Plant Physiology Preview. Published on March 22, 2013, as DOI:10.1104/pp.112.211938
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Running Head:
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Soybean photosynthesis and yield with global change
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Correspondence:
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Carl J. Bernacchi
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193 E.R. Madigan Laboratory
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1201 W. Gregory Drive
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Urbana, IL 61801
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E-mail: [email protected]
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Tel : +1-217-333-8048
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Journal Research Area
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Whole Plant and Ecophysiology
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Copyright 2013 by the American Society of Plant Biologists
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Global warming can negate the expected CO
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photosynthesis and productivity for soybean grown in the
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Midwest United States
stimulation in
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Ursula M. Ruiz-Vera1,2, Matthew Siebers1,2, Sharon B. Gray1,2, David W. Drag1, David M.
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Rosenthal3, Bruce A. Kimball4, Donald R. Ort3,1,2, Carl J. Bernacchi3,1,2
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USA
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USA
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Department of Plant Biology, University of Illinois at Urbana-Champaign, Urbana, IL 61801,
Institute for Genomic Biology, University of Illinois at Urbana-Champaign, Urbana, IL 61801,
Global Change and Photosynthesis Research Unit, United States Department of Agriculture,
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Agricultural Research Service, Urbana, IL 61801, USA
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Agricultural Research Service, Maricopa, AZ, 85138, USA
U.S. Arid-Land Agricultural Research Center, United States Department of Agriculture,
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Financial source:
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Funding for this research was provided by the United States Department of Agriculture (USDA)
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Agriculture Research Service (ARS) and by the Office of Science (BER), US Department of
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Energy, through the Midwestern Center of the National Institute for Climate Change Research
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(NICCR).
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Abstract
Extensive evidence shows that increasing CO2 concentration ([CO2]) stimulates, and
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increasing temperature decreases, both net photosynthetic carbon assimilation (A) and biomass
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production for C3 plants. However the [CO2]-induced stimulation in A is projected to increase
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further with higher temperature. While the influence of increasing temperature and [CO2],
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independent of each other, on A and biomass production have been widely investigated, the
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interaction between these two major global changes have not been tested on field-grown crops.
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Here, the interactive effect of both elevated [CO2] (~585 μmol mol-1) and temperature (+3.5 °C)
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on soybean (Glycine max Merr.) A, biomass, and yield were tested over two growing seasons in
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the Temperature by Free-Air CO2 Enrichment experiment at the Soybean Free Air CO2
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Enrichment facility. Measurements of A, stomatal conductance (gs), and intercellular [CO2] (Ci)
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were collected along with meteorological, water potential, and growth data. Elevated
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temperatures caused lower A, which was largely attributed to declines in gs and Ci and led in turn
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to lower yields. Increasing both [CO2] and temperature stimulated A relative to elevated [CO2]
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alone on only two sampling days during 2009 and on no days in 2011. In 2011, the warmer of
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the two years, there were no observed increases in yield in the elevated temperature plots
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regardless of whether [CO2] was elevated. All treatments lowered the harvest index for soybean,
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although the effect of elevated [CO2] in 2011 was not statistically significant. These results
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provide a better understanding of the physiological responses of soybean to future climate
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change conditions and suggest that the potential is limited for elevated [CO2] to mitigate the
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influence of rising temperatures on photosynthesis, growth, and yields of C3 crops.
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Introduction
The global atmospheric concentration of CO2 ([CO2]) is predicted to rise from current
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concentrations of ~390 μmol mol-1 to between 730 and 1020 μmol mol-1 by 2100 (IPCC, 2007;
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Canadell et al., 2007). An increase of [CO2] is expected to stimulate photosynthesis, as has been
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demonstrated experimentally for a wide range of C3 species (e.g., Curtis & Wang, 1998;
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Bernacchi et al., 2003a; Nowak et al., 2004; Long et al., 2004; Ainsworth & Long, 2005;
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Ainsworth & Rogers, 2007). Increasing [CO2] coupled with the continued accumulation of other
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greenhouses gases (GHG) in the atmosphere is predicted to increase the global average
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temperatures between 2.4 to 6.4°C by the end of the century (A1FI scenario; IPCC, 2007). While
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the thermal optimum (Topt) for photosynthesis ranges between 20°C to 35°C for C3 species (Sage
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et al., 2008), plants have considerable capacity to acclimate to long-term temperature increases
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under current [CO2]. Consequently, the combined changes in the atmospheric composition and
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climate are likely to impart significant effects on terrestrial ecosystems because both CO2 and
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temperature are critical determinants of photosynthetic rates (Sage & Kubien, 2007).
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Soybean, grown in rotation with maize, represents the largest land-use in the United
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States combining to cover an estimated area of 67 million hectares (USDA, 2011). Soybean is
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the fourth most important commodity crop globally with nearly 40% of world production coming
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from the Midwestern US region. As one of the two crops that dominates the Midwestern
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landscape, soybean strongly impacts regional ecosystem services, such as water quality,
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hydrologic cycling and, as a grain legume, soil nitrogen production. Thus, global change-induced
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alterations in soybean production may have large-scale socioeconomic and ecological impacts.
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Effective strategies to adapt agricultural production to global change require improved
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predictions of crop responses to global change scenarios. The Soybean Free Air CO2 Enrichment
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(SoyFACE) research facility was developed to address the molecular, physiological, and growth
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responses of the Midwestern crops soybean and maize to global change through the use of the
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Free Air CO2 Enrichment (FACE) technology (Miglietta et al., 2001). This technology provides
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in-field fumigation of CO2 to simulate future atmospheric conditions while growing crops under
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otherwise natural field conditions using current agronomic practices. Previous results from
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SoyFACE showed that the daily integral of carbon uptake (A’) is increased by ~25% for soybean
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grown under elevated [CO2] (Rogers et al., 2004; Bernacchi et al., 2006). This occurs despite the
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accompanying photosynthetic acclimation most evident as the reduction in the activity and/or
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content of the primary carboxylating enzyme Ribulose-1,5-bisphosphate carboxylase/oxygenase
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(Rubisco) (Bernacchi et al., 2005; Ainsworth & Long, 2005). However, in soybean and other C3
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grain crops, CO2-induced increases in growth and yield are observed to be lower than the
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increase in net photosynthesis (Morgan et al., 2005; Long et al., 2006). In addition to increasing
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carbon uptake (A) of soybean, elevated [CO2] also reduces stomatal conductance (gs) relative to
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plants grown in ambient [CO2] (Ainsworth et al., 2002; Rogers et al., 2004; Bernacchi et al.,
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2006; Bernacchi et al., 2007). This reduction in gs can lead to lower canopy water use, improved
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water use efficiency and conservation of soil moisture (Bernacchi et al., 2007; Leakey et al.,
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2006).
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While FACE experiments have improved our understanding of the plant physiological
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responses to a [CO2] enriched atmosphere, the interactive effects of the two major global change
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factors, rising [CO2] and warming have not been investigated by a direct manipulative
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experiment under field conditions for any crop. It has been shown that the stimulatory effect of
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elevated [CO2] on A is enhanced at higher daily temperatures (Bernacchi et al., 2006), in
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agreement with theory (e.g., Long 1991). However, this analysis was based on the natural
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variation in temperature during15 days over three growing seasons thus confounding the
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correlation with other environmental factors and neglecting long-term acclimation effects to
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higher temperature (Long 1991; Sage & Kubien, 2007). Recent multiple regression analyses of
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historical yield data and growing season temperatures indicate that yields of soybean are
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depressed in warmer years (Lobell & Field, 2007; Kucharik & Serbin, 2008), with a steeper
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decline in yield above, compared with the incline below, a critical temperature (Schlenker &
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Roberts, 2009). It is also predicted that a 0.8°C increase in temperature could increase soybean
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yields in the Midwestern US by ~1.7% based on the mean air temperatures of 22.5°C but
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decrease yields for the warmer conditions in the Southern US (Hatfield et al., 2011). The results
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from this review (Hatfield et al., 2011) suggest that the impact of warming on yield of soybean is
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highly dependent on baseline conditions. Because of the empirical nature of these analyses, the
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mechanisms involved in the decline of soybean productivity above the thermal optimum are
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unclear (Ainsworth & Ort, 2010). Accurately projecting the impact of global change on crop
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productivity relies on understanding how rising [CO2] and increasing temperature together
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influence photosynthesis, growth, phenology, and yield of major crop species.
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The objectives of this study were to quantify and understand the biological processes
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involved in photosynthesis, growth and biomass production for soybean under a warmer and
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CO2-enriched atmosphere. Specifically, we hypothesized that increasing the growing season
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temperature of a soybean canopy by 3.5°C above the current ambient conditions, an increase
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expected midway through this century for terrestrial areas (Rowlands et al., 2012), will result in
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lower photosynthesis, biomass productivity and yields. This is consistent to what has been
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observed historically for warmer years. We further hypothesized that the combination of elevated
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[CO2] and warmer temperatures will yield higher photosynthesis, biomass accumulation and
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yield relative to the elevated [CO2] treatment alone. Given the high interannual variability in
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climate, these hypotheses were tested over two growing seasons; we hypothesized that the
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responses to elevated [CO2], warmer temperature, and the combined treatment would be
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consistent across growing seasons.
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Results
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Meteorological conditions contrasted between the 2009 and 2011 growing seasons
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The mean temperatures for July, August and September were lower in 2009 and higher in
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2011 when compared to the 30-year mean (Table 1). The largest departure from normal in 2009
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was observed in July with temperatures approximately 2.9°C below average. In 2011, July had
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the highest departure with mean temperatures of 2.8°C above average. In both years, April and
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May experienced higher than average precipitation ensuring that both growing seasons began
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with soil moisture near field capacity. The entire 2009 growing season experienced near-average
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precipitation, whereas in 2011 there were significant shortfalls of 60% in July and 47% in
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August compared to the 30-year means for those months (Table 1). Growth stages
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(Supplementary Table 1) and specific meteorological conditions (Fig. 1; Supplementary Table 2)
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associated with each measurement day varied within and between growing seasons.
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Photosynthesis and stomatal conductance varied among CO2, temperature, and
combined treatments.
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Measurements of A were collected throughout the daylight hours on seven (2009) and six
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(2011) days throughout each growing season. The measurements were taken in conditions set to
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mimic the field conditions at the specific time (Supplementary Figs. 1 and 2). Diurnal
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measurements showed variable responses of the key gas exchange parameters A, gs, Ci, and
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iWUE over the course of the two growing seasons (Supplementary Tables 3 and 4). Relative to
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the control, the eC plots yielded higher A, the eT plots lower A and the eT+eC plots higher A
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over most of the time points (Supplementary Figs. 1 and 2).
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The diurnal measurements of A were integrated across the daylight hours to obtain the
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daily integral of photosynthesis (A’). Overall, the effect on A’ of eT and of eC relative to the
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control plots were consistent across both growing seasons, although the increase in eC and the
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decrease in eT was greater in 2011 (Fig. 2). In 2009 there was a statistically significant
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Temperature by CO2 interaction. This interaction is explained by a lack of statistical difference
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between the control and eT plot while the eT+eC plot had much higher A’ relative to the control
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(Tables 2 and 3). In 2009 both eC and eT+eC treatments had significantly higher A’ than the
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ambient [CO2] treatments (i.e., control and eT; Fig. 2; Table 2), although eC and eC+eT were not
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detectably different from each other (Table 3). The responses of A’ among the treatments in 2009
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did not result in statistically significant interactions of main effects with DOY (Table 2;
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Supplementary Table 3).
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In contrast to 2009, in 2011 there were no statistically significant interactive effects of
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temperature and [CO2] on A’ suggesting that the main effects alone were responsible for the
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observed differences. Elevated [CO2] increased A’ within a temperature treatment (eC vs. control
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and eT+eC vs. eT) and elevated temperature decreased A’ within a CO2 treatment (eT vs. control
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and eT+eC vs. eC; Tables 2 and 3; Fig. 2). The CO2 effect, based on percentage change, was
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greater than the temperature effect, thus the combined influence of increasing temperature and
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rising [CO2] stimulated A’ in the eC+eT treatment relative to the control, but the increase was
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lower than the eC vs. control comparison (Table 3, Fig. 2). This response was different from the
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pattern observed in 2009 where A’ in eT+eC showed the highest value although significantly
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different from eC. The effect of temperature varied by DOY in 2011 when temperature did not
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have significant effects on A’ on two measurement dates (DOY 186 and 251; Fig. 2;
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Supplementary Table 4).
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Over both years, elevated [CO2] and warming reduced gs when treatments were applied
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independently and in combination (Fig. 2; Table 2), with the eT+eC treatment showing the
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lowest gs overall for both years (Table 3; Fig. 2). The influence of CO2 relative to temperature,
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however, appears to change from 2009 to 2011. In 2009, elevated [CO2] has a greater impact on
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gs compared with temperature whereas in 2011 temperature has a bigger impact on gs than [CO2]
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(Fig. 2). The impact of elevated temperature and/or [CO2] on gs varied based on DOY for both
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years (Table 2; Supplementary Tables 3 and 4). The [CO2] treatment differences were
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statistically significant on all but one day for each of the years. The temperature-induced
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reduction in gs was statistically significant on four of the seven measurement days for 2009 and
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on all measurement days in 2011 (Fig. 2; Table 3; Supplementary Tables 3 and 4).
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Over both growing seasons, elevated temperatures reduced and elevated [CO2] increased
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Ci relative to the controls (Tables 2 and 3; Fig. 2). While the pattern of responses were similar
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over both growing seasons, the influence of temperature in 2011 was much greater than that
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observed in 2009. Despite a significant temperature by CO2 interaction in 2011, the increase in
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Ci for the eC treatment and the decrease in Ci for the eT treatment appeared to have an additive
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effect on the eT+eC treatment for both years.
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The percent change in A’ within a [CO2] level (eT vs. Control and eT+eC vs. eC) was
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plotted as a function of daily maximum canopy temperature based on the temperatures measured
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in the heated plots (Fig. 3). The percent change in A’ between the eT+eC and eC treatments
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increased with temperature in 2009 and decreased with temperature in 2011 (Fig. 3). The decline
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in A’ for eT+eC relative to eC in 2011 was rapid, and stabilized at daily maximum temperatures
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above 34°C. The eT treatment decreased A’ slightly relative to control in 2009 and remained
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about 20% lower for all daily temperatures in 2011 (Fig. 3).
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The relationship of instantaneous A to gs increased to an asymptote for all treatments (Fig.
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4). While it was difficult to discern differences within a [CO2] treatment (eT vs. Control and
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eT+eC vs. eC), it was clear that for a given gs the elevated [CO2] treatments had much higher A.
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Averaging A and gs within each measurement day for both years to calculate the daily mean and
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seasonal mean intrinsic water use efficiency (iWUE; A/gs) indicated significant differences
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among the treatments (Table 2). For both years, there were statistically significant increases in
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iWUE associated with elevated temperature and with [CO2] treatment (Table 3; Fig. 4). While
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the responses of iWUE were similar for both growing seasons, the CO2 effect was greater in
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2009 than in 2011 and the temperature effect was greater in 2011 than in 2009 (Table 3; Fig. 4).
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For both years it appears that the influence of the two main effects was additive (Table 3; Fig. 4).
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Elevated temperature slightly reduced leaf water potential and increased leaf-to-air
VPD.
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Leaf water potential estimated using thermocouple psychrometry was determined on leaf
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tissue collected at midday of each measurement date. Temperature, regardless of the [CO2], had
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a small but significant effect on total water potential (WP) and turgor pressure (TP) in both years
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(Fig. 5; Table 2). Elevated temperature decreased growing season mean WP by 7% in 2009 and
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by 16% in 2011 (Table 3). While no statistically significant results were observed with osmotic
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potential (OP) for either year; the temperature main effect decreased TP by 17% in 2009 and
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16% in 2011. The seasonal and daily mean values of WP, OP, and TP in 2011 were nearly half
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the values obtained in 2009 (Fig. 5).
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The seasonal mean leaf-to-air vapor pressure deficit (VPD) obtained from the gas
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exchange system during the in situ measurements showed higher values in the warmer (1.58 ±
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0.022 kPa for eT, 1.77 ± 0.023 kPa for eT+eC) relative to the reference (1.27 ± 0.018 kPa for
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control, 1.49 ± 0.020 kPa for eC) temperature plots in 2009. The relative responses in 2011 were
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similar to 2009 with the heated plots showing higher VPD (1.93 ± 0.030 kPa for eT, 2.09 ± 0.033
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kPa for eT+eC) relative to the reference (1.51 ± 0.025 kPa for control, 1.68 ± 0.026 kPa for eC)
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temperature plots. These values gave percentages deviations from control of 24.7% for eT,
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17.6% for eC and 39.6% for eT+eC in 2009; and 28.1% for eT, 11.4% for eC and 38.4% in 2011.
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Elevated CO2 increased biomass and yields but the impact of temperature varied with
growing season.
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Both growing seasons resulted in statistically significant CO2 by temperature interactions
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for above-ground biomass (AGB) indicating that a synergistic effect occurred between these two
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global changes. The treatment responses, however, were not consistent over both growing
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seasons. In 2009 the only two differences among the treatment were between the eT+eC
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comparison with the control plot and the eT+eC comparison with the eT plot (Tables 2 and 3;
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Fig. 6). In 2011 AGB in the eC plots were higher than the control and the eT+eC plots (Tables 2
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and 3; Fig. 6).
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The general responses of seed yield (SY) for both growing seasons were relatively
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similar to the observations of AGB, however, in 2009 the only statistically significant differences
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occurred between the eT+eC and the eT treatment, with the eT treatment showing the lowest and
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the eT+eC treatment the highest SY (Tables 2 and 3; Fig. 6). The impact of temperature had a
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strong negative impact on yields in 2011 with the eT and the eT+eC plots having lower SY
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compared with the both the control and the eC plots (Tables 2 and 3; Fig. 6).
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All treatments appeared to decrease the harvest index (HI) in both years (Fig. 6) however
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in 2011 the only statistically significant differences were between the eC+eT and the control
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(Table 2). Overall, the HI in 2011 was much lower relative to 2009 and the response of HI to the
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various treatments was amplified. In 2011 neither eT nor eC differed from the control plots but
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the eC+eT treatment differed from the control, eT, and eC plots (Table 2). The differences
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between the treatments and the control in 2011 were greater than in 2009, however there was
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also much greater variance in the measurements (Fig. 6).
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Discussion:
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This experiment was designed to test the hypotheses that (1) increasing soybean canopy
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temperature above ambient will result in lower photosynthesis, biomass productivity and yields,
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an effect that is historically characteristic of warmer years; and (2) that concomitant increases in
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[CO2] and temperature will result in higher photosynthesis, biomass production and yields
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compared to elevated [CO2] alone. The results only partially support the first hypothesis.
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Significant differences between the control and eT treatment were observed only for
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photosynthesis (Fig. 2) and SY (Fig. 6) in 2011, the warmer of the two growing seasons. The
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results also indicate that the second hypothesis is not supported. In 2009, the eT+eC treatment
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yielded significantly greater A on only two sampling days relative to the eC treatment and in
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2011 the eT+eC treatment yielded significantly lower photosynthesis than the eC treatment.
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Moreover, in 2011 the response of photosynthesis for the eT+eC treatment, which was slightly
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higher than the control plots, did not translate to increases in SY, rather the eT+eC plot had
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lower SY than any other treatment. The combined eT+eC treatment yielded higher
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photosynthetic rates in both years compared with the eT treatment, suggesting that eC is able to
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at least partially mitigate the negative effects of eT, but this response did not lead to higher SY
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for the eT+eC plot compared with the eT plot in 2011. In 2011 the eT plots, with (eT+eC) or
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without (eT) elevated [CO2] yielded lower SY relative to the control.
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The influence of rising [CO2] on photosynthesis, growth and yield has been well
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documented for soybean (Rogers et al., 2004; Bernacchi et al., 2006) as well as for other species
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(Bernacchi et al., 2003a; Nowak et al., 2004; Long et al., 2004; Ainsworth & Long, 2005;
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Ainsworth & Rogers, 2007). Consistent with previous research on soybean grown at SoyFACE
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(e.g., Leakey et al., 2009), significant increases in photosynthesis in elevated [CO2] were
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observed in both years (Tables 2 and 3). The 2009 growing season was the only time out of ten
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growing seasons at SoyFACE in which increases in SY with elevated [CO2] were absent. One of
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the key benefits of an increase in photosynthesis under elevated [CO2] is the reduction of
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photorespiration (Long, 1991; Long et al., 2004; Ainsworth & Rogers, 2007). The smaller than
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predicted response in 2009 could be attributed to cooler temperatures where the inhibition of
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photosynthesis due to photorespiration was low (Jiao & Grodzinski, 1996). This, coupled with a
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large decrease in gs (Fig. 2) under elevated [CO2] could have contributed to the muted yield
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response in 2009. The 2011 growing season was warmer than typical, thus the ability to suppress
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photorespiration at high [CO2] likely conferred a greater benefit under these conditions. The
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2011 growing season showed higher biomass and yields for the elevated [CO2] grown plants as
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observed for most growing seasons at SoyFACE.
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The heated plots showed consistently reduced photosynthetic carbon uptake for both
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growing seasons relative to the control. It was clear that the increase in temperature had a greater
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effect on reducing photosynthesis in 2011 than in 2009, likely driven by the much warmer
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background temperatures in 2011. This is observed in the seasonal percent deviation of A’ for eT
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vs. Control, which shows a slight decrease in 2009 and a much larger decrease in 2011 (Table 3).
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This is also seen in the percent deviation of A’ versus daily maximum temperature for eT vs.
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Control (Fig. 3). In 2009 as temperature in the heated plots increased, the percent difference of
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A’ between the eT+eC vs. eC plots continued to increase. Contrary to this, the differences
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between the eT vs. control plots declined, indicating greater heat-induced suppression of A’ with
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temperature. In 2011 A’ was consistently lower in the eT treatment relative to the control by
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~20% regardless of daily maximum temperature whereas the stimulation associated with the
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eT+eC plot dropped as temperatures rose (Fig. 3). These results suggest that in 2009
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photosynthesis in the non-heated plots were below the thermal optimum driving photosynthesis
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higher as heat was applied whereas in 2011 photosynthesis for the non-heated plots was
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operating above the thermal optimum such that any further increases in temperatures drove
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photosynthesis down.
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The potential importance of the interaction of elevated [CO2] and increased temperature
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on photosynthesis is well described using mechanistic theory (e.g., Long 1991; Sage & Kubien
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2007) and demonstrated using correlative data collected over many days over different growing
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seasons (e.g., Bernacchi et al., 2006). The results presented here show that under field
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conditions, the importance of the elevated [CO2] and temperature effect on photosynthesis,
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growth and yield is dependent on the extent of heating, on whether the temperature was above or
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below optimum at any particular time, and on the interaction with other environmental factors.
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Of particular importance is the role of changes associated with the underlying biochemistry of
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photosynthesis. Elevated [CO2] is shown to down-regulate the maximum velocity for
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carboxylation (Vc,max) for soybean grown in elevated [CO2], however this acclimation had little
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impact on photosynthetic rates as soybean is not Vc,max limited in elevated [CO2] (Bernacchi et
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al., 2005). Acclimation has been shown to occur in response to higher growth temperature for
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Vcmax and maximum rate of electron transport (Jmax; June et al., 2004; Onoda et al., 2005; Kattge
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and Knorr, 2007). Over the same growing seasons and coupled with the measurements presented
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here, in depth analysis of Vc,max and Jmax for soybean at SoyFACE (Rosenthal et al., submitted)
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shows elevated [CO2]-induced down-regulation of Vc,max consistent with previous reports on
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soybean but not for Jmax. The elevated temperature plots show declines in Jmax, regardless of
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whether [CO2] is increased (Rosenthal et al., submitted).
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To determine whether photosynthesis was predominately Rubisco- or RuBP-regeneration
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limited over each diurnal for all treatments we coupled the results from Rosenthal et al.
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(submitted) for Vc,max and Jmax with the leaf photosynthesis model (Farquhar et al., 1980)
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corrected for temperature (Bernacchi et al., 2001; 2003b). Using this modeled data, we
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determined whether photosynthesis is Rubisco- or RuBP regeneration-limited for all data points
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collected over the two growing seasons. This analysis showed that over 85% of all data points
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were RuBP-limited (Supplemental Figs. 1 and 2). Because Rubisco-limited photosynthesis was
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rare, any down-regulation in Vc,max is likely to not influence A. Given its importance for RuBP
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regeneration limited A, the down-regulation of Jmax is likely to drive down productivity.
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The responses of photosynthesis to elevated [CO2] and warmer temperature over these
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two growing seasons are not likely driven exclusively by the temperature and CO2 sensitivity of
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Rubisco kinetics and RuBP regeneration (e.g., Rosenthal et al., submitted). Previous research at
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SoyFACE showed that elevated [CO2] resulted in ~16% mean reduction in gs (Bernacchi et al.,
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2006), which is substantially less than the reduction observed here (Table 3). Thus, the
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pronounced reduction of gs under elevated [CO2] and/or temperature over both years is likely to
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336
influence the deviation of the observations from theoretical responses. Over two sampling dates
337
in 2009 (DOY 183 and 238) the differences in gs were minimal for the eT+eC vs. eC treatments
338
(Fig. 2). The combined increase in [CO2] and temperature for these two days yielded much
339
higher A’, consistent with the theory presented previously (e.g., Long, 1991). All other
340
measurements days during 2009 yielded gs values that were lower in the eT+eC relative to the eC
341
treatment and did not show differences in A’ between these treatments. The temperature-induced
342
reduction in gs led to lower Ci within a CO2 treatment (Figure 2). The effect of temperature
343
resulted in a much greater decrease for Ci in 2011 than in 2009. In 2011, Ci in the eT+eC
344
treatment was only ca 20% higher than the control despite atmospheric CO2 being ca 50%
345
higher.
346
Despite the reductions in gs, the eT, eC and eT+eC treatments showed a higher iWUE
347
(Fig. 4; Table 3). This increase in iWUE is predicted for plants grown in elevated [CO2] as
348
stomatal limitation to photosynthesis is consistently shown to be lower despite a decrease in gs
349
(e.g., Bernacchi et al., 2005; Rosenthal et al., submitted). The elevated-temperature-grown plants
350
also showed an increase in iWUE across both growing seasons relative to the control. The
351
increase in iWUE for the heated treatments within a [CO2] (eT vs. control and eT+eC vs. eC)
352
was less than that measured within a temperature treatment (eC vs. control and eT+eC vs. eC).
353
The increase associated with the eT treatment relative to the control occurred as a result of the
354
decrease in gs being proportionately greater than the decrease in A’ (Table 3). This indicates that
355
while all treatments experienced a higher iWUE, the mechanisms behind these responses varied
356
among treatments.
357
A characteristic of an experiment that heats the canopy instead of the air will lead to an
358
increase in VPD at the leaf surface, which likely leads to an increase in water use (Kimball,
359
2005; Kimball, 2011; De Boeck et al., 2012). Averaged across time points in which gas
360
exchange measurements were collected, the effect of heating increased the leaf to air vapor
361
pressure deficit by 0.3 kPa in 2009 and 0.4 kPa in 2011 within a CO2 treatment (eT vs. control
362
and eT+eC vs. eC). Both growing seasons experienced significant precipitation during spring,
363
and 2009 had ample precipitation throughout the season (Table 1). Leaf water potential data for
364
both years showed the same responses to temperature, with a general response of temperature,
365
within a CO2 treatment showing more negative WP relative to the non-heated reference plots
366
(Fig. 5; Table 2). The differences in WP, OP and TP in 2011 compared to 2009 indicate that the
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367
variability in climate between the two growing seasons had a dominant influence on leaf water
368
potential relative to the treatment imposed by the infrared heating arrays. Moreover, the pairwise
369
comparison analysis showed no statistical differences among treatments for the WP and TP
370
variables in either year, suggesting that the photosynthetic and productivity values obtained for
371
2011 are representative for the environmental conditions tested and not artificially altered by the
372
experiment. Thus, it is not likely that the additional water use in the heated plots had a
373
substantial effect on growth and physiology during 2009.
374
With the exception of the eC+eT treatment relative to the control in 2011, the responses
375
observed for A’ were similar in responses to those observed for AGB. It is interesting, however,
376
that the response of SY to the various treatments did not follow the responses of A’ and of AGB.
377
In 2009 the AGB was significantly higher in the eT+eC treatments relative to the control but the
378
SY for this treatment did not differ statistically from the control. The statistically significant
379
increase in SY for the eT+eC relative to the eT treatment was the only statistically significant
380
difference in SY in 2009. This suggests that, in this year, the increase in [CO2] offset the losses
381
typically associated with an increase in temperature. In 2011, there were no differences in SY
382
between the eT+eC and the eT treatments which implies that the benefit of both factors together
383
are not universal. In 2011, increases occurred for both AGB and SY in the eC treatment relative
384
to the control but the loss in SY was amplified in relation to the loss in AGB for both heated
385
treatments (Table 3).
386
Within a growing season, increasing temperature appears to reduce yields (Table 3, Fig.
387
6), despite the 13.5% decrease in 2009 not being statistically different from the control (p<0.15).
388
Recent multiple regression analyses of historical yield data and growing season temperatures
389
indicate a negative relationship, meaning that yields of soybean are depressed in warmer years
390
(Lobell & Field 2007; Kucharik & Serbin 2008) a phenomena that is consistent with our
391
findings. A separate analysis, however, suggests that increases in yields with rising temperatures
392
are likely to occur in cooler areas (e.g., Midwestern US) while decreases in yields with
393
temperature are to occur in traditionally warmer areas (e.g., southern US; Hatfield et al., 2011).
394
Our data indicates that additional heating did not confer an advantage to SY, even in a year when
395
background temperatures were much cooler than the long-term mean (2009). A problem with
396
historical trends is that they neglect other confounding factors that cannot be controlled for, such
397
as an interaction with an increase in [CO2]. When the interaction between rising [CO2] and
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398
temperature was considered (e.g., Fig. 6), it was clear that the yield responses were not consistent
399
with the observed photosynthetic responses and that they varied based on growing season
400
conditions. The results from the 2009 growing season suggest that the increased [CO2]
401
completely negated the detriment of increased temperature on yield. The 2011 growing season
402
showed that the addition of [CO2] with higher temperatures did nothing to mitigate the influence
403
of higher temperature. As the conditions associated with 2011 growing season are predicted to
404
become more common (Hayhoe et al., 2010), these results suggest that the assumptions, based on
405
theory that rising [CO2] and increasing temperature could synergistically increase yields, needs
406
to be reassessed.
407
All treatments in 2009 and the elevated temperature treatment in 2011 resulted in
408
decreases in harvest index compared to control. The decline in HI for elevated [CO2] grown
409
soybean are consistent with a number of previous studies on soybean (Amthor et al., 1994;
410
Heagle et al., 1998; Ziska & Bunce, 2000; Morgan et al., 2005). Similarly, the influence of
411
increasing temperatures drive harvest indices for soybean down, with a decrease in seed size
412
being a major factor for this response (Boote et al., 2005). All treatments in 2009 had a smaller
413
percentage decrease on HI compared to the control in 2009 than in 2011 (Fig. 6). This is
414
consistent with previous reports for soybean that show an accelerated decline in HI as
415
temperatures increase (Boote et al., 2005). While higher temperatures were not directly imposed
416
upon the eC treatments in 2011, the CO2-induced closure of gs warmed canopies above the
417
temperatures in the control plots, as reported in previous years (Bernacchi et al., 2007). The
418
measured canopy temperature data used in the heating control system (Supplementary Fig. 4)
419
indicates that season-mean increases in CO2 resulted in ca 1°C warmer canopy temperatures
420
during midday hours. This CO2-induced warming, which was apparent in 2011 but not in 2009,
421
could potentially contribute to the larger decline in HI for the elevated [CO2] treatment relative
422
to the control. There were marked differences in biomass components, leaf physiology, and
423
water potential between the 2009 and 2011 growing seasons. The factors that can influence each
424
of these processes are complex and subjected to a significant number of environmental factors. A
425
full understanding of the drivers behind differences between these two growing seasons would
426
need to account for these factors and require analyses that extend beyond the measurements in
427
this paper.
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428
429
Conclusion
The results from this research show that increased temperatures reduced photosynthesis,
430
growth and yield in soybean. These responses were linked with reductions in gs although
431
biochemical changes to photosynthesis (e.g., Rosenthal et al., submitted) likely also influence
432
these photosynthetic results. Moreover, the combined effects of elevated [CO2] and warmer
433
temperature did not lead to significant increases in photosynthesis compared with an increase in
434
[CO2] alone. In fact, the combined increases in [CO2] and temperature led to reduced
435
photosynthesis relative to elevated [CO2] alone in one of the two years. The contrasting climatic
436
conditions over the two years of measurements played a significant role for the different
437
photosynthetic, growth and yield rates observed. These results suggest that in future climate
438
change conditions the interactive effects of elevated [CO2] and warmer temperatures will likely
439
not benefit soybean physiology, growth and development as predicted from theory due to
440
overriding environmental factors.
441
Materials and methods:
442
Site description and experimental design
443
This experiment was conducted on soybean [Glycine max (L.) Merr., cv. Pioneer 93B15]
444
during the 2009 and 2011 growing seasons, as part of the Temperature by Free Air CO2
445
Enrichment (T-FACE) experiment located within the SoyFACE research facility in Champaign,
446
IL, USA. The entire SoyFACE research farm consists of a 32 ha (80 acres) field in Illinois (40°
447
2' 30.49" N, 88° 13' 58.80 W, 230 m a.s.l.). Characteristics of the site and details of agriculture
448
practices can be found in Ainsworth et al. (2004), Rogers et al. (2004), and Bernacchi et al.
449
(2006). The experiment consisted of a randomized complete block design with four blocks to
450
account for field topographic and soil variation. Each block contained one control and one
451
elevated [CO2] plot; each plot had a diameter of 20 m and they were separated from each other
452
by 100 m as described previously (details in Miglietta et al., 2001). The target concentration of
453
585 μmol mol-1 in 2009 and 590 μmol mol-1 in 2011 for the elevated [CO2] plots was maintained
454
from sunrise to sunset and applied from emergence to harvest. Ambient [CO2] was ~385 μmol
455
mol-1 in 2009 and ~390 μmol mol-1 in 2011. The T-FACE experimental areas consisted of a 3-m-
17
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456
diameter reference and heated plots nested within each of the four 20 m diameter control and
457
elevated [CO2] plots.
458
Each heated plot contained 6 infrared heaters (Salamander Aluminum Extrusion
459
Reflector Assembly Housing for Ceramic Infrared Heaters; Mor Electric Heating Association
460
Inc., Comstock Park, MI, USA) each fitted with four infrared heating elements (Mor-FTE
461
1000W, 240V heaters; Mor Electric Heating Association Inc.). The six heaters were arranged in
462
a 3-m-diameter hexagonal pattern with a total heating area of 7.1 m2 (Supplementary Fig. 3). The
463
heaters were maintained 1.2 m above the canopy, tilted toward the center of the plot at a 45°
464
angle as in Kimball et al. (2008). The heater output was regulated using a custom built industrial
465
dimmer system in which two thyristors (dimmers) were controlled using one circuit board, all of
466
which were taken from one complete dimmer assembly (Model LCED-2484, 240V, 35A; Kalglo
467
Electronics Co., Inc., Bethlehem, PA USA). The dimmer circuit board controlled a range of
468
output up to 24,000W of infrared heating power. The actual 0 to 240V AC output was scaled
469
from a 0-10 V DC input signal to the dimmer. Each heated plot was controlled using a datalogger
470
(CR1000 Micrologger; Campbell Scientific, Inc., Logan, UT USA). The datalogger used a
471
proportional-integrative-derivative (PID) feedback control system, similar to the ones used in
472
Kimball (2005), to maintain a ~3.5°C increase over the ambient temperature 24h/day throughout
473
the growing seasons (Supplementary Fig. 4). The reference and heated canopy temperatures were
474
measured using infrared radiometers (SI-121; Apogee Instruments, Inc., Logan, UT, USA) wired
475
into the datalogger equipped with a voltage output module (SDM-CV04; Campbell Scientific
476
Inc.). Based on the canopy temperature difference between the heated vs. reference plots the
477
voltage output module supplied the 0-10V signal to the dimmer to maintain the target
478
temperature rise of heated plots above the reference plots. The full experiment consisted of four
479
treatments: control (ambient [CO2] & ambient temperature), elevated temperature (ambient
480
[CO2] & +3.5°C in temperature, eT), elevated [CO2] (585 μmol mol-1 [CO2] & ambient
481
temperature, eC), and elevated temperature plus elevated [CO2] (585 μmol mol-1 [CO2] & +3.5°C
482
in temperature, eT+eC)..
483
Meteorological and micrometeorological data
484
Temperature, humidity and solar radiation for the research site were obtained from a
485
meteorological station associated with the Surface Radiation Network (SURFRAD, 40.05N,
486
88.37W, http://www.srrb.noaa.gov/surfrad/index.html), processed as described in Vanloocke et
18
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Copyright © 2013 American Society of Plant Biologists. All rights reserved.
487
al. (2010). Precipitation was obtained from the Willard airport station (40.04N, 88.27W,
488
http://cdo.ncdc.noaa.gov/qclcd/QCLCD). A record for 30-year mean temperature and
489
precipitation for Zone 5 of the Illinois climate divisions (which correspond to Champaign) was
490
obtained from the Midwestern Regional Climate Center (MRCC, http://mrcc.isws.illinois.edu/).
491
Gas exchange measurements and midday sampling
492
Diurnal measurements of instantaneous A and other physiological data, such as Ci and gs
493
were collected using portable open gas-exchange systems with incorporated infrared CO2 and
494
water vapor analyzer (Li-Cor 6400; Li-Cor, Inc., Lincoln, NE, USA) coupled with an integrated
495
chlorophyll fluorometer (LI-6400-40 leaf chamber fluorometer; Li-Cor, Inc.). The infrared CO2
496
and water vapor analyzers were zeroed and the gas exchange systems were calibrated as
497
described in Bernacchi et al. (2006).
498
Gas exchange sampling occurred every two weeks throughout both growing seasons
499
starting with the V3 vegetative developmental stage (i.e., following the emergence of the 3rd
500
trifoliate) and ending with the ~R6 developmental stage (full seed) based on the development
501
classifications of Ritchie et al. (1993). There were a total of seven measurement days in 2009
502
and six in 2011 (Supplementary Table 1). The measurements were taken at 2-hour intervals
503
between 9 am to 5 pm, on 3 plants per plot from the youngest fully expanded leaves. Four
504
research teams each using matched instrumentation conducted measurements at each time point
505
of the diurnal in different blocks to sample all sixteen plots within 45 min. The order of sampling
506
for each team was randomized among blocks. At the beginning of each time point measurement,
507
Photosynthetic Photon Flux Density (PPFD; LI-190; LI-COR, Inc.) and air temperature (HMP-
508
45C; Campbell Scientific, Inc., mounted in aspirated temperature shield model 076B; Met One
509
Instruments, Grants Pall, OR USA) were recorded from sensors located at SoyFACE. The block
510
temperature of the gas exchange systems were set according to ambient air temperature and
511
adjusted to higher temperatures (ambient + 3.5 °C) for the heated plots. The sample RH were
512
between ~50-70%. The [CO2] in the gas exchange system reference chamber was set to
513
concentrations that corresponded to the control (400 μmol mol-1) or elevated (600 μmol mol-1)
514
[CO2] plots. These concentrations, while above the mean concentrations in each plot, allowed for
515
the leaf to draw CO2 down in the sample chambers to closely match plot means and accounted
516
for the difference in the control and elevated [CO2] for 2009 compared to 2011. The values of A,
517
gs and Ci were calculated using the integrated software in the gas exchange system according to
19
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Copyright © 2013 American Society of Plant Biologists. All rights reserved.
518
von Caemmerer & Farquhar (1981). The daily integrated carbon uptake (A’) was calculated from
519
instantaneous A as described in Leakey et al. (2004).
520
Values for maximum carboxylation capacity (Vcmax), maximum linear electron transport
521
through photosystem II (Jmax) and respiration in the light (Rd) at 25°C were obtained from A vs.
522
Ci curves measured within 1-2 days of each diurnal for both growing seasons (Rosenthal et al.,
523
submitted). These parameters were used to model A using the leaf photosynthesis model
524
(Farquhar et al., 1980) to determine which processes, Rubisco or RuBP regeneration, was
525
limiting photosynthesis at each time point for all treatments. The model was corrected for
526
measured leaf temperature using the temperature functions provided previously (Bernacchi et al.
527
2001, 2003b).
528
Percent stimulation of A’ per plot for each day was calculated with the plot mean values
529
for eT vs. Control and for eT+eC vs. eC. The percent stimulation was plotted as a function of the
530
daily maximum temperatures for the heated plot. The values used were from 4 measurement
531
days in 2009 (DOY 197, 210, 224, 238) and 2011 (DOY 200, 214, 228, 242), selected according
532
to similarities in the vapor pressure deficit and solar radiation and adequate canopy cover to
533
prevent the influence of soil in the measurements of canopy temperature (LAI > 2). The intrinsic
534
water use efficiency (iWUE) was calculated with A divided by gs.
535
Samples to determine leaf water potential (WP) were collected during the midday time
536
point on each measurement day with five subsamples taken per plot. Three leaf tissue discs of
537
1.2 cm diameter were excised per plant and sealed in psychrometer chambers (C-30; Wescor,
538
Inc., Logan, UT USA). The chambers were equilibrated in a controlled environmental growth
539
chamber at 25°C as described previously (Leakey et al., 2006). After thermal equilibration, WP
540
was measured using a dew point micro-voltmeter (HR-33T; Wescor) integrated into the
541
psychrometers. Upon measuring WP, the chambers were submerged into liquid nitrogen and the
542
potentials were recorded on the lysed plant tissue to determine osmotic potential (OP). The
543
turgor potential (TP) was calculated as WP–OP. A calibration standard was obtained
544
independently each year using sucrose solutions ranging in concentration from 0 to 1.60 M.
545
Above-ground biomass and yield measurements
546
Above-ground biomass (AGB) was obtained at the end of each growing season after full
547
maturity (growth stage R8) was reached (DOY 267 in 2009 and DOY 298 in 2011). Five 1.5 m
548
rows of soybeans per plot in 2009 and two 1.0 m rows per plot in 2011 were harvested by hand.
20
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Copyright © 2013 American Society of Plant Biologists. All rights reserved.
549
At harvest, plants had few attached leaves, so AGB included only pods and stems. These
550
biomass components are typically used for determining harvest index. Each component was
551
dried to constant weight (~7 days) at 65°C and weighed. The pod tissues were then run through a
552
thresher to isolate the seeds, and the seeds were weighted to obtain seed yield (SY). The harvest
553
index (HI) was calculated by dividing SY by AGB.
554
Statistical analysis
555
Photosynthesis, water potential, and iWUE were analyzed using a complete block
556
repeated measures mixed model analysis of variance (ANOVA) using the PROC MIXED
557
command with the Kenward-Roger method in SAS System 9.3 (SAS Institute, Cary, NC USA).
558
The fixed effects for the seasonal analysis were: day of the year (DOY), [CO2], temperature,
559
temperature by [CO2] interaction and DOY with the interaction of the other fixed effects.
560
Statistical tests of within day differences among the treatments were analyzed separately for each
561
day using time of day, rather than DOY, as the repeated factor in the analysis. The above-ground
562
biomass, yield data and HI were analyzed similarly to the previous variables but without
563
including DOY in the analysis. The differences of least square means from t-tests were used to
564
compare individual treatment means, this option is integrated into the SAS System 9.3. To lower
565
the possibility of a Type II error, the statistical significance was evaluated at alpha ≤ 0.1.
21
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566
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706
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Tables
Table 1.Annual, 6 months (from April to September) and monthly mean temperature (°C) and
precipitation (mm) for a period of 30 years and for 2009 and 2011.
Temperature
(°C)
30-year mean
2009
2011
Precipitation
(mm)
30-year mean
2009
2011
Apr
May
Jun
Jul
Aug
Sep
10.3
9.7
10.6
16.4
16.4
16.3
21.6
22.0
22.3
23.5
20.6
26.3
22.3
20.8
23.1
18.5
18.1
17.0
Apr
May
Jun
Jul
Aug
Sep
92.0
151.9
176.0
106.9
135.9
140.7
98.4
107.2
101.4
113.2
105.7
44.5
99.4
114.1
52.8
68.9
27.9
94.5
710
28
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Copyright © 2013 American Society of Plant Biologists. All rights reserved.
6-month
mean
17.8
16.7
18.2
Annual
mean
10.4
9.9
11.0
6 month
mean
578.9
642.6
609.9
Annual
mean
968.7
1184.4
987.3
Main effects
CO₂
Temp
Temp×CO₂
DOY
DOY×CO₂
DOY×Temp
DOY×Temp×
CO₂
<0.02
<0.001
<0.001
ns
ns
ns
<0.001
<0.02
ns
<0.02
ns
<0.001
<0.001
<0.05
ns
<0.01
<0.001
ns
ns
<0.05
<0.07
<0.01
ns
ns
ns
ns
ns
<0.09
<0.09
ns
<0.001
<0.001
<0.001
<0.001
<0.001
<0.001
<0.001
ns
<0.001
<0.04
ns
ns
ns
<0.03
ns
<0.001
<0.001
ns
ns
ns
<0.001
ns
<0.09
ns
ns
ns
ns
ns
<0.001
<0.02
<0.001
ns
ns
ns
<0.001
<0.09
ns
ns
<0.001
<0.001
<0.001
<0.002
ns
<0.06
<0.001
<0.01
<0.001
<0.04
ns
ns
<0.06
ns
ns
ns
<0.07
<0.1
<0.02
ns
<0.001
<0.001
<0.001
<0.001
<0.001
<0.001
<0.001
<0.06
<0.02
<0.02
<0.005
ns
<0.06
<0.02
<0.01
<0.001
<0.05
ns
ns
ns
<0.06
ns
ns
<0.09
ns
ns
ns
<0.07
2009
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A'
gs
Ci
WP
OP
TP
iWUE
AGB
SY
HI
2011
A'
gs
Ci
WP
OP
TP
iWUE
AGB
SY
HI
―
―
―
―
―
―
―
―
―
―
―
―
―
―
―
―
―
―
―
―
―
―
―
―
Table 2. Seasonal complete block repeated measures analysis of variance for the daily integral of carbon uptake (A’), stomatal
conductance (gs), intercellular [CO2] (Ci), water potential (WP), osmotic potential (OP), turgor pressure (TP), intrinsic water use
efficiency (iWUE), above-ground biomass (AGB), seed yield (SY), and harvest index (HI) for soybean grown in a CO2 by
temperature interaction. The main effects are [CO2] (CO2), temperature (Temp) and day of the year (DOY). The statistically
significant differences (p<0.1) and non-statistical significance (ns) are shown in the table. Main effects not applied are indicated with a
line ( ).
―
29
% Deviation in main
effects
% Deviation
CO₂
Temp
eC vs.
Control
eT vs.
Control
eT+eC
vs.
Control
eT+eC
vs. eT
eT+eC
vs. eC
14.3 *
-31.8 *
41.8 *
2.0
-4.3
8.0
84.4 *
19.7 *
11.7
-6.8*
-0.9
-21.5 *
-5.4 *
-6.7 *
-0.7
-17.3 *
16.8 *
1.8
-1.6
-3.2 *
9.7 *
-34.6 *
43.0 *
1.9
-4.8
16.2 *
84.6 *
7.3
-1.5
-8.1 *
-5.2
-24.4 *
-4.5 *
-6.9
-1.2
-10.0
17.0 *
-9.7
-13.9
-4.7 *
13.0 *
-45.8 *
34.3 *
-4.6
-5.0
-11.1
115.5 *
20.6 *
9.3
-9.7 *
19.2 *
-28.2 *
40.6 *
2.1
-3.7
-1.2
84.2 *
33.5 *
27.0 *
-5.3 *
3.0
-17.1 *
-6.1 *
-6.6
-0.2
-23.5 *
16.7 *
12.5
11.0
-1.7
24.6 *
-25.6 *
44.0 *
3.9
0.4
-2.1
63.8 *
26.0 *
-12.4 *
-37.5 *
-16.6 *
-16.0 *
-3.0
-15.8 *
37.9 *
-24.0 *
-33.5 *
-12.4 *
21.8 *
-25.9 *
45.0 *
5.2
-0.3
3.8
66.1 *
38.2 *
20.5
-13.0
-14.8 *
-37.7 *
-15.9 *
-14.6 *
-3.7
-10.4
39.9 *
-14.5
-20.4 *
-7.2
9.1 *
-53.4 *
20.2 *
-11.4
-2.6
-18.2
126.9 *
-4.4
-32.9 *
-28.9 *
28.0 *
-25.1 *
42.9 *
2.9
1.0
-8.7
62.2 *
11.8
-15.8
-23.4 *
-10.4 *
-37.1 *
-17.2 *
-17.4 *
-2.3
-21.1 *
36.6 *
-30.9 *
-44.3 *
-18.3 *
2009
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A'
gs
Ci
WP
OP
TP
iWUE
AGB
SY
HI
2011
A'
gs
Ci
WP
OP
TP
iWUE
AGB
SY
HI
4.4
-18.0
Table 3. The percentage (%) deviations from control and between treatments are shown, negative values mean a reduction while
positive values mean an increase in the rate of parameters. Statistically significant differences of the pairwise comparisons are
indicated (*).
30
Figure Legends
Figure 1. Meteorological conditions measured during the 2009 and 2011 growing
seasons. The top panels show the daily total solar radiation (black circles) and the daily
precipitation (grey bars) for the 2009 (Panel A) and 2011 (Panel B) growing seasons. The bottom
panels show the vapor pressure deficit (VPD, grey line), the daily mean air temperatures (black
circles) and the maximum and minimum temperatures (top and bottom of the error bars) for the
2009 (Panel C) and 2011 (Panel D) growing seasons. Days in which field sampling occurred are
indicated with triangles.
Figure 2. Daily integral of carbon assimilation (A′; Panels A and B), stomata
conductance (gs; Panels C and D) and intercellular [CO2] (Ci; Panels E and F) for the 2009
(Panels A, C, and E) and 2011 (Panels B, D and F) growing seasons. Each day represents the
daily mean values collected using gas exchange (gs and Ci) and each day A’. Seasonal means for
each variable is also presented at the right of each graph. Error bars represent one SE around the
mean.
Figure 3. Percent deviation of integrated carbon uptake (A’) as a function of daily
maximum canopy temperature for the 2009 (Panel A) and 2011 (Panel B) growing seasons. The
percent stimulation of A’ was calculated with the plot means between the elevated temperature
treatment (eT) compared to control (black points and black line) and between the combined
effect of elevated temperature and [CO2] (eT+eC) compared to elevated [CO2] (eC). Data was
used from measurement days in each year that occurred after canopy closure and before
senescence. The lines reflect second-order polynomials fitted to each comparison.
Figure 4. The relationship between carbon uptake (A) and stomatal conductance (gs) per
treatment for 2009 (Panel A) and 2011 (Panel C). Each point represents the plots means (three
subsamples per plot) for each hourly time point measured across all days within a season for A
vs. gs. The intrinsic water use efficiency (iWUE), calculated as A/gs, for all the measurement
days during 2009 (Panel B) and 2011 (Panel D). Seasonal means for each treatment in both years
are presented at the right of each graph. Bars are as in Fig. 2. Error bars represent one SE around
the mean.
Figure 5. Water potential (WP; Panels A and B), osmotic potential (OP; Panels C and D)
and turgor pressure (TP; Panels E and F) for the days where measurements were done during
31
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2009 (Panels A, C, and E) and 2011 (Panels B, D, and F). Seasonal means of WP, OP and TP for
each treatment in both years are also presented in the right in each graph. Bars are as in Fig. 2.
Error bars represent one SE around the mean.
Figure 6. Means for the above-ground biomass (AGB; Panels A and B), seed yield (SY;
Panels C and D), harvest index (HI; Panels E and F) for 2009 (Panels A, C, and E) and 2011
(Panels B, D, and F). Bars are as in Fig. 2. Error bars represent one SE around the mean.
32
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