloba was grown under controlled climatic conditions at two different day/night temperature regimes (25/20 °C and 35/30 °C) to investigate the impact of heat stress. Photosynthetic CO₂-uptake and electron transport were reduced at the higher temperature, while rates of respiration were greater; suggesting that the carbon balance of the leaves was adversely affected. Stomatal conductance and the potential for evaporative cooling of the leaves was reduced at the higher temperature. Furthermore, the capacity of the leaves to dissipate excess energy was also reduced at 35/30 °C, indicating that photo-protective mechanisms were no longer functioning effectively. Leaf economics were adversely affected by heat stress, exhibiting an increase in leaf mass per area and leaf construction costs. This may be consistent with the selective pressures experienced by fossil Ginkgoales during intervals of global warming such as the Triassic - Jurassic boundary or Early Eocene Climatic Optimum. The physiological and morphological responses of the $$G$$. biloba leaves were closely interrelated; these relationships may be used to infer the leaf economics and photosynthetic/stress physiology of fossil plants.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1559790

Journal Information:: Scientific Reports, Vol. 8, Issue 1; ISSN 2045-2322

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 12 works

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References (70)

Paleobotanical Evidence for Near Present-Day Levels of Atmospheric CO2 During Part of the Tertiary Royer, D. L. Science, Vol. 292, Issue 5525 https://doi.org/10.1126/science.292.5525.2310	journal	June 2001
Energetic Costs of Tissue Construction in Yellow-poplar and White Oak Trees Exposed to Long-term CO2Enrichment Wullschleger, S. Annals of Botany, Vol. 80, Issue 3 https://doi.org/10.1006/anbo.1997.0434	journal	September 1997
Fossil Plants and Global Warming at the Triassic-Jurassic Boundary McElwain, J. C. Science, Vol. 285, Issue 5432 https://doi.org/10.1126/science.285.5432.1386	journal	August 1999
High resolution estimates of paleo-CO2 levels through the Campanian (Late Cretaceous) based on Ginkgo cuticles Quan, Cheng; Sun, Chunlin; Sun, Yuewu Cretaceous Research, Vol. 30, Issue 2 https://doi.org/10.1016/j.cretres.2008.08.004	journal	April 2009
Interaction of drought and high temperature on photosynthesis and grain-filling of wheat Shah, N. H.; Paulsen, G. M. Plant and Soil, Vol. 257, Issue 1 https://doi.org/10.1023/A:1026237816578	journal	November 2003
Brassinolide Application Improves the Drought Tolerance in Maize Through Modulation of Enzymatic Antioxidants and Leaf Gas Exchange: Brassinolide Improves Drought Tolerance in Maize Anjum, S. A.; Wang, L. C.; Farooq, M. Journal of Agronomy and Crop Science, Vol. 197, Issue 3 https://doi.org/10.1111/j.1439-037X.2010.00459.x	journal	January 2011
Different sensitivity of isoprene emission, respiration and photosynthesis to high growth temperature coupled with drought stress in black poplar (Populus nigra) saplings Centritto, M.; Brilli, F.; Fodale, R. Tree Physiology, Vol. 31, Issue 3 https://doi.org/10.1093/treephys/tpq112	journal	March 2011
Evidence for rapid climate change in the Mesozoic–Palaeogene greenhouse world Jenkyns, Hugh C. Philosophical Transactions of the Royal Society of London. Series A: Mathematical, Physical and Engineering Sciences, Vol. 361, Issue 1810 https://doi.org/10.1098/rsta.2003.1240	journal	July 2003
Acclimation to long-term water deficit in the leaves of two sunflower hybrids: photosynthesis, electron transport and carbon metabolism Pankovic, D.; Sakac, Z.; Kevresan, S. Journal of Experimental Botany, Vol. 50, Issue 330 https://doi.org/10.1093/jxb/50.330.128	journal	January 1999
Relationship between specific leaf area, leaf thickness, leaf water content and SPAD-502 readings in six Amazonian tree species Marenco, R. A.; Antezana-Vera, S. A.; Nascimento, H. C. S. Photosynthetica, Vol. 47, Issue 2 https://doi.org/10.1007/s11099-009-0031-6	journal	June 2009
Leaf dynamics of a deciduous forest canopy: no response to elevated CO 2 Norby, Richard J.; Sholtis, Johnna D.; Gunderson, Carla A. Oecologia, Vol. 136, Issue 4 https://doi.org/10.1007/s00442-003-1296-2	journal	August 2003
Vegetation history, diversity patterns, and climate change across the Triassic/Jurassic boundary Bonis, Nina R.; Kürschner, Wolfram M. Paleobiology, Vol. 38, Issue 2 https://doi.org/10.1666/09071.1	journal	January 2012
An assessment of the use of epidermal micro-morphological features to estimate leaf economics of Late Triassic–Early Jurassic fossil Ginkgoales Haworth, Matthew; Raschi, Antonio Review of Palaeobotany and Palynology, Vol. 205 https://doi.org/10.1016/j.revpalbo.2014.02.007	journal	June 2014
Trends, Rhythms, and Aberrations in Global Climate 65 Ma to Present Zachos, J. Science, Vol. 292, Issue 5517 https://doi.org/10.1126/science.1059412	journal	April 2001
Palaeo leaf economics reveal a shift in ecosystem function associated with the end-Triassic mass extinction event Soh, W. K.; Wright, I. J.; Bacon, K. L. Nature Plants, Vol. 3, Issue 8 https://doi.org/10.1038/nplants.2017.104	journal	July 2017
The palaeoclimatology, palaeoecology and palaeoenvironmental analysis of mass extinction events Twitchett, Richard J. Palaeogeography, Palaeoclimatology, Palaeoecology, Vol. 232, Issue 2-4 https://doi.org/10.1016/j.palaeo.2005.05.019	journal	March 2006
Increased Atmospheric SO2 Detected from Changes in Leaf Physiognomy across the Triassic–Jurassic Boundary Interval of East Greenland Bacon, Karen L.; Belcher, Claire M.; Haworth, Matthew PLoS ONE, Vol. 8, Issue 4 https://doi.org/10.1371/journal.pone.0060614	journal	April 2013
Transient Floral Change and Rapid Global Warming at the Paleocene-Eocene Boundary Wing, S. L. Science, Vol. 310, Issue 5750 https://doi.org/10.1126/science.1116913	journal	November 2005
Photosynthetic Response and Adaptation to Temperature in Higher Plants Berry, J.; Bjorkman, O. Annual Review of Plant Physiology, Vol. 31, Issue 1 https://doi.org/10.1146/annurev.pp.31.060180.002423	journal	June 1980
Fossil leaf economics quantified: calibration, Eocene case study, and implications Royer, Dana L.; Sack, Lawren; Wilf, Peter Paleobiology, Vol. 33, Issue 4 https://doi.org/10.1666/07001.1	journal	December 2007
Deep-time evidence of a link between elevated CO2 concentrations and perturbations in the hydrological cycle via drop in plant transpiration Steinthorsdottir, Margret; Woodward, F. Ian; Surlyk, Finn Geology, Vol. 40, Issue 9 https://doi.org/10.1130/G33334.1	journal	September 2012
Adaptation to high temperature mitigates the impact of water deficit during combined heat and drought stress in C3 sunflower and C4 maize varieties with contrasting drought tolerance Killi, Dilek; Bussotti, Filippo; Raschi, Antonio Physiologia Plantarum, Vol. 159, Issue 2 https://doi.org/10.1111/ppl.12490	journal	September 2016
Variation in Ginkgo biloba L. leaf characters across a climatic gradient in China Sun, B.; Dilcher, D. L.; Beerling, D. J. Proceedings of the National Academy of Sciences, Vol. 100, Issue 12 https://doi.org/10.1073/pnas.1232419100	journal	May 2003
Differences in the scaling of area and mass of Ginkgo biloba (Ginkgoaceae) leaves and their relevance to the study of specific leaf area Niklas, Karl J.; Christianson, Michael L. American Journal of Botany, Vol. 98, Issue 8 https://doi.org/10.3732/ajb.1100106	journal	August 2011
The Maidenhair Tree (Ginkgo biloba, L.) Seward, A. C.; Gowan, J. Annals of Botany, Vol. os-14, Issue 1 https://doi.org/10.1093/oxfordjournals.aob.a088765	journal	March 1900
Climate warming in the latest Permian and the Permian-Triassic mass extinction Joachimski, M. M.; Lai, X.; Shen, S. Geology, Vol. 40, Issue 3 https://doi.org/10.1130/G32707.1	journal	January 2012
Chlorophyll fluorescence—a practical guide Maxwell, Kate; Johnson, Giles N. Journal of Experimental Botany, Vol. 51, Issue 345 https://doi.org/10.1093/jexbot/51.345.659	journal	April 2000
Effects of moderate heat stress on photosynthesis: importance of thylakoid reactions, rubisco deactivation, reactive oxygen species, and thermotolerance provided by isoprene Sharkey, Thomas D. Plant, Cell and Environment, Vol. 28, Issue 3 https://doi.org/10.1111/j.1365-3040.2005.01324.x	journal	March 2005
An explanation for conflicting records of Triassic-Jurassic plant diversity Mander, L.; Kurschner, W. M.; McElwain, J. C. Proceedings of the National Academy of Sciences, Vol. 107, Issue 35 https://doi.org/10.1073/pnas.1004207107	journal	August 2010
Sensitivity of Photosynthesis in a C4 Plant, Maize, to Heat Stress Crafts-Brandner, Steven J.; Salvucci, Michael E. Plant Physiology, Vol. 129, Issue 4 https://doi.org/10.1104/pp.002170	journal	June 2002
The Acetyl Bromide Method Is Faster, Simpler and Presents Best Recovery of Lignin in Different Herbaceous Tissues than Klason and Thioglycolic Acid Methods Moreira-Vilar, Flavia Carolina; Siqueira-Soares, Rita de Cássia; Finger-Teixeira, Aline PLoS ONE, Vol. 9, Issue 10 https://doi.org/10.1371/journal.pone.0110000	journal	October 2014
Increased fire activity at the Triassic/Jurassic boundary in Greenland due to climate-driven floral change Belcher, Claire M.; Mander, Luke; Rein, Guillermo Nature Geoscience, Vol. 3, Issue 6 https://doi.org/10.1038/ngeo871	journal	May 2010
Plant spore walls as a record of long-term changes in ultraviolet-B radiation Lomax, Barry H.; Fraser, Wesley T.; Sephton, Mark A. Nature Geoscience, Vol. 1, Issue 9 https://doi.org/10.1038/ngeo278	journal	August 2008
Evolution of leaf-form in land plants linked to atmospheric CO2 decline in the Late Palaeozoic era Beerling, D. J.; Osborne, C. P.; Chaloner, W. G. Nature, Vol. 410, Issue 6826 https://doi.org/10.1038/35066546	journal	March 2001
Causes and consequences of variation in leaf mass per area (LMA): a meta‐analysis Poorter, Hendrik; Niinemets, Ülo; Poorter, Lourens New Phytologist, Vol. 182, Issue 3 https://doi.org/10.1111/j.1469-8137.2009.02830.x	journal	April 2009
Accurate Estimation of Stomatal Aperture from Silicone Rubber Impressions Weyers, Jonathan D. B.; Johansen, Liv G. New Phytologist, Vol. 101, Issue 1 https://doi.org/10.1111/j.1469-8137.1985.tb02820.x	journal	September 1985
Genetic variation of Ginkgo biloba L. (Ginkgoaceae) based on cpDNA PCR-RFLPs: inference of glacial refugia Shen, L.; Chen, X-Y; Zhang, X. Heredity, Vol. 94, Issue 4 https://doi.org/10.1038/sj.hdy.6800616	journal	November 2004
The influence of leaf morphology on litter flammability and its utility for interpreting palaeofire Belcher, Claire M. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 371, Issue 1696 https://doi.org/10.1098/rstb.2015.0163	journal	June 2016
Sulphur dioxide fumigation effects on stomatal density and index of non-resistant plants: Implications for the stomatal palaeo-[CO2] proxy method Haworth, Matthew; Elliott-Kingston, Caroline; Gallagher, Angela Review of Palaeobotany and Palynology, Vol. 182 https://doi.org/10.1016/j.revpalbo.2012.06.006	journal	August 2012
Extremely elevated CO2 concentrations at the Triassic/Jurassic boundary Steinthorsdottir, Margret; Jeram, Andrew J.; McElwain, Jennifer C. Palaeogeography, Palaeoclimatology, Palaeoecology, Vol. 308, Issue 3-4 https://doi.org/10.1016/j.palaeo.2011.05.050	journal	August 2011
Is photosynthesis related to concentrations of nitrogen and Rubisco in leaves of Australian native plants? Warren, Charles R.; Adams, Mark A.; Chen, ZuLiang Functional Plant Biology, Vol. 27, Issue 5 https://doi.org/10.1071/PP98162	journal	January 2000
Nitrogen Availability and Vegetative Development Influence the Response of Ribulose 1,5-Bisphosphate Carboxylase/Oxygenase, Phosphoenolpyruvate Carboxylase, and Heat-Shock Protein Content to Heat Stress in Zea mays L. Heckathorn, Scott A.; Poeller, Gretchen J.; Coleman, James S. International Journal of Plant Sciences, Vol. 157, Issue 5 https://doi.org/10.1086/297374	journal	September 1996
The Small, Methionine-Rich Chloroplast Heat-Shock Protein Protects Photosystem II Electron Transport during Heat Stress Heckathorn, Scott A.; Downs, Craig A.; Sharkey, Thomas D. Plant Physiology, Vol. 116, Issue 1 https://doi.org/10.1104/pp.116.1.439	journal	January 1998
Rubisco activase constrains the photosynthetic potential of leaves at high temperature and CO2 Crafts-Brandner, S. J.; Salvucci, M. E. Proceedings of the National Academy of Sciences, Vol. 97, Issue 24 https://doi.org/10.1073/pnas.230451497	journal	November 2000
Investigation of the CO ₂ Dependence of Quantum Yield and Respiration in Eucalyptus pauciflora Kirschbaum, Miko U. F.; Farquhar, Graham D. Plant Physiology, Vol. 83, Issue 4 https://doi.org/10.1104/pp.83.4.1032	journal	April 1987
Use of thermography for quantitative studies of spatial and temporal variation of stomatal conductance over leaf surfaces Jones, H. G. Plant, Cell & Environment, Vol. 22, Issue 9 https://doi.org/10.1046/j.1365-3040.1999.00468.x	journal	September 1999
An atmospheric pCO2 reconstruction across the Cretaceous-Tertiary boundary from leaf megafossils Beerling, D. J.; Lomax, B. H.; Royer, D. L. Proceedings of the National Academy of Sciences, Vol. 99, Issue 12 https://doi.org/10.1073/pnas.122573099	journal	June 2002
Inhibition and Acclimation of Photosynthesis to Heat Stress Is Closely Correlated with Activation of Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase Law, R. David; Crafts-Brandner, Steven J. Plant Physiology, Vol. 120, Issue 1 https://doi.org/10.1104/pp.120.1.173	journal	May 1999
The role of increasing temperature variability in European summer heatwaves Schär, Christoph; Vidale, Pier Luigi; Lüthi, Daniel Nature, Vol. 427, Issue 6972 https://doi.org/10.1038/nature02300	journal	January 2004
Estimating paleoatmospheric pCO2 during the Early Eocene Climatic Optimum from stomatal frequency of Ginkgo, Okanagan Highlands, British Columbia, Canada Smith, Robin Y.; Greenwood, David R.; Basinger, James F. Palaeogeography, Palaeoclimatology, Palaeoecology, Vol. 293, Issue 1-2 https://doi.org/10.1016/j.palaeo.2010.05.006	journal	July 2010
Moderately High Temperatures Inhibit Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase (Rubisco) Activase-Mediated Activation of Rubisco Feller, Urs; Crafts-Brandner, Steven J.; Salvucci, Michael E. Plant Physiology, Vol. 116, Issue 2 https://doi.org/10.1104/pp.116.2.539	journal	February 1998
Rising atmospheric CO2 as a possible trigger for the end-Triassic mass extinction Huynh, Tran T.; Poulsen, Christopher J. Palaeogeography, Palaeoclimatology, Palaeoecology, Vol. 217, Issue 3-4 https://doi.org/10.1016/j.palaeo.2004.12.004	journal	February 2005
Evolutionary Trends in the Genus Ginkgo Tralau, Hans Lethaia, Vol. 1, Issue 1 https://doi.org/10.1111/j.1502-3931.1968.tb01728.x	journal	January 1968
Water-use responses of ‘living fossil’ conifers to CO2 enrichment in a simulated Cretaceous polar environment Llorens, Laura; Osborne, Colin P.; Beerling, David J. Annals of Botany, Vol. 104, Issue 1 https://doi.org/10.1093/aob/mcp108	journal	May 2009
Can atmospheric composition influence plant fossil preservation potential via changes in leaf mass per area? A new hypothesis based on simulated palaeoatmosphere experiments. Bacon, Karen L.; Haworth, Matthew; Conroy, Elizabeth Palaeogeography, Palaeoclimatology, Palaeoecology, Vol. 464 https://doi.org/10.1016/j.palaeo.2015.12.006	journal	December 2016
A rapid method for determining the efficiency of biosynthesis of plant biomass Vertregt, N.; Penning de Vries, F. W. T. Journal of Theoretical Biology, Vol. 128, Issue 1 https://doi.org/10.1016/S0022-5193(87)80034-6	journal	September 1987
Climatic Variation in Forage Grasses. I. Leaf Development in Climatic Races of Lolium and Dactylis Cooper, J. P. The Journal of Applied Ecology, Vol. 1, Issue 1 https://doi.org/10.2307/2401588	journal	May 1964
Comparison of Palaeobotanical Observations with Experimental Data on the Leaf Anatomy of Durmast Oak [Quercus petraea(Fagaceae)] in Response to Environmental Change KÜRschner, W. Annals of Botany, Vol. 81, Issue 5 https://doi.org/10.1006/anbo.1998.0605	journal	May 1998
Correlated terrestrial and marine evidence for global climate changes before mass extinction at the Cretaceous-Paleogene boundary Wilf, P.; Johnson, K. R.; Huber, B. T. Proceedings of the National Academy of Sciences, Vol. 100, Issue 2 https://doi.org/10.1073/pnas.0234701100	journal	January 2003
High Temperature Effects on Electron and Proton Circuits of Photosynthesis Sharkey, Thomas D.; Zhang, Ru Journal of Integrative Plant Biology, Vol. 52, Issue 8 https://doi.org/10.1111/j.1744-7909.2010.00975.x	journal	July 2010
On the reconstruction of plant photosynthetic and stress physiology across the Triassic–Jurassic boundary Haworth, Matthew; Gallagher, Angela; Sum, Elysia TURKISH JOURNAL OF EARTH SCIENCES, Vol. 23 https://doi.org/10.3906/yer-1202-4	journal	January 2014
The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence Genty, Bernard; Briantais, Jean-Marie; Baker, Neil R. Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 990, Issue 1 https://doi.org/10.1016/S0304-4165(89)80016-9	journal	January 1989
GEOCARB III: A revised model of atmospheric CO2 over Phanerozoic time Berner, R. A. American Journal of Science, Vol. 301, Issue 2 https://doi.org/10.2475/ajs.301.2.182	journal	February 2001
Harvesting sunlight safely Demmig-Adams, Barbara; Adams, William W. Nature, Vol. 403, Issue 6768 https://doi.org/10.1038/35000315	journal	January 2000
Antiquity and fundamental processes of the antler cycle in Cervidae (Mammalia) Rössner, Gertrud E.; Costeur, Loïc; Scheyer, Torsten M. The Science of Nature, Vol. 108, Issue 1 https://doi.org/10.1007/s00114-020-01713-x	journal	December 2020
Moderately High Temperatures Inhibit Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase (Rubisco) Activase-Mediated Activation of Rubisco Feller, Urs; Crafts-Brandner, Steven J.; Salvucci, Michael E. American Society of Plant Physiologists https://doi.org/10.7892/boris.83864	text	January 1998
The CO2/O2 specificity of ribulose 1,5-bisphosphate carboxylase/oxygenase: Dependence on ribulosebisphosphate concentration, pH and temperature Jordan, Douglas B.; Ogren, William L. Planta, Vol. 161, Issue 4 https://doi.org/10.1007/bf00398720	journal	June 1984
Large igneous provinces and mass extinctions Wignall, P. B. Earth-Science Reviews, Vol. 53, Issue 1-2 https://doi.org/10.1016/s0012-8252(00)00037-4	journal	March 2001
Estimation of Tissue Construction Cost from Heat of Combustion and Organic Nitrogen Content. Williams, K.; Percival, F.; Merino, J. Plant, Cell and Environment, Vol. 10, Issue 9 https://doi.org/10.1111/1365-3040.ep11604754	journal	December 1987
Leaf Traits are good Predictors of Plant Performance Across 53 rain Forest Species Poorter, Lourens; Bongers, Frans Ecology, Vol. 87, Issue 7 https://doi.org/10.1890/0012-9658(2006)87[1733:ltagpo]2.0.co;2	journal	July 2006

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