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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Diverging temperature responses of CO<sub>2</sub> assimilation and plant development explain the overall effect of temperature on biomass accumulation in wheat leaves and grains</title><author><name sortKey="Lohraseb, Iman" sort="Lohraseb, Iman" uniqKey="Lohraseb I" first="Iman" last="Lohraseb">Iman Lohraseb</name><affiliation><nlm:aff id="plw092-aff1">Australian Centre for Plant Functional Genomics, University of Adelaide, School of Agriculture Food and Wine, Hartley Grove, Urrbrae, South Australia, 5064, Australia</nlm:aff></affiliation></author><author><name sortKey="Collins, Nicholas C" sort="Collins, Nicholas C" uniqKey="Collins N" first="Nicholas C." last="Collins">Nicholas C. Collins</name><affiliation><nlm:aff id="plw092-aff1">Australian Centre for Plant Functional Genomics, University of Adelaide, School of Agriculture Food and Wine, Hartley Grove, Urrbrae, South Australia, 5064, Australia</nlm:aff></affiliation></author><author><name sortKey="Parent, Boris" sort="Parent, Boris" uniqKey="Parent B" first="Boris" last="Parent">Boris Parent</name><affiliation><nlm:aff id="plw092-aff1">Australian Centre for Plant Functional Genomics, University of Adelaide, School of Agriculture Food and Wine, Hartley Grove, Urrbrae, South Australia, 5064, Australia</nlm:aff></affiliation><affiliation><nlm:aff id="plw092-aff2">Present address: INRA, UMR759 Laboratoire d’Ecophysiologie des Plantes sous Stress Environnementaux. Place Viala, F-34060 Montpellier, France</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">28069595</idno><idno type="pmc">5391697</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5391697</idno><idno type="RBID">PMC:5391697</idno><idno type="doi">10.1093/aobpla/plw092</idno><date when="2017">2017</date><idno type="wicri:Area/Pmc/Corpus">002265</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">002265</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Diverging temperature responses of CO<sub>2</sub> assimilation and plant development explain the overall effect of temperature on biomass accumulation in wheat leaves and grains</title><author><name sortKey="Lohraseb, Iman" sort="Lohraseb, Iman" uniqKey="Lohraseb I" first="Iman" last="Lohraseb">Iman Lohraseb</name><affiliation><nlm:aff id="plw092-aff1">Australian Centre for Plant Functional Genomics, University of Adelaide, School of Agriculture Food and Wine, Hartley Grove, Urrbrae, South Australia, 5064, Australia</nlm:aff></affiliation></author><author><name sortKey="Collins, Nicholas C" sort="Collins, Nicholas C" uniqKey="Collins N" first="Nicholas C." last="Collins">Nicholas C. Collins</name><affiliation><nlm:aff id="plw092-aff1">Australian Centre for Plant Functional Genomics, University of Adelaide, School of Agriculture Food and Wine, Hartley Grove, Urrbrae, South Australia, 5064, Australia</nlm:aff></affiliation></author><author><name sortKey="Parent, Boris" sort="Parent, Boris" uniqKey="Parent B" first="Boris" last="Parent">Boris Parent</name><affiliation><nlm:aff id="plw092-aff1">Australian Centre for Plant Functional Genomics, University of Adelaide, School of Agriculture Food and Wine, Hartley Grove, Urrbrae, South Australia, 5064, Australia</nlm:aff></affiliation><affiliation><nlm:aff id="plw092-aff2">Present address: INRA, UMR759 Laboratoire d’Ecophysiologie des Plantes sous Stress Environnementaux. Place Viala, F-34060 Montpellier, France</nlm:aff></affiliation></author></analytic><series><title level="j">AoB Plants</title><idno type="eISSN">2041-2851</idno><imprint><date when="2017">2017</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Under rising temperature, the rate of any developmental process increased with temperature more rapidly than that of CO<sub>2</sub> assimilation. We found that this discrepancy, summarised by the CO<sub>2</sub> assimilation rate per unit of plant development, could explain the observed reductions in biomass accumulation in leaves and grain under high temperatures. This simple model describes the effects of night and day temperature equally well, and offers a simple framework for describing the effects of temperature on plant growth, without any supplementary effect of rising night temperatures.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Alkhatib, K" uniqKey="Alkhatib K">K Alkhatib</name></author><author><name sortKey="Paulsen, Gm" uniqKey="Paulsen G">GM. Paulsen</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Atkin, Ok" uniqKey="Atkin O">OK Atkin</name></author><author><name sortKey="Scheurwater, I" uniqKey="Scheurwater I">I Scheurwater</name></author><author><name sortKey="Pons, Tl" uniqKey="Pons T">TL. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">AoB Plants</journal-id><journal-id journal-id-type="iso-abbrev">AoB Plants</journal-id><journal-id journal-id-type="publisher-id">aobpla</journal-id><journal-title-group><journal-title>AoB Plants</journal-title></journal-title-group><issn pub-type="epub">2041-2851</issn><publisher><publisher-name>Oxford University Press</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">28069595</article-id><article-id pub-id-type="pmc">5391697</article-id><article-id pub-id-type="doi">10.1093/aobpla/plw092</article-id><article-id pub-id-type="publisher-id">plw092</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group></article-categories><title-group><article-title>Diverging temperature responses of CO<sub>2</sub> assimilation and plant development explain the overall effect of temperature on biomass accumulation in wheat leaves and grains</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Lohraseb</surname><given-names>Iman</given-names></name><xref ref-type="aff" rid="plw092-aff1">1</xref></contrib><contrib contrib-type="author"><name><surname>Collins</surname><given-names>Nicholas C.</given-names></name><xref ref-type="aff" rid="plw092-aff1">1</xref></contrib><contrib contrib-type="author" corresp="yes"><name><surname>Parent</surname><given-names>Boris</given-names></name><xref ref-type="aff" rid="plw092-aff1">1</xref><xref ref-type="aff" rid="plw092-aff2">2</xref><xref ref-type="corresp" rid="plw092-cor1"></xref><pmc-comment>boris.parent@supagro.inra.fr </pmc-comment>
</contrib></contrib-group><aff id="plw092-aff1"><label>1</label>Australian Centre for Plant Functional Genomics, University of Adelaide, School of Agriculture Food and Wine, Hartley Grove, Urrbrae, South Australia, 5064, Australia</aff><aff id="plw092-aff2"><label>2</label>Present address: INRA, UMR759 Laboratoire d’Ecophysiologie des Plantes sous Stress Environnementaux. Place Viala, F-34060 Montpellier, France</aff><author-notes><fn id="plw092-FM2"><p><bold>Associate Editor:</bold> Rafael Oliveira</p></fn><fn id="plw092-FM1"><p><bold>Citation:</bold> Lohraseb I, Collins NC, Parent B. 2017. Diverging temperature responses of CO<sub>2</sub> assimilation and plant development explain the overall effect of temperature on biomass accumulation in wheat leaves and grains. <italic>AoB PLANTS</italic><bold>9</bold>: plw092; doi:10.1093/aobpla/plw092</p></fn><corresp id="plw092-cor1"><label>*</label>Corresponding author’s e-mail address: <email>boris.parent@supagro.inra.fr</email></corresp></author-notes><pub-date pub-type="collection"><month>1</month><year>2017</year></pub-date><pub-date pub-type="epub" iso-8601-date="2017-01-09"><day>09</day><month>1</month><year>2017</year></pub-date><pub-date pub-type="pmc-release"><day>09</day><month>1</month><year>2017</year></pub-date><pmc-comment> PMC Release delay is 0 months and 0 days and was based on the
<volume>9</volume><issue>1</issue><elocation-id>plw092</elocation-id><history><date date-type="received"><day>7</day><month>7</month><year>2016</year></date><date date-type="accepted"><day>4</day><month>1</month><year>2017</year></date></history><permissions><copyright-statement>© The Authors 2017. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For Permissions, please email: journals.permissions@oup.com</copyright-statement><copyright-year>2017</copyright-year><license xlink:href="http://creativecommons.org/licenses/by/4.0/" license-type="cc-by"><license-p>This is an Open Access article distributed under the terms of the Creative Commons Attribution License (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link>), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.</license-p></license></permissions><self-uri xlink:href="plw092.pdf"></self-uri><abstract abstract-type="teaser"><p>Under rising temperature, the rate of any developmental process increased with temperature more rapidly than that of CO<sub>2</sub> assimilation. We found that this discrepancy, summarised by the CO<sub>2</sub> assimilation rate per unit of plant development, could explain the observed reductions in biomass accumulation in leaves and grain under high temperatures. This simple model describes the effects of night and day temperature equally well, and offers a simple framework for describing the effects of temperature on plant growth, without any supplementary effect of rising night temperatures.</p></abstract><abstract><title>Abstract</title><p>There is a growing consensus in the literature that rising temperatures influence the rates of biomass accumulation by shortening the development of plant organs and the whole plant and by altering the rates of respiration and photosynthesis. A model describing the net effects of these processes on biomass would be useful, but would need to reconcile reported differences in the effects of night and day temperature on plant productivity. In this study, the working hypothesis was that the temperature responses of CO<sub>2</sub> assimilation and plant development rates were divergent, and that their net effects could explain observed differences in biomass accumulation. In wheat (<italic>Triticum aestivum</italic>) plants, we followed the temperature responses of photosynthesis, respiration and leaf elongation, and confirmed that their responses diverged. We measured the amount of carbon assimilated per ‘unit of plant development’ in each scenario and compared it to the biomass that accumulated in growing leaves and grains. Our results suggested that, up to a temperature optimum, the rate of any developmental process increased with temperature more rapidly than that of CO<sub>2</sub> assimilation and that this discrepancy, summarised by the CO<sub>2</sub> assimilation rate per unit of plant development, could explain the observed reductions in biomass accumulation in plant organs under high temperatures. The model described the effects of night and day temperature equally well, and offers a simple framework for describing the effects of temperature on plant growth.</p></abstract><kwd-group kwd-group-type="author"><kwd>Biomass</kwd><kwd>development</kwd><kwd>grain growth</kwd><kwd>photosynthesis</kwd><kwd>respiration</kwd><kwd>specific leaf area</kwd><kwd>temperature</kwd><kwd>thermal time</kwd><kwd>wheat</kwd></kwd-group><counts><page-count count="13"></page-count></counts></article-meta></front><body><sec><title>Introduction</title><p>High temperatures decrease biomass accumulation in plant leaves (<xref rid="plw092-B45" ref-type="bibr">Vile <italic>et al.</italic> 2012</xref>), cereal grains (<xref rid="plw092-B53" ref-type="bibr">Wheeler <italic>et al.</italic> 1996</xref>) and whole plants, with implications for agricultural productivity and ecology under a climate change scenario (<xref rid="plw092-B29" ref-type="bibr">Peng <italic>et al.</italic> 2004</xref>). An emerging consensus is that carbon balance is a critical factor in responses of biomass accumulation processes to temperature changes. This view comes from studying temperature responses of grain dry mass (<xref rid="plw092-B50" ref-type="bibr">Wardlaw 1994</xref>; <xref rid="plw092-B53" ref-type="bibr">Wheeler <italic>et al.</italic> 1996</xref>), and leaf dry mass per area (LMA) or its reciprocal, the specific leaf area (<xref rid="plw092-B32" ref-type="bibr">Poorter <italic>et al.</italic> 2009</xref>). Most of these studies investigated the effect of very high temperatures within the ‘stressing range’ where photosynthesis was demonstrated to be negatively affected (<xref rid="plw092-B21" ref-type="bibr">Loveys <italic>et al.</italic> 2002</xref>; <xref rid="plw092-B44" ref-type="bibr">Vasseur <italic>et al.</italic> 2011</xref>). Accordingly, high CO<sub>2</sub> or light, which increases photosynthesis, can partially offset the impact of high temperature on biomass accumulation in vegetative tissues (<xref rid="plw092-B43" ref-type="bibr">Taub <italic>et al.</italic> 2000</xref>; <xref rid="plw092-B44" ref-type="bibr">Vasseur <italic>et al.</italic> 2011</xref>) and in grains (<xref rid="plw092-B50" ref-type="bibr">Wardlaw 1994</xref>; <xref rid="plw092-B53" ref-type="bibr">Wheeler <italic>et al.</italic> 1996</xref>).</p><p>By contrast, rising temperatures in the ‘non-stressing’ temperature range increase the rate of photosynthesis (<xref rid="plw092-B4" ref-type="bibr">Atkin and Tjoelker 2003</xref>; <xref rid="plw092-B39" ref-type="bibr">Sage and Kubien 2007</xref>). One consequence is accelerated dry weight accumulation in the grain (<xref rid="plw092-B53" ref-type="bibr">Wheeler <italic>et al.</italic> 1996</xref>), which reflects faster accumulation of photosynthate. High temperatures also accelerate cell expansion and division, and hasten genetic programs of organ differentiation, consequently shortening the period over which biomass can accumulate (<xref rid="plw092-B28" ref-type="bibr">Parent <italic>et al.</italic> 2010a</xref>). These effects are largely independent of variations in carbon fixation (<xref rid="plw092-B23" ref-type="bibr">Morita <italic>et al.</italic> 2005</xref>). Temperature during grain filling impacts final single grain weight with effects on both the rate and duration of grain filling (<xref rid="plw092-B40" ref-type="bibr">Sofield <italic>et al.</italic> 1977</xref>; <xref rid="plw092-B54" ref-type="bibr">Yin <italic>et al.</italic> 2009</xref>). Similarly, temperature influences LMA by impacting photosynthesis and the rates of leaf expansion (<xref rid="plw092-B41" ref-type="bibr">Tardieu <italic>et al.</italic> 1999</xref>).</p><p>Predicting temperature effects on biomass accumulation requires an understanding of the dynamics of carbon assimilation and plant development responses. The temperature response of respiration and photosynthesis are now well-described under the ‘non-stressing’ temperature range (<xref rid="plw092-B4" ref-type="bibr">Atkin and Tjoelker 2003</xref>; <xref rid="plw092-B39" ref-type="bibr">Sage and Kubien 2007</xref>). These responses are divergent (<xref rid="plw092-B3" ref-type="bibr">Atkin <italic>et al.</italic> 2007</xref>), and both change after exposure to a period of high temperature, <italic>i.e.</italic> they show acclimation behaviour (<xref rid="plw092-B2" ref-type="bibr">Atkin <italic>et al.</italic> 2006</xref>; <xref rid="plw092-B10" ref-type="bibr">Campbell <italic>et al.</italic> 2007</xref>). <xref rid="plw092-B26" ref-type="bibr">Parent and Tardieu (2012)</xref> demonstrated that multiple developmental processes followed a common temperature response curve within a given species. Indeed, rates of processes as diverse as leaf expansion, progression towards flowering or other developmental milestones (<italic>e.g.</italic> percentage of final grain fill duration per day = grain development rate), shared similar temperature responses and are hereafter referred to as ‘development rates’. The temperature responses of these developmental processes followed different patterns to photosynthesis, and other enzymatic reactions involved in primary metabolism (<xref rid="plw092-B25" ref-type="bibr">Parent <italic>et al.</italic> 2010a</xref>).</p><p>However, in crop temperature response models, different formalisms are currently used to describe development and leaf expansion (<xref rid="plw092-B27" ref-type="bibr">Parent and Tardieu 2014</xref>; <xref rid="plw092-B19" ref-type="bibr">Kumudini <italic>et al.</italic> 2014</xref>). Predicted responses of development to temperature depend on the chosen equation and its parameterisation, and few models consider equations that accommodate different day and night temperature (example: Crop Heat Unit, reviewed by <xref rid="plw092-B19" ref-type="bibr">Kumudini <italic>et al.</italic> 2014</xref>), or different plant stages. There are currently efforts from the community of crop modellers to make these equations converge (<xref rid="plw092-B22" ref-type="bibr">Makowski <italic>et al.</italic> 2015</xref>) with suites of tools such as APSIM (<xref rid="plw092-B37" ref-type="bibr">Rosenzweig <italic>et al.</italic> 2013</xref>). The same applies to the response of photosynthesis or radiation use efficiency, with several equations used in the various models (reviewed in <xref rid="plw092-B27" ref-type="bibr">Parent and Tardieu 2014</xref>). While many crop models consider specific leaf area to be a result of leaf expansion and biomass, many others consider SLA as a genetic parameter with leaf expansion being driven by leaf biomass (reviewed in <xref rid="plw092-B27" ref-type="bibr">Parent and Tardieu 2014</xref>). In addition, there is still debate about specific night temperature effects on biomass or production (<xref rid="plw092-B30" ref-type="bibr">Peraudeau <italic>et al.</italic> 2015</xref>; <xref rid="plw092-B13" ref-type="bibr">Fang <italic>et al.</italic> 2015</xref>; <xref rid="plw092-B15" ref-type="bibr">Glaubitz <italic>et al.</italic> 2014</xref>; <xref rid="plw092-B17" ref-type="bibr">Kanno and Makino 2010</xref>; <xref rid="plw092-B29" ref-type="bibr">Peng <italic>et al.</italic> 2004</xref>).</p><p>Due to the different and non-linear temperature response curves of development rate, photosynthesis, and respiration, the relative impacts of these component traits on biomass accumulation (and their temperature dynamics) would depend on the particular growth temperature range. Here, we address these divergences by using rates of respiration, photosynthesis and various developmental processes observed across a range of thermal scenarios in wheat to model the temperature responses of these traits. We then express the net photoassimilate accumulation per ‘unit of leaf development’ or ‘unit of grain development’ or ‘unit of whole plant development’ at a given temperature in terms of the equivalent value at 20 °C. As such, this approach provides a framework for describing the relative contributions of photosynthesis and respiration to biomass accumulation across a temperature range, with reference to a standard unit.</p></sec><sec sec-type="methods"><title>Methods</title><sec><title>Plant growth conditions</title><p>All experiments were carried out with the bread wheat (<italic>Triticum aestivum</italic>) cultivar Apogee. Seeds were sown in plastic pots (8 × 8 × 20 cm) filled with a coir-peat-based potting mix. Plants were grown in several identical growth chambers (GC-20 Bigfoot series, BioChambers, Winnipeg, Canada). The light was supplied by fluorescent bulbs (Photosynthetically Active Radiation, PAR = 380 µmol m<sup>−</sup><sup>2</sup> s<sup>−</sup><sup>1</sup>) for 12 h of photoperiod (PP) with an overall daily PAR (3.6 ± 0.1 MJ m<sup>−</sup><sup>2</sup> d<sup>−</sup><sup>1</sup>) similar to that observed in the field at vegetative stage (<xref rid="plw092-B11" ref-type="bibr">O'Connell <italic>et al.</italic> 2004</xref>). CO<sub>2</sub> naturally varied during the day but daily average CO<sub>2</sub> concentration was similar in all treatments. In each of the three experiments, plants were initially grown under temperatures of 25 °C day (T°<sub>day</sub>) and 20 °C night (T°<sub>night</sub>) and the soil was watered close to the saturation level.</p><p>In Experiment 1, plants were transferred to different constant temperatures (11, 17, 20, 23 and 29 °C) at the appearance of leaf 6. Leaf temperature, measured with an infrared thermometer (Raynger MX4, Raytek Corporation, Santa Cruz, CA, USA), was close (ΔT° < 1 °C) to the air temperature, during both nights and days. Because air relative humidity was stable in all treatments (60 ± 5 %), vapour pressure deficit varied from 0.5 kPa at 11 °C to 1.8 kPa at 29 °C.</p><p>In Experiment 2, plants at the appearance of leaf 4 were transferred to several thermal regimes (T°<sub>day</sub>/T°<sub>night</sub>: 20/15, 20/20, 25/15 and 25/20 °C) where they remained until anthesis (appearance of first anthers on the main spike).</p><p>In Experiment 3, plants at anthesis were transferred to several thermal regimes (T°<sub>day</sub>/T°<sub>night</sub>: 20/15, 20/20, 25/15 and 25/20 °C) where they remained until maturity. At heading (head of the main tiller fully emerged), plants were pruned leaving the main tiller with its three youngest leaves. New tillers were then removed weekly.</p></sec><sec><title>Leaf measurements</title><p>In Experiments 1 and 2, leaf elongation rate (LER) was measured on leaf 6, by measuring leaf length with a ruler, at leaf appearance and again after a further 24 h. In parallel, it was determined that this developmental stage corresponded to the linear phase of elongation under all tested thermal scenarios (data not shown).</p><p>In Experiments 1 and 2, photosynthesis rate during the day and respiration rate during the night were analysed on fully-developed leaf 4 when leaf 6 was elongating, using a gas exchange system (LI-6400, Li-Cor, Lincoln, NE). Photosynthesis was measured at least 2 h after the lights were switched on and 2 h before the lights were switched off. Artificial illumination was supplied from a red-blue LED light source with PAR = 380 µmol m<sup>−</sup><sup>2</sup> s<sup>−</sup><sup>1</sup>, similar to the growth chambers, or under saturating light (PAR = 2000 µmol m<sup>−</sup><sup>2</sup> s<sup>−</sup><sup>1</sup>). Respiration rate during the night was measured at predawn, during the last 3 h of the night cycle. CO<sub>2</sub> was maintained at 400 ppm (Reference) using the CO<sub>2</sub> mixer (flow rate = 500 µmol s<sup>−</sup><sup>1</sup>).</p><p>The daily net photosynthesis rate during the day (P<sub>N</sub>, mol m<sup>−</sup><sup>2</sup> d<sup>−</sup><sup>1</sup>) and daily respiration rate during the night (R, mol m<sup>−</sup><sup>2</sup> d<sup>−</sup><sup>1</sup>) were calculated by integrating the measured instantaneous rates of photosynthesis and respiration during the night during the respective times of light and dark (12 h) to arrive at a daily integral. The overall net CO<sub>2</sub> assimilation rate per day (A<sub>N</sub>, mol m<sup>−</sup><sup>2</sup> d<sup>−</sup><sup>1</sup>) was calculated:
<disp-formula id="E1"><label>(Eq.1)</label><mml:math id="MM1"><mml:msub><mml:mrow><mml:mi>A</mml:mi></mml:mrow><mml:mrow><mml:mi>N</mml:mi></mml:mrow></mml:msub><mml:mo>=</mml:mo><mml:msub><mml:mrow><mml:mi>P</mml:mi></mml:mrow><mml:mrow><mml:mi>N</mml:mi></mml:mrow></mml:msub><mml:mo>-</mml:mo><mml:mi>R</mml:mi></mml:math></disp-formula></p><p>Unless indicated otherwise, values of A<sub>N</sub> and P<sub>N</sub> used were those measured at PAR = 380 µmol m<sup>−</sup><sup>2</sup> s<sup>−</sup><sup>1</sup>.</p><p>In Experiment 2, leaves 4, 5, 6 and 7 were collected at anthesis. Leaf length was measured with a ruler, leaf area was measured with a planimeter (PATON electronic belt driven planimeter, CSIRO, Canberra, Australia) and leaf dry weight was determined after 2 days at 85 °C.</p></sec><sec><title>Data analysis</title><p>The R language (<xref rid="plw092-B34" ref-type="bibr">R Development Core Team 2005</xref>) was used for all statistical analyses and model regressions, namely a comparison of means (function <italic>pairwise.t.test</italic> with ‘BH’ method), Pearson correlation tests (function <italic>cor.test</italic>), linear regression (function <italic>lm)</italic>, non-linear regression (function <italic>nls</italic>) and analysis of variance (function <italic>anova</italic>). Data and scripts are available on demand.</p></sec><sec><title>Temperature responses</title><p>Temperature responses were described by the equation of <xref rid="plw092-B16" ref-type="bibr">Johnson <italic>et al.</italic> (1942)</xref>, modified by <xref rid="plw092-B26" ref-type="bibr">Parent and Tardieu (2012)</xref>:
<disp-formula id="E2"><label>(Eq.2)</label><mml:math id="MM2"><mml:mrow><mml:mi>F</mml:mi><mml:mo stretchy="false">(</mml:mo><mml:mi>T</mml:mi><mml:mo stretchy="false">)</mml:mo><mml:mo>=</mml:mo><mml:mfrac><mml:mrow><mml:mi mathvariant="normal">A</mml:mi><mml:mi>T</mml:mi><mml:msup><mml:mi>e</mml:mi><mml:mrow><mml:mrow><mml:mo stretchy="true">(</mml:mo><mml:mrow><mml:mfrac><mml:mrow><mml:mo>−</mml:mo><mml:mi>Δ</mml:mi><mml:msubsup><mml:mi mathvariant="normal">H</mml:mi><mml:mi mathvariant="normal">A</mml:mi><mml:mtext>‡</mml:mtext></mml:msubsup></mml:mrow><mml:mrow><mml:mi mathvariant="normal">R</mml:mi><mml:mi>T</mml:mi></mml:mrow></mml:mfrac></mml:mrow><mml:mo stretchy="true">)</mml:mo></mml:mrow></mml:mrow></mml:msup></mml:mrow><mml:mrow><mml:mn>1</mml:mn><mml:mo>+</mml:mo><mml:msup><mml:mrow><mml:mrow><mml:mo stretchy="true">[</mml:mo><mml:mrow><mml:msup><mml:mi>e</mml:mi><mml:mrow><mml:mrow><mml:mo stretchy="true">(</mml:mo><mml:mrow><mml:mfrac><mml:mrow><mml:mo>−</mml:mo><mml:mi>Δ</mml:mi><mml:msubsup><mml:mi mathvariant="normal">H</mml:mi><mml:mi mathvariant="normal">A</mml:mi><mml:mtext>‡</mml:mtext></mml:msubsup></mml:mrow><mml:mrow><mml:mi mathvariant="normal">R</mml:mi><mml:mi>T</mml:mi></mml:mrow></mml:mfrac></mml:mrow><mml:mo stretchy="true">)</mml:mo></mml:mrow></mml:mrow></mml:msup></mml:mrow><mml:mo stretchy="true">]</mml:mo></mml:mrow></mml:mrow><mml:mrow><mml:mi>α</mml:mi><mml:mrow><mml:mo stretchy="true">(</mml:mo><mml:mrow><mml:mn>1</mml:mn><mml:mo>−</mml:mo><mml:mfrac><mml:mi>T</mml:mi><mml:mrow><mml:msub><mml:mi mathvariant="normal">T</mml:mi><mml:mn>0</mml:mn></mml:msub></mml:mrow></mml:mfrac></mml:mrow><mml:mo stretchy="true">)</mml:mo></mml:mrow></mml:mrow></mml:msup></mml:mrow></mml:mfrac></mml:mrow></mml:math></disp-formula>where <italic>F(T)</italic> is the considered rate, <italic>T</italic> is the temperature (Kelvin, K), <italic>Δ</italic><inline-formula id="IE1"><mml:math id="MM100"><mml:msubsup><mml:mrow><mml:mi mathvariant="normal">H</mml:mi></mml:mrow><mml:mrow><mml:mi mathvariant="normal">A</mml:mi></mml:mrow><mml:mrow><mml:mtext>‡</mml:mtext></mml:mrow></mml:msubsup></mml:math></inline-formula> (J mol<sup>−</sup><sup>1</sup>) is the enthalpy of activation of the process and determines the curvature at low temperature, <italic>α</italic> (dimensionless) determines how sharp is the decrease in rate at high temperature and is fixed at 3.5 for development processes (<xref rid="plw092-B26" ref-type="bibr">Parent and Tardieu 2012</xref>), T<sub>0</sub> (K) determines the temperature at which the rate is maximum, and A is the trait scaling coefficient. Temperature responses of LER, P<sub>N</sub>, and R were calculated by non-linear regressions on the values measured in Experiment 1. The response of A<sub>N</sub> to temperature was then calculated from the temperature responses of R and P<sub>N</sub>, using <xref ref-type="disp-formula" rid="E1">Eq.1</xref>.</p></sec><sec><title>Thermal compensation of time and rates</title><p>For any measured rate <italic>J</italic>(<italic>T</italic>) at temperature <italic>T</italic>, a temperature compensated rate was calculated as the equivalent rate at 20 °C.
<disp-formula id="E3"><label>(Eq.3)</label><mml:math id="MM3"><mml:msub><mml:mrow><mml:mi>J</mml:mi></mml:mrow><mml:mrow><mml:mn>20</mml:mn><mml:mo>°</mml:mo><mml:mi mathvariant="normal">C</mml:mi></mml:mrow></mml:msub><mml:mo>=</mml:mo><mml:mi>J</mml:mi><mml:mo>(</mml:mo><mml:mi>T</mml:mi><mml:mo stretchy="true">)</mml:mo><mml:mfrac><mml:mrow><mml:mi>F</mml:mi><mml:mfenced separators="|"><mml:mrow><mml:mn>20</mml:mn><mml:mo>°</mml:mo><mml:mi mathvariant="normal">C</mml:mi></mml:mrow></mml:mfenced></mml:mrow><mml:mrow><mml:mi>F</mml:mi><mml:mo>(</mml:mo><mml:mi>T</mml:mi><mml:mo>)</mml:mo></mml:mrow></mml:mfrac></mml:math></disp-formula>with <italic>F(T)</italic> being the response of development to temperature (here the response of LER). Because developmental time (or thermal time t<sub>20°C</sub>) is the reciprocal of development rate, it results in:
<disp-formula id="E4"><label>(Eq.4)</label><mml:math id="MM4"><mml:msub><mml:mrow><mml:mi>t</mml:mi></mml:mrow><mml:mrow><mml:mn>20</mml:mn><mml:mo>°</mml:mo><mml:mi mathvariant="normal">C</mml:mi></mml:mrow></mml:msub><mml:mo>=</mml:mo><mml:mi>t</mml:mi><mml:mo>(</mml:mo><mml:mi>T</mml:mi><mml:mo stretchy="true">)</mml:mo><mml:mfrac><mml:mrow><mml:mi>F</mml:mi><mml:mfenced separators="|"><mml:mrow><mml:mi>T</mml:mi></mml:mrow></mml:mfenced></mml:mrow><mml:mrow><mml:mi>F</mml:mi><mml:mo>(</mml:mo><mml:mn>20</mml:mn><mml:mo>°</mml:mo><mml:mi mathvariant="normal">C</mml:mi><mml:mo>)</mml:mo></mml:mrow></mml:mfrac></mml:math></disp-formula></p><p>Such a procedure was already applied in different studies of developmental processes (<xref rid="plw092-B20" ref-type="bibr">Louarn <italic>et al.</italic> 2010</xref>; <xref rid="plw092-B24" ref-type="bibr">Parent <italic>et al.</italic> 2009</xref>; <xref rid="plw092-B28" ref-type="bibr">Parent <italic>et al.</italic> 2010b</xref>), and was applied here for biomass accumulation processes and net CO<sub>2</sub> assimilation rate (A<sub>N</sub>).</p><p>In Experiment 2 and 3, <inline-formula id="IE2"><mml:math id="MM5"><mml:mfrac><mml:mrow><mml:mi>F</mml:mi><mml:mfenced separators="|"><mml:mrow><mml:mn>20</mml:mn><mml:mo>°</mml:mo><mml:mi mathvariant="normal">C</mml:mi></mml:mrow></mml:mfenced></mml:mrow><mml:mrow><mml:mi>F</mml:mi><mml:mo>(</mml:mo><mml:mi>T</mml:mi><mml:mo>)</mml:mo></mml:mrow></mml:mfrac></mml:math></inline-formula> was calculated in each thermal treatment from LER values directly measured in Experiment 2. In the other cases, <inline-formula id="IE3"><mml:math id="MM6"><mml:mfrac><mml:mrow><mml:mi>F</mml:mi><mml:mfenced separators="|"><mml:mrow><mml:mn>20</mml:mn><mml:mo>°</mml:mo><mml:mi mathvariant="normal">C</mml:mi></mml:mrow></mml:mfenced></mml:mrow><mml:mrow><mml:mi>F</mml:mi><mml:mo>(</mml:mo><mml:mi>T</mml:mi><mml:mo>)</mml:mo></mml:mrow></mml:mfrac></mml:math></inline-formula> was inferred from the regression function <italic>LER(T)</italic>.</p></sec><sec><title>Leaf senescence profiles</title><p>In Experiment 3, chlorophyll content was measured with a SPAD chlorophyll meter (Minolta, Plainfield, Illinois, USA). Each measurement was the average of 15 readings: 5 taken from along each of the three last-developed leaves. In each treatment, four plants were measured repeatedly: at anthesis and at 7, 13, 19, 25, 31, 38, 42 and 46 days after anthesis.</p><p>In each thermal scenario, a bilinear model was fitted to the dataset (<bold>see <xref ref-type="supplementary-material" rid="sup1">Supporting Information—Methods S1</xref></bold>). It comprised a constant value (SPAD<sub>0</sub>) until a time of senescence (t<sub>s</sub>), followed by a linear decrease in content after this point, with a slope a<sub>s</sub>. Because plants had the same thermal treatment before anthesis, SPAD<sub>0</sub> was fixed for all thermal scenarios and equalled the average value at anthesis for all treatments (SPAD<sub>0 </sub> = <sub> </sub>57.3). A similar procedure was carried out considering time <italic>t</italic> and t<sub>s</sub> as developmental time (<italic>t</italic><sub>20°C</sub> and t<sub>s.20°C</sub>, d<sub>20°C</sub>).</p></sec><sec><title>Biomass accumulation in the grain</title><p>In Experiment 3, the main spikes of four plants per thermal scenario were collected at 7, 13, 19, 25, 31 days after anthesis and at grain maturity, and seed number and average single grain dry weight (GDW) were measured after three days at 85 °C. Spikes with fewer than 30 seeds were not used in the analysis (6 in total were discarded from the whole experiment; <italic>n</italic> <inline-formula id="IE4"><mml:math id="MM7"><mml:mo>≥</mml:mo></mml:math></inline-formula> 3 was used for all sampling dates and thermal treatments).</p><p>Curves of biomass accumulation in the grain can be described with a 3 parameter logistic equation (<xref rid="plw092-B23" ref-type="bibr">Morita <italic>et al.</italic> 2005</xref>), modified here to obtain the theoretical grain weight at anthesis (W<sub>0</sub>, mg) as a parameter of the following equation (<bold>see <xref ref-type="supplementary-material" rid="sup1">Supporting Information—Methods S1</xref></bold>):
<disp-formula id="E5"><label>(Eq.5)</label><mml:math id="MM8"><mml:mi>W</mml:mi><mml:mfenced separators="|"><mml:mrow><mml:mi>t</mml:mi></mml:mrow></mml:mfenced><mml:mo>=</mml:mo><mml:mfrac><mml:mrow><mml:msub><mml:mrow><mml:mi mathvariant="normal">W</mml:mi></mml:mrow><mml:mrow><mml:mn>0</mml:mn></mml:mrow></mml:msub><mml:mfenced separators="|"><mml:mrow><mml:mn>1</mml:mn><mml:mo>+</mml:mo><mml:msup><mml:mrow><mml:mi mathvariant="normal">e</mml:mi></mml:mrow><mml:mrow><mml:mfenced separators="|"><mml:mrow><mml:mi mathvariant="normal">λ</mml:mi><mml:mi mathvariant="normal"> </mml:mi><mml:msub><mml:mrow><mml:mi mathvariant="normal">t</mml:mi></mml:mrow><mml:mrow><mml:mn>0</mml:mn></mml:mrow></mml:msub></mml:mrow></mml:mfenced></mml:mrow></mml:msup></mml:mrow></mml:mfenced></mml:mrow><mml:mrow><mml:mn>1</mml:mn><mml:mo>+</mml:mo><mml:msup><mml:mrow><mml:mi mathvariant="normal">e</mml:mi></mml:mrow><mml:mrow><mml:mfenced separators="|"><mml:mrow><mml:mo>-</mml:mo><mml:mi mathvariant="normal">λ</mml:mi><mml:mi mathvariant="normal"> </mml:mi><mml:mfenced separators="|"><mml:mrow><mml:mi>t</mml:mi><mml:mo>-</mml:mo><mml:msub><mml:mrow><mml:mi mathvariant="normal">t</mml:mi></mml:mrow><mml:mrow><mml:mn>0</mml:mn></mml:mrow></mml:msub></mml:mrow></mml:mfenced></mml:mrow></mml:mfenced></mml:mrow></mml:msup></mml:mrow></mml:mfrac></mml:math></disp-formula></p><p><italic>W(t)</italic> is the weight of one seed (mg) at time <italic>t</italic> (in days) after anthesis, λ (in d<sup>−</sup><sup>1</sup>) is the slope factor controlling the steepness of the curve and <italic>t</italic><sub>0</sub> is the inflection point, or time at which the seed is half the final weight. Because the plants were transferred to the different thermal treatments at anthesis, W<sub>0</sub> was considered as common in all treatments (W<sub>0 </sub> = <sub> </sub>1.65 mg, <bold>see <xref ref-type="supplementary-material" rid="sup1">Supporting Information—Methods S1</xref></bold>).</p><p><xref ref-type="disp-formula" rid="E5">Eq.5</xref> was fitted in each thermal scenario, considering either time or developmental time (<italic>t<sub>20°C</sub></italic> in d<sub>20°C</sub>). In the last case, the two free parameters are expressed with developmental time units (<italic>t</italic><sub>0.20°C</sub> in d<sub>20°C</sub>; λ<sub>20°C</sub> in d<sub>20°C</sub><sup>−</sup><sup>1</sup>). Because <italic>t</italic><sub>0.20°C</sub> values were similar between treatments, a single <italic>t</italic><sub>0_20°C</sub> value common to all treatments was determined (<bold>see <xref ref-type="supplementary-material" rid="sup1">Supporting Information—Methods S1</xref></bold>). Respective values of <italic>t</italic><sub>0</sub> were then calculated in each treatment. In this case, λ is the only free parameter.</p><p>The grain growth rate <italic>GGR(t)</italic>, was obtained by derivation of <xref ref-type="disp-formula" rid="E5">Eq.5</xref> (<bold>see <xref ref-type="supplementary-material" rid="sup1">Supporting Information—Methods S1</xref></bold>). The grain growth rate is maximal (GGR<sub>max</sub>) at the inflection point, namely <italic>t</italic><sub>0</sub>.
<disp-formula id="E6"><label>(Eq.6)</label><mml:math id="MM9"><mml:msub><mml:mrow><mml:mi mathvariant="normal">G</mml:mi><mml:mi mathvariant="normal">G</mml:mi><mml:mi mathvariant="normal">R</mml:mi></mml:mrow><mml:mrow><mml:mi mathvariant="normal">m</mml:mi><mml:mi mathvariant="normal">a</mml:mi><mml:mi mathvariant="normal">x</mml:mi></mml:mrow></mml:msub><mml:mo>=</mml:mo><mml:mi mathvariant="normal">G</mml:mi><mml:mi mathvariant="normal">G</mml:mi><mml:mi mathvariant="normal">R</mml:mi><mml:mo>(</mml:mo><mml:msub><mml:mrow><mml:mi> </mml:mi><mml:mi>t</mml:mi></mml:mrow><mml:mrow><mml:mn>0</mml:mn></mml:mrow></mml:msub><mml:mo>)</mml:mo><mml:mo>=</mml:mo><mml:mfrac><mml:mrow><mml:msub><mml:mrow><mml:mi mathvariant="normal">λ</mml:mi><mml:mi mathvariant="normal"> </mml:mi><mml:mi mathvariant="normal">W</mml:mi></mml:mrow><mml:mrow><mml:mn>0</mml:mn></mml:mrow></mml:msub><mml:mfenced separators="|"><mml:mrow><mml:mn>1</mml:mn><mml:mo>+</mml:mo><mml:msup><mml:mrow><mml:mi mathvariant="normal">e</mml:mi></mml:mrow><mml:mrow><mml:mfenced separators="|"><mml:mrow><mml:mi mathvariant="normal">λ</mml:mi><mml:msub><mml:mrow><mml:mi mathvariant="normal"> </mml:mi><mml:mi mathvariant="normal">t</mml:mi></mml:mrow><mml:mrow><mml:mn>0</mml:mn></mml:mrow></mml:msub></mml:mrow></mml:mfenced></mml:mrow></mml:msup></mml:mrow></mml:mfenced></mml:mrow><mml:mrow><mml:mn>4</mml:mn></mml:mrow></mml:mfrac></mml:math></disp-formula>with time and model parameters expressed either with time or developmental time units.</p><p>Note that with <italic>t</italic><sub>0.20°C</sub> and W<sub>0</sub> fixed, GGR<sub>max.20°C</sub> depends only on λ<sub>20°C</sub> (and the reciprocal, λ<sub>20°C</sub> depends only on GGR<sub>max.20°C</sub>). GGR<sub>max.20°C</sub> alone can therefore explain the kinetics of grain growth rate.</p><p>Grain filling duration (t<sub>f</sub>) was calculated as the duration between anthesis and the time at which the grain reached 95% of its final weight (<bold>see <xref ref-type="supplementary-material" rid="sup1">Supporting Information—Methods S1</xref></bold>).
<disp-formula id="E7"><label>(Eq.7)</label><mml:math id="MM10"><mml:msub><mml:mrow><mml:mi mathvariant="normal">t</mml:mi></mml:mrow><mml:mrow><mml:mi mathvariant="normal">f</mml:mi></mml:mrow></mml:msub><mml:mo>=</mml:mo><mml:mo>-</mml:mo><mml:mfrac><mml:mrow><mml:mn>1</mml:mn><mml:mi> </mml:mi></mml:mrow><mml:mrow><mml:mi>λ</mml:mi><mml:mo></mml:mo></mml:mrow></mml:mfrac><mml:mrow><mml:mrow><mml:mi mathvariant="normal">ln</mml:mi></mml:mrow><mml:mo></mml:mo><mml:mrow><mml:mfenced open="[" close="]" separators="|"><mml:mrow><mml:mfrac><mml:mrow><mml:mn>5</mml:mn><mml:mi> </mml:mi></mml:mrow><mml:mrow><mml:mn>95</mml:mn><mml:mo></mml:mo></mml:mrow></mml:mfrac></mml:mrow></mml:mfenced></mml:mrow></mml:mrow><mml:mo>+</mml:mo><mml:msub><mml:mrow><mml:mi mathvariant="normal">t</mml:mi></mml:mrow><mml:mrow><mml:mn>0</mml:mn></mml:mrow></mml:msub></mml:math></disp-formula></p></sec><sec><title>Grain growth simulations</title><p>For any thermal scenario, a time series (0 to 100 days after anthesis, time step =1 d) was built, with corresponding photoperiod <italic>PP(t)</italic>, <italic>T°<sub>day</sub>(t)</italic>, <italic>T°<sub>night</sub>(t)</italic> and <italic>T°<sub>ave</sub>(t). t<sub>20°C</sub>(t)</italic>, <italic>P<sub>N</sub>(t)</italic>, <italic>R(t)</italic> were calculated from parameters of <xref ref-type="disp-formula" rid="E2">Eq.2</xref> (parameter values differing between processes). <italic>A<sub>N.20°C</sub>(t)</italic> was calculated from <xref ref-type="disp-formula" rid="E1">Eq.1</xref> and <xref ref-type="disp-formula" rid="E3">3</xref>. <italic>λ <sub>20°C</sub> (t)</italic> was inferred from the linear relationship between λ <sub>20°C</sub> and A<sub>N.20°C</sub> obtained in Experiment 3. <italic>GGR</italic><sub>20°C</sub><italic>(t)</italic> was calculated (<bold>see <xref ref-type="supplementary-material" rid="sup1">Supporting Information—Methods S1</xref></bold>) and individual grain weight was then obtained at each <italic>t</italic> by numerically integrating <italic>GGR</italic><sub>20°C</sub> between anthesis and the corresponding <italic>t<sub>20°C</sub>(t)</italic>.
<disp-formula id="E8"><label>(Eq.8)</label><mml:math id="MM11"><mml:mi>W</mml:mi><mml:mfenced separators="|"><mml:mrow><mml:mi>t</mml:mi></mml:mrow></mml:mfenced><mml:mo>=</mml:mo><mml:mi>W</mml:mi><mml:mfenced separators="|"><mml:mrow><mml:msub><mml:mrow><mml:mi>t</mml:mi></mml:mrow><mml:mrow><mml:mn>20</mml:mn><mml:mo>°</mml:mo><mml:mi>C</mml:mi></mml:mrow></mml:msub></mml:mrow></mml:mfenced><mml:mo>=</mml:mo><mml:msub><mml:mrow><mml:mi>W</mml:mi></mml:mrow><mml:mrow><mml:mn>0</mml:mn></mml:mrow></mml:msub><mml:mrow><mml:msubsup><mml:mo stretchy="false">∫</mml:mo><mml:mrow><mml:mi>x</mml:mi><mml:mo>=</mml:mo><mml:mn>0</mml:mn></mml:mrow><mml:mrow><mml:msub><mml:mrow><mml:mi>t</mml:mi></mml:mrow><mml:mrow><mml:mn>20</mml:mn><mml:mo>°</mml:mo><mml:mi>C</mml:mi></mml:mrow></mml:msub></mml:mrow></mml:msubsup><mml:mrow><mml:msub><mml:mrow><mml:mi>G</mml:mi><mml:mi>G</mml:mi><mml:mi>R</mml:mi></mml:mrow><mml:mrow><mml:mn>20</mml:mn><mml:mo>°</mml:mo><mml:mi>C</mml:mi></mml:mrow></mml:msub><mml:mo>(</mml:mo><mml:mi>x</mml:mi><mml:mo>)</mml:mo><mml:mi>d</mml:mi><mml:mi>x</mml:mi></mml:mrow></mml:mrow></mml:math></disp-formula></p></sec><sec><title>Data from the literature</title><p>Some data were collected from the literature (<xref rid="plw092-B1" ref-type="bibr">Alkhatib and Paulsen 1984</xref>; <xref rid="plw092-B42" ref-type="bibr">Tashiro and Wardlaw 1990</xref>; <xref rid="plw092-B47" ref-type="bibr">Wardlaw <italic>et al.</italic> 2002</xref>; <xref rid="plw092-B48" ref-type="bibr">Wardlaw <italic>et al.</italic> 1989a,b</xref>; <xref rid="plw092-B55" ref-type="bibr">Zahedi <italic>et al.</italic> 2003</xref>; <xref rid="plw092-B56" ref-type="bibr">Zhao <italic>et al.</italic> 2007</xref>) and are summarized online <bold>[see <xref ref-type="supplementary-material" rid="sup1">Supporting Information—Table S1</xref>]</bold>. The positions of the data points were recorded in figures by image analysis (software ImageJ; <ext-link ext-link-type="uri" xlink:href="http://rsbweb.nih.gov/ij">http://rsbweb.nih.gov/ij/</ext-link>). The grain weight reductions between thermal treatments found in these studies were compared to simulations carried out with the above procedure.</p></sec></sec><sec><title>Results</title><sec><title>Net CO<sub>2</sub> assimilation rate per unit of plant development decreased when temperature rose</title><p>In plants where leaf 6 was emerging, rate of leaf 6 elongation (LER) was measured at five constant temperatures in the range 11 to 29 °C (<xref ref-type="fig" rid="plw092-F1">Fig.1a;</xref> Experiment 1, <italic>n</italic> > 8). The equation of <xref rid="plw092-B16" ref-type="bibr">Johnson <italic>et al.</italic> (1942)</xref> modified by <xref rid="plw092-B26" ref-type="bibr">Parent and Tardieu (2012)</xref> fitted well with experimental data (<xref ref-type="fig" rid="plw092-F1">Fig.1a</xref>, <italic>R</italic><sup>2 </sup> = <sup> </sup>0.99) with response parameters (Δ<inline-formula id="IE5"><mml:math id="MM101"><mml:msubsup><mml:mrow><mml:mi mathvariant="normal">H</mml:mi></mml:mrow><mml:mrow><mml:mi mathvariant="normal">A</mml:mi></mml:mrow><mml:mrow><mml:mtext>‡</mml:mtext></mml:mrow></mml:msubsup></mml:math></inline-formula>=69.1 kJ mol<sup>−</sup><sup>1</sup>; <italic>T</italic><sub>0 </sub> = <sub> </sub>29.2 °C) close to those previously determined in the meta-analysis of <xref rid="plw092-B26" ref-type="bibr">Parent and Tardieu (2012)</xref>. The temperature response curves of net day photosynthesis (P<sub>N</sub>) and dark respiration (R) were also both adequately described by this equation (<xref ref-type="fig" rid="plw092-F1">Fig.1b</xref>, <italic>n</italic> > 4, <italic>R</italic><sup>2 </sup> = <sup> </sup>0.99 and 0.97, respectively). Response of respiration was not far from that of development (Δ<inline-formula id="IE6"><mml:math id="MM102"><mml:msubsup><mml:mrow><mml:mi mathvariant="normal">H</mml:mi></mml:mrow><mml:mrow><mml:mi mathvariant="normal">A</mml:mi></mml:mrow><mml:mrow><mml:mtext>‡</mml:mtext></mml:mrow></mml:msubsup></mml:math></inline-formula>=74.9 kJ mol<sup>−</sup><sup>1</sup>) but the slope of P<sub>N</sub> was flatter under rising temperatures, as indicated by the low value of Δ<inline-formula id="IE7"><mml:math id="MM103"><mml:msubsup><mml:mrow><mml:mi mathvariant="normal">H</mml:mi></mml:mrow><mml:mrow><mml:mi mathvariant="normal">A</mml:mi></mml:mrow><mml:mrow><mml:mtext>‡</mml:mtext></mml:mrow></mml:msubsup></mml:math></inline-formula> (19.3 kJ mol<sup>−</sup><sup>1</sup>). When measured under saturating light, the response of photosynthesis was steeper (Δ<inline-formula id="IE8"><mml:math id="MM104"><mml:msubsup><mml:mrow><mml:mi mathvariant="normal">H</mml:mi></mml:mrow><mml:mrow><mml:mi mathvariant="normal">A</mml:mi></mml:mrow><mml:mrow><mml:mtext>‡</mml:mtext></mml:mrow></mml:msubsup></mml:math></inline-formula>=36.2 kJ mol<sup>−</sup><sup>1</sup>, not shown) but still less than that of respiration or development. The temperature response curve of the net CO<sub>2</sub> assimilation per day (A<sub>N</sub>, <xref ref-type="fig" rid="plw092-F1">Fig.1b</xref>) was then calculated from P<sub>N</sub> and R (<xref ref-type="disp-formula" rid="E1">Eq.1</xref>).
<fig id="plw092-F1" orientation="portrait" position="float"><label>Figure 1</label><caption><p>Temperature responses (experiment 1) of leaf elongation rate (LER), daily net photosynthesis (P<sub>N</sub>), daily dark respiration (R) and daily net CO<sub>2</sub> assimilation per day (A<sub>N</sub>) expressed with time (d) or developmental time units (A<sub>N.20°C</sub>, d<sub>20°C</sub>). Dots: average values; error bars: confidence intervals (<italic>p</italic> =0.95); lines: regression from Eq.2. (<bold>a</bold>) LER (<italic>n</italic> > 8). (<bold>b</bold>) P<sub>N</sub> (squares), R (triangles) and A<sub>N</sub> (circles) (<italic>n</italic> > 4). (<bold>c</bold>) LER (black dots) and A<sub>N</sub> (white dots) normalised by their respective values at 20 °C. Dashed line displays the temperature response of A<sub>N</sub> under saturating light. (<bold>d</bold>) A<sub>N.20°C</sub>.</p></caption><graphic xlink:href="plw092f1p"></graphic></fig></p><p>Temperature response curves were normalized so that they intersected the same value at 20 °C (<xref ref-type="fig" rid="plw092-F1">Fig.1c</xref>), facilitating the comparison in the absence of any differences in units or magnitude (<xref rid="plw092-B25" ref-type="bibr">Parent <italic>et al.</italic> 2010a</xref>). Because leaf elongation is part of the multitude of development processes sharing a common response to temperature (<xref rid="plw092-B28" ref-type="bibr">Parent <italic>et al.</italic> 2010b</xref>; <xref rid="plw092-B26" ref-type="bibr">Parent and Tardieu 2012</xref>), this temperature response of normalized LER was considered as the response of development processes to temperature. It was used to adjust times and rates of other processes by the effect of temperature on general development (developmental time calculation).</p><p>The development rate accelerated more than the carbon assimilation rate as temperature increased, until the optimum temperature was reached (26.6 and 25.5 °C for LER and A<sub>N</sub>, respectively). Under saturating light, the two responses were more similar, although development still accelerated more than A<sub>N</sub> (data not shown). Expressing A<sub>N</sub> per unit of developmental time (A<sub>N.20°C</sub>) can be thought as an amount of carbon assimilated per standard unit of leaf elongation (and by inference, per unit of any developmental process). A<sub>N.20°C</sub> decreased when the temperature rose across the measured range (<xref ref-type="fig" rid="plw092-F1">Fig.1d</xref>), indicating that the amount of assimilated carbon available per unit of development decreased under rising temperatures.</p></sec><sec><title>Net CO<sub>2</sub> assimilation rate per unit of leaf development was linked to the dry mass per leaf area for plants grown under different thermal regimes without an additional effect of night temperature</title><p>Various scenarios of day/night temperature were applied at the appearance of leaf 6 to allow the net CO<sub>2</sub> assimilation rate to be viewed independently of development (<xref ref-type="fig" rid="plw092-F2">Fig. 2</xref>; Experiment 2, <italic>n</italic> = 6). LER increased about equally under increasing T°<sub>night</sub> or T°<sub>day</sub> (<xref ref-type="fig" rid="plw092-F2">Fig. 2a</xref>), and was therefore essentially the same under thermal scenarios (T°<sub>day</sub>/T°<sub>night</sub>) 20/20 °C and 25/15 °C. By contrast, R only increased under rising T°<sub>night</sub> and P<sub>N</sub> only increased under rising T°<sub>day</sub> [<bold>see <xref ref-type="supplementary-material" rid="sup1">Supporting Information<bold>—</bold>Table S2</xref></bold>]. Because P<sub>N</sub> values were much higher than R values and explained most of the variance in A<sub>N</sub> (not shown), significant differences in A<sub>N</sub> were only observed when T°<sub>day</sub> differed (<xref ref-type="fig" rid="plw092-F2">Fig. 2b</xref>). Therefore, treatment comparisons where only the night temperature differed (20/15 vs. 20/20 °C, or 25/15 vs. 25/20 °C) showed differences in LER with essentially no change in A<sub>N</sub>. Conversely, the comparison 25/15 vs. 20/20 °C showed differences in A<sub>N</sub> with essentially no change in LER. Overall, these thermal treatments resulted in contrasting CO<sub>2</sub> assimilation rates per unit of developmental time (<xref ref-type="fig" rid="plw092-F2">Fig. 2c</xref>), viewed here as the amount of assimilated carbon available per unit of leaf development.
<fig id="plw092-F2" orientation="portrait" position="float"><label>Figure 2</label><caption><p>Leaf elongation rate (LER, (<bold>a</bold>), net CO<sub>2</sub> assimilation per day (A<sub>N</sub>, (<bold>b</bold>) or day at 20 °C (A<sub>N.20°C</sub>, (<bold>c</bold>), leaf dry mass per area (LMA, averaged for leaves 4, 5, 6 and 7, (<bold>d</bold>) and the relationship between A<sub>N.20°C</sub> and LMA (<bold>e</bold>) under four different temperature scenarios (T°<sub>day</sub>/T°<sub>night</sub>, experiment 2). Bars: average values (<italic>n</italic> = 6); error bars: confidence intervals (<italic>p</italic> =0.95). Means with the same letter indicate that there were no significant differences in a pairwise t-test.</p></caption><graphic xlink:href="plw092f2p"></graphic></fig></p><p>The leaf dry mass per area (LMA), measured at anthesis on leaves 4, 5, 6 and 7, was affected by thermal treatments in all leaves <bold>[see <xref ref-type="supplementary-material" rid="sup1">Supporting Information—Fig. S1</xref>]</bold> even in leaves 4 and 5, which were already partly elongated before applying the different thermal scenarios. Consequently, the average LMA in the 4 measured leaves differed significantly between treatments (<xref ref-type="fig" rid="plw092-F2">Fig. 2d</xref>). These differences were mostly due to differences in leaf biomass rather than leaf area (respectively explaining 86.2 % and 2.7 % of the total variance, not shown). A temperature-induced rise in A<sub>N</sub> while maintaining similar leaf expansion rate would increase the amount of assimilated carbon per unit of leaf area expansion. Accordingly, LMA was significantly greater in the 25/15 °C treatment than in the 20/20 °C treatment (60.0 ± 4.1 versus 41.4 ± 3.8 g m<sup>−</sup><sup>2</sup>, <xref ref-type="fig" rid="plw092-F2">Fig. 2d</xref>). Conversely, a temperature-induced increase in LER without any changes in A<sub>N</sub> would decrease the amount of assimilated carbon per unit of leaf expansion. Accordingly, LMA was less under 20/20 °C than 20/15 °C (41.4 ± 3.8 versus 51.6 ± 2.5 g m<sup>−</sup><sup>2</sup>), and less under 25/20 °C than 25/15 °C (45.4 ± 2.9 versus 60.0 ± 4.1g m<sup>−</sup><sup>2</sup>). Overall, A<sub>N.20°C</sub> showed a strong positive correlation with LMA (<xref ref-type="fig" rid="plw092-F2">Fig. 2e</xref>, <italic>R</italic><sup>2 </sup> = <sup> </sup>0.96; <italic>p</italic> = 0.022 in a Pearson correlation test). Therefore, A<sub>N.20°C</sub> integrated the temperature effects on leaf expansion rate and CO<sub>2</sub> assimilation rate to explain differences in LMA observed between these different thermal scenarios.</p></sec><sec><title>Rates of progress towards grain maturity and leaf senescence depended only on the temperature response of development</title><p>Plants at anthesis were introduced to several temperature scenarios, and then leaf senescence and biomass accumulation in the grain were measured over time (<xref ref-type="fig" rid="plw092-F3">Fig. 3a</xref> and <xref ref-type="fig" rid="plw092-F4">Fig. 4a;</xref> Experiment 3; <italic>n</italic> > 4 for each time point). Chlorophyll content in the three last developed leaves, defined in SPAD units, was at first stable, and then decreased linearly. Fitting a bilinear model enabled the calculation of the time at which the chlorophyll level started to decrease (t<sub>s</sub>). This parameter was closely correlated with the average daily temperatures (from 20.0 ± 1.7 at 25/20 °C to 26.5 ± 3.4 d at 20/15 °C, <xref ref-type="fig" rid="plw092-F3">Fig. 3a</xref> inset). When time and model parameters were expressed in developmental time units (<xref ref-type="fig" rid="plw092-F3">Fig. 3b</xref>), profiles of leaf senescence were similar between thermal treatments (<italic>t</italic><sub>s.20°C</sub> ranging from 21.8 ± 3.4 to 23.2 ± 3.7 d<sub>20°C</sub>; <xref ref-type="fig" rid="plw092-F3">Fig. 3b</xref> inset).
<fig id="plw092-F3" orientation="portrait" position="float"><label>Figure 3</label><caption><p>Time courses of leaf chlorophyll amount (SPAD units) under different temperature regimes (experiment 3), 20/15 °C (blue), 20/20 °C (green), 25/15 °C (red) and 25/20 °C (orange). Time is expressed either as day (d, <bold>a</bold>) or developmental time (d<sub>20°C</sub>, <bold>b</bold>). Dots: average values (<italic>n</italic>≥ 4). Error bar: average confidence intervals (<italic>p</italic> = 0.95). Lines are bilinear regressions with 3 parameters (SPAD<sub>0</sub>, t<sub>s</sub>, a<sub>s</sub>). SPAD<sub>0</sub> is fixed and common to all treatments. <bold>Inset in a)</bold> Values of t<sub>s</sub>. Bars: parameter value ± confidence interval calculated by bootstrap (<italic>p</italic> = 0.95). <bold>Inset in b)</bold> Values of t<sub>s.20°C</sub>. Bars: parameter value ± confidence interval (<italic>p</italic> = 0.95).</p></caption><graphic xlink:href="plw092f3p"></graphic></fig><fig id="plw092-F4" orientation="portrait" position="float"><label>Figure 4</label><caption><p>Time courses of individual grain dry weight (GDW) under different temperature regimes (experiment 3), 20/15 °C (blue), 20/20 °C (green), 25/15 °C (red), 25/20 °C (orange). Time is expressed either as days (<bold>a</bold>, <bold>c</bold>) or developmental time (d<sub>20°C</sub>, <bold>b</bold>). <italic>M</italic>.: grain maturity. Dots: average values (<italic>n</italic>≥ 4). Error bars: average confidence intervals (<italic>P</italic> = 0.95). Lines are logistic regressions with 3 parameters (W<sub>0</sub>, <italic>t</italic><sub>0</sub>, λ). W<sub>0</sub> is fixed and common to all treatments. (<bold>a)</bold> λ and <italic>t</italic><sub>0</sub> are free in each treatment. <bold>Inset in a)</bold> values of <italic>t</italic><sub>0 </sub>± confidence interval (<italic>p</italic> = 0.95). (<bold>b</bold>) λ and <italic>t</italic><sub>0</sub> are free in each treatment but with time expressed as developmental time (d<sub>20°C</sub>). <bold>Inset in b)</bold> values of <italic>t</italic><sub>0_20°C </sub>±<sub> </sub>confidence interval (<italic>P</italic> = 0.95). (<bold>c</bold>) λ is the only free parameter in each treatment. <italic>t</italic><sub>0</sub> (<bold>d</bold>) is calculated in each treatment from a single <italic>t</italic><sub>0_20°C</sub> value (d<sub>20°C</sub>), common to all treatments.</p></caption><graphic xlink:href="plw092f4p"></graphic></fig></p><p>Fitting logistic curves (<xref ref-type="disp-formula" rid="E5">Eq.5</xref>) to the time courses of single grain dry weight (GDW; <xref ref-type="fig" rid="plw092-F4">Fig. 4a</xref>) resulted in various values of <italic>t</italic><sub>0</sub>, the time at which grain weight reached half of the final dry weight and growth was maximal (<xref ref-type="fig" rid="plw092-F4">Fig. 4a</xref> inset). Its values decreased with rising average temperatures (from 24.0 ± 0.5 to 17.9 ± 0.7 d). Similarly, the time taken for complete grain fill (t<sub>f</sub>) decreased by 11 d with rising temperatures (from 46.6 to 35.1 d, not shown). However, grain filling duration was similar in the 25/15 and 20/20 °C treatments (36.8 d and 38.4 d, not shown) indicating that it was largely independent of carbon assimilation. When time was expressed in developmental time units (d<sub>20°C</sub>, <xref ref-type="fig" rid="plw092-F4">Fig. 4b</xref>), values of <italic>t</italic><sub>0_20°C</sub> were similar across treatments (ranging from 19.8 ± 0.3 to 21.6 ± 0.7 d<sub>20°C</sub>, <xref ref-type="fig" rid="plw092-F4">Fig. 4b</xref> inset) as were the values of grain filling duration (from 39.2 to 42.3 d<sub>20°C</sub>, not shown).</p><p>Overall, rates toward grain maturity and rates of leaf senescence were similar across thermal treatments when expressed in developmental time. Grain filling duration was only dependent on average temperature, and mostly independent of carbon supply.</p></sec><sec><title>Maximum rates of biomass accumulation in individual grains were dependent on net CO<sub>2</sub> assimilation but independent of development rates</title><p>The time courses of biomass accumulation in the grain were adequately described by the logistic model when only one parameter (λ) was kept free in each thermal scenario (W<sub>0</sub> and <italic>t</italic><sub>0_20°C</sub> fixed in all treatments, <xref ref-type="fig" rid="plw092-F4">Fig. 4c</xref>, <italic>t</italic><sub>0_20°C </sub> = 20.2 d<sub>20°C</sub>; see Material and Methods <bold>[see <xref ref-type="supplementary-material" rid="sup1">Supporting Information—Methods S1</xref>]</bold>).</p><p>As the maximum rate of accumulation of dry weight in single grains (GGR<sub>max</sub>) and λ are interdependent variables (<xref ref-type="disp-formula" rid="E6">Eq.6</xref>), grain growth responses to temperature are hereafter described in terms of GGR<sub>max</sub> only (more intuitive than λ). GGR<sub>max</sub> varied between thermal treatments, especially where day temperature differed (<xref ref-type="fig" rid="plw092-F4 plw092-F5">Figs 4c and 5a</xref>). Because temperature accelerated leaf senescence and progress towards grain maturity similarly, effects of temperature on rates of grain dry weight accumulation could not be attributed to one or the other of these factors.
<fig id="plw092-F5" orientation="portrait" position="float"><label>Figure 5</label><caption><p>Values of maximum grain growth rate (GGR<sub>max</sub>, (<bold>a</bold>) estimated from regression displayed in Fig.4c (W<sub>0</sub> and <italic>t</italic><sub>0</sub> fixed), expressed with time (black bars) or developmental time units (white bars), and the relationship between net CO<sub>2</sub> assimilation per d<sub>20°C</sub> (A<sub>N.20°C</sub>) and final individual grain weight or GGR<sub>max.20°C</sub> in the 4 different temperature scenarios (<bold>b</bold>). (<bold>a</bold>) Bars: estimated parameter value. Error bar: confidence interval (<italic>P</italic> = 0.95). (<bold>b</bold>) Grey triangles: final grain weight. White circles: GGR<sub>max.20°C</sub>. A<sub>N.20°C</sub> values were measured in Experiment 2 and shown in <xref ref-type="fig" rid="plw092-F2">Fig. 2</xref><bold>[see <xref ref-type="supplementary-material" rid="sup1">Supporting Information<bold>—</bold>Table S2</xref>]</bold>.</p></caption><graphic xlink:href="plw092f5p"></graphic></fig></p><p>Relative to the 25/15 °C treatment, the 20/20 °C treatment showed an increase in CO<sub>2</sub> assimilation (A<sub>N</sub>) and GGR<sub>max</sub> (1.18 ± 0.01 to 1.44 ± 0.02 mg d<sup>−</sup><sup>1</sup>, <xref ref-type="fig" rid="plw092-F5">Fig. 5a</xref>) but a similar rate of progress toward grain maturity. By contrast, increasing night temperature, <italic>i.e.</italic> 20/15 vs. 20/20 °C, or 25/15 vs. 25/20 °C, increased development rate but not A<sub>N</sub> or GGR<sub>max</sub> (<xref ref-type="fig" rid="plw092-F5">Fig. 5a</xref>). Therefore, GGR<sub>max</sub> appeared to be only dependent on carbon assimilation rate and largely independent of development rate.</p><p>Overall, the two contributors to final grain weight, the rate toward grain maturity and the rate of biomass accumulation in the grain, behaved independently, and correlated with temperature responses of development and of carbon assimilation, respectively.</p></sec><sec><title>Net CO<sub>2</sub> assimilation rate expressed in developmental units explained the differences in dynamics of grain biomass accumulation</title><p>When expressed in developmental units, maximum grain growth rate (GGR<sub>max.20°C</sub>, <xref ref-type="fig" rid="plw092-F5">Fig. 5a</xref>) was dependent on both the rate of development and of CO<sub>2</sub> assimilation. GGR<sub>max.20°C</sub> can be thought as the biomass accumulation per standard unit of grain development. In the same way, A<sub>N</sub> expressed per unit of developmental time (A<sub>N.20°C</sub>) can be thought as the amount of assimilated carbon available per unit of grain development. An increase in CO<sub>2</sub> assimilation for a similar grain development rate increased GGR<sub>max.20°C</sub> (20/20 <italic>vs</italic>. 25/15 °C; 1.18 to 1.40 mg d<sub>20°C</sub><sup>−</sup><sup>1</sup>, <xref ref-type="fig" rid="plw092-F5">Fig. 5a</xref>). Increasing the grain development rate without increasing the CO<sub>2</sub> assimilation rate resulted in lower GGR<sub>max.20°C</sub>, as shown in treatments 20/15 <italic>vs</italic>. 20/20 °C or 25/15 <italic>vs</italic>. 25/20 °C, <xref ref-type="fig" rid="plw092-F5">Fig. 5a</xref>). A<sub>N.20°C</sub> was positively correlated with GGR<sub>max.20°C</sub> (<xref ref-type="fig" rid="plw092-F5">Fig. 5b</xref>, <italic>R</italic><sup>2 </sup> = <sup> </sup>0.97, <italic>p</italic> = 0.009 in a Pearson correlation test). Because GGR<sub>max.20°C</sub> could completely describe the time course of biomass accumulation, A<sub>N.20°C</sub> was correlated with final grain weight (<xref ref-type="fig" rid="plw092-F5">Fig. 5b</xref>, <italic>R</italic><sup>2 </sup> = <sup> </sup>0.98, <italic>p</italic> = 0.005 in a Pearson correlation test).</p><p>Overall, by integrating the temperature effects on the rates of grain development and CO<sub>2</sub> assimilation, A<sub>N.20°C</sub> was able to explain the differences in the grain growth rate and final grain weight observed between the different thermal scenarios.</p><p>This relationship was used to simulate final grain weight effects reported in seven different papers for various thermal scenarios involving T°<sub>day</sub> up to 30 °C and T°<sub>night</sub> up to 25 °C (<xref ref-type="fig" rid="plw092-F6">Fig. 6</xref>). The predicted grain weight reductions were not far from the observed ones (<italic>R</italic><sup>2 </sup> = <sup> </sup>0.79), suggesting that the relationship between A<sub>N.20°C</sub> and grain growth rate could hold true for other genotypes, environmental conditions, and thermal scenarios within the investigated range. However, the model had a tendency to over-estimate the negative effect of rising temperatures (average bias of 16%), indicating a genetic variability for this relationship, or the influence of other physiological processes such as carbon remobilization to the grains.
<fig id="plw092-F6" orientation="portrait" position="float"><label>Figure 6</label><caption><p>Observed values <italic>vs.</italic> calculated values for the reduction in final grain weight between temperatures treatments. Observed data come from the literature <bold>[see <xref ref-type="supplementary-material" rid="sup1">Supporting Information—Table S1</xref>]</bold>. Dashed line is the model x = y.</p></caption><graphic xlink:href="plw092f6p"></graphic></fig></p></sec></sec><sec><title>Discussion</title><sec><title>Temperature response patterns of biomass accumulation in leaves and grains as a consequence of the discrepancy between development and carbon assimilation responses</title><p>Various studies have emphasized a role of altered carbon supply-demand in the effects of high temperature on plant processes (<xref rid="plw092-B43" ref-type="bibr">Taub <italic>et al.</italic> 2000</xref>; <xref rid="plw092-B44" ref-type="bibr">Vasseur <italic>et al.</italic> 2011</xref>; <xref rid="plw092-B45" ref-type="bibr">Vile <italic>et al.</italic> 2012</xref>). Yet, this concept has rarely been tested by concurrently monitoring temperature responses of development, carbon assimilation and biomass accumulation (<xref rid="plw092-B32" ref-type="bibr">Poorter <italic>et al.</italic> 2009</xref>), or in a range of temperatures that were not harmful to photosynthesis (<xref rid="plw092-B44" ref-type="bibr">Vasseur <italic>et al.</italic> 2011</xref>; <xref rid="plw092-B45" ref-type="bibr">Vile <italic>et al.</italic> 2012</xref>). Therefore, we simultaneously monitored the temperature responses of development, respiration and photosynthesis in the non-stressing range. These responses were divergent, resulting in a variation in carbon supply relative to development across various thermal treatments. Under rising temperatures, an increase in photosynthesis increased both LMA and grain weight, while accelerated development reduced leaf and grain weights. We showed that the discrepancy between the temperature responses of development and carbon assimilation could explain the observed patterns of biomass accumulation in wheat leaves and grains across a range of thermal scenarios.</p></sec><sec><title>Expressing net CO<sub>2</sub> assimilation and biomass accumulation per unit of development summarizes the effects of temperature on development and carbon assimilation</title><p>Here, we examined the possibility of using the thermal compensation of time and rates to dissect the factors influencing biomass accumulation. Previously, this concept was applied to enable the effects of other environmental variables on leaf expansion (<xref rid="plw092-B28" ref-type="bibr">Parent <italic>et al.</italic> 2010b</xref>), cell expansion profiles in leaf (<xref rid="plw092-B24" ref-type="bibr">Parent <italic>et al.</italic> 2009</xref>) or endogenous rhythms (<xref rid="plw092-B31" ref-type="bibr">Poire <italic>et al.</italic> 2010</xref>) to be studied independently of the effect of temperature on development. In the current study, by expressing the rates of processes not classified as ‘development processes’, such as biomass accumulation in tissues, in terms of rate per unit of development, we were able to quantify the component of the biomass accumulation response that was controlled purely by fluctuations in net carbon assimilation. Expressing the net assimilation rate in terms of developmental time therefore summarized the effects of temperature on photosynthesis, respiration and development. It can be thought as the ratio of the source/development sink, or as the amount of assimilated carbon available per unit of plant development. In addition, a simple model using this trait as the indicator of source-sink dynamics was able to explain most of the effects of thermal scenarios on grain weight, across different genotypes and environmental conditions.</p><p>By allowing the contribution of net carbon fixation on biomass accumulation across a temperature range to be followed independently of the effect of temperature on development, this approach makes possible an assessment of the impact of other factors (<italic>e.g.</italic> light intensity) on biomass accumulation across a range of temperatures. Furthermore, it could provide an approach for quantifying longer lasting heat damage caused by factors such as protein denaturation that are likely encountered at much higher temperatures, independent of reversible responses of a purely thermodynamic nature.</p></sec><sec><title>Rising night temperature is likely to decrease biomass production</title><p>Increasing either night or day temperature would accelerate development by the same degree (<xref rid="plw092-B23" ref-type="bibr">Morita <italic>et al.</italic> 2005</xref>; <xref rid="plw092-B25" ref-type="bibr">Parent <italic>et al.</italic> 2010a</xref>), but only increases in T°<sub>night</sub> would increase respiration without any compensatory increase in photosynthesis. Simple simulations also indicate that A<sub>N.20°C</sub> would be more sensitive to an increase in T°<sub>night</sub> than to a similar increase in T°<sub>day</sub> or the 24-h average temperature T°<sub>ave</sub> (not shown). Indeed, our own experiment employing four day/night thermal treatments demonstrated that increasing T°<sub>night</sub> reduced grain biomass more than increasing T°<sub>day</sub> or T°<sub>ave</sub>. In the simulation shown in <xref ref-type="supplementary-material" rid="sup1"><bold>Supporting Information—Fig. S2</bold></xref>, increasing night temperature by 5 °C decreased A<sub>N.20°C</sub> from 1.33 to 1.09 mol m<sup>−</sup><sup>2</sup> d<sub>20°C</sub><sup>−1</sup> (not shown) and therefore decreased final grain weight by 15.3 %.</p><p>The effect of maximum daily temperature (T<sub>max</sub>) and minimum daily temperature (T<sub>min</sub>; which occurs during the night) on the performance of wheat and rice in the field has been examined using data across multiple environments. Such studies have revealed greater and more frequent negative impacts of warming during the night than warming during the day (<xref rid="plw092-B29" ref-type="bibr">Peng <italic>et al.</italic> 2004</xref>; <xref rid="plw092-B52" ref-type="bibr">Welch <italic>et al.</italic> 2010</xref>; <xref rid="plw092-B60" ref-type="bibr">Lobell and Ortiz-Monasterio 2007</xref>; <xref rid="plw092-B12" ref-type="bibr">Cossani and Reynolds 2012</xref>). Our findings offer a potential explanation for these differential effects of day and night temperature on crop productivity in the field. In this study, no additional ‘hidden’ effect of night temperature was detected.</p></sec><sec><title><italic>Could temperature acclimation change this pattern</italic>?</title><p>While temperature changes in the non-stressing range can perturb photosynthesis and respiration in the short-term, the rates of these two processes can eventually recover completely, due to acclimation (<xref rid="plw092-B2" ref-type="bibr">Atkin <italic>et al.</italic> 2006</xref>; <xref rid="plw092-B10" ref-type="bibr">Campbell <italic>et al.</italic> 2007</xref>). Acclimation might make net CO<sub>2</sub> assimilation insensitive to any long-term temperature change (<xref rid="plw092-B2" ref-type="bibr">Atkin <italic>et al.</italic> 2006</xref>). By contrast, development rate was found to be stably dependent on temperature, and did not acclimate (<xref rid="plw092-B26" ref-type="bibr">Parent and Tardieu 2012</xref>). Therefore, it is possible that long term responses of biomass accumulation to rising temperature, such as those experienced across the seasons, may only depend on the temperature responses of development, resulting in a greater reduction in biomass (mass per unit of development) than is predicted from the presented model. The model may apply better to day to day fluctuations, such as brief heat waves of several days duration, which commonly occur in the southern Australian wheat belt during the flowering and grain filling period and correlate with significant grain yield losses (<xref rid="plw092-B50" ref-type="bibr">Wardlaw and Wrigley 1994</xref>).</p></sec><sec><title>Diversity of biomass accumulation responses</title><p>The temperature response of CO<sub>2</sub> assimilation per unit of plant development can present a large diversity. Firstly, there is a large diversity between plant species for the temperature responses of photosynthesis and respiration rates (<xref rid="plw092-B21" ref-type="bibr">Loveys <italic>et al.</italic> 2002</xref>), as well as for temperature acclimation of these processes (<xref rid="plw092-B2" ref-type="bibr">Atkin <italic>et al.</italic> 2006</xref>). In addition, there is a large genetic variability for development rate <italic>per se</italic> (<xref rid="plw092-B9" ref-type="bibr">Borras-Gelonch <italic>et al.</italic> 2010</xref>). The temperature response of development, while highly conserved in each species presented also a large variability between species (<xref rid="plw092-B26" ref-type="bibr">Parent and Tardieu 2012</xref>). It follows that the overall response of the net assimilation per unit of plant development could present a large diversity between genotypes or species.</p><p>Grain biomass and yield in a broad sense do not depend only on the total assimilated carbon. A large genetic variability can be found in the ability of plants to mobilize and allocate carbon to the grains (<xref rid="plw092-B36" ref-type="bibr">Reynolds <italic>et al.</italic> 2009</xref>). It probably explains why the model over-estimated the effects of temperature on grain size in <xref ref-type="fig" rid="plw092-F6">Fig. 6</xref>. These processes have their own response to temperature (<xref rid="plw092-B33" ref-type="bibr">Poorter <italic>et al.</italic> 2012</xref>) and can therefore present interesting genetic variability. In wheat, improving photosynthesis efficiency and partitioning to the grain are the central targets of the International Wheat Consortium (IWC, <xref rid="plw092-B35" ref-type="bibr">Reynolds <italic>et al.</italic> 2011</xref>).</p><p>The presented model was intentionally simple, used only to test the presented hypothesis, that the discrepancy between CO<sub>2</sub> assimilation and development responses were responsible for the response of biomass accumulation in tissues. However, the diversity of underlying physiological processes presented above would result in a wide diversity of carbon assimilation per unit of plant development. Experimenters need to be aware of these factors, and this model should be built on or adjusted to account for them, to suit any particular experimental system.</p></sec></sec><sec sec-type="conclusion"><title>Conclusion</title><p>Models based on data collected under controlled conditions were developed to predict net CO<sub>2</sub> assimilation rate per unit of plant development under various temperature scenarios. This unit for expressing biomass accumulation rate (i) summarized the effect of the temperature responses of development, respiration and photosynthesis, (ii) provided a means of comparing rates of biomass accumulation obtained under different growth conditions, independent of the effects of temperature on development, and (iii) represents a potential approach for quantifying irreversible versus reversible responses that may occur in the extremely high temperature range. The model is likely to require modification under certain circumstances, <italic>e.g.</italic> where acclimation, photosynthate mobilization processes, and genotypic variation are additional factors in temperature responses.</p></sec><sec><title>Sources of Funding </title><p>This work was supported by the European projects FP7-244374 (DROPS) and FP7-613817 (MODEXTREME) and the Grains Research and Development Corporation (GRDC) project UA00123. ACPFG was also funded by the GRDC, the Australian Research Council, the Government of South Australia and the University of Adelaide.</p></sec><sec><title>Contributions by the Authors</title><p>Iman Lohraseb carried out most experiments; Nicholas C. Collins contributed to interpretation of the data and preparation of the manuscript; Boris Parent performed most analyses and prepared the manuscript</p></sec><sec><title>Conflict of Interest Statement</title><p>None declared.</p></sec><sec sec-type="supplementary-material"><title>Supplementary Material</title><supplementary-material content-type="local-data" id="sup1"><label>Supplementary Data</label><media xlink:href="plw092_Supp.pdf"><caption><p>Click here for additional data file.</p></caption></media></supplementary-material></sec></body><back><ack><title>Acknowledgements</title><p>The authors thank Dr. Everard Edwards for precious advice on gas exchange measurements, and Dr. Pierre Martre and Dr. Denis Vile for useful comments on the manuscript.</p><sec><title>Supporting Information</title><p>The following additional information is available in the online version of this article —</p><p><bold>Figure S1</bold>. Mass per leaf area in different leaves and thermal treatments.</p><p><bold>Figure S2</bold>. Simulation of the effect of night temperature on time courses of grain dry weight.</p><p><bold>Table S1</bold>. Summary of data coming from the literature.</p><p><bold>Table S2</bold>. 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