Warming puts the squeeze on photosynthesis – lessons from tropical trees

Highlight This article comments on: Slot M, Winter K. 2017. Photosynthetic acclimation to warming in tropical forest tree seedlings. Journal of Experimental Botany 68, 2275–2284.


Thermal acclimation capacity of tropical tree species
While we have considerable data on how temperate species respond to increased growth temperatures, there are only a handful of studies looking at the thermal acclimation capacity of tropical tree species, and this paucity of information impedes our ability to predict how low-latitude forests will respond to a future, warmer world. The new paper by Slot and Winter (2017) provides one of the most comprehensive studies on thermal acclimation of tropical trees to date. They grew seedlings of three common lowland tropical species at 25 °C, 30 °C and 35 °C and assessed how photosynthesis, respiration and growth were affected by the different temperature regimes.
The good news is that all the species acclimated to the warmer temperatures: the thermal optimum of photosynthesis (T opt , the temperature at which carbon uptake is maximized) increased with increasing growth temperature, and respiration rates were lower in plants from warmer treatments (indicating a reduction in carbon losses). But there was also bad news. The shift in T opt was smaller than the shift in growth temperature, net photosynthetic rates at the growth temperature (P growth , the most ecologically relevant measurement of CO 2 uptake) were reduced in plants grown at the warmest temperature, and the photosynthetic capacity of leaves showed little plasticity to growth temperature. Most strikingly, one of the three species (Calophyllum longifolium) grew so poorly at 35 °C that Slot and Winter had to use a 33 °C treatment to provide enough leaves to collect their data. Even under this lower, 'severe' warming treatment, the late-successional C. longifolium showed substantial reductions in photosynthesis compared to seedlings grown at 25 and 30 °C, and also compared to the other species in the study, Ficus insipida and Ochroma pyramidale, which are both early-successional. Overall, the results indicate that while photosynthesis in the study species shows some plasticity to increasing temperatures, acclimation cannot keep pace with warming, and this failure to acclimate successfully may be worse in late-successional species, as also seen in Cheesman and Winter (2013).
High-temperature CO 2 compensation point One of the most interesting parts of the work by Slot and Winter (2017) was their assessment of the high-temperature CO 2 compensation point, the upper leaf temperature at which net CO 2 assimilation rates were zero (T max ; see Box 1). Recent work has explored how thermal acclimation affects photosynthetic traits such as T opt and P growth , Yamori et al., 2014). Also, Yamori et al. (2014) noted that the span of leaf temperatures that realizes 80% of the maximum photosynthetic rate was invariant with growth temperature, implying that the temperature response of net photosynthesis is not narrowed or broadened by warming. However, there is almost nothing known about how T max is affected by changes in growth temperature. In their study, Slot and Winter (2017) found that a 10 °C change in growth temperature had no effect on T max , but T max did vary between species: while T max was 45 °C in C. longifolium (the latesuccessional species with pronounced mortality at 35 °C), T max was 50 °C for both F. insipida and O. pyramidale. The combination of a shift in T opt without a corresponding shift in T max in plants grown at warmer temperatures resulted in a narrowing of the temperature-response curve of photosynthesis.
To further explore the extent to which T max changes in response to an increase in growth temperature, we collated data from 34 published studies (Box 2; Table 1) that reported temperature-response curves of net photosynthesis for plants grown at two or more different thermal regimes. Only papers with measurements that included points of declining net CO 2 assimilation rates above the T opt were used, ensuring a robust estimate of T max . We then estimated T max for both control and warm-grown plants for each reported species using a secondorder polynomial fit to the temperature-response curve of net photosynthesis. Although there is considerable variation in the relationship between the degree of warming and the shift in T max , overall, a 1 °C increase in growth temperature led to a 0.4 °C increase in T max . Unfortunately, there is insufficient data to determine if there are significant differences in the thermal acclimation of T max between plant functional types, but in 25% of the cases assessed, T max actually decreased with increasing growth temperature (Box 2). Based on these findings, the inability of the tropical species investigated in Slot and Winter (2017) to shift their T max is uncommon, and may be related to the high values for T max , which are close to temperatures that can cause irreversible damage to leaves (Krause et al., 2010;.

Perspectives
Although Slot and Winter (2017) provide critical data on how carbon fluxes in tropical species acclimate to warming, there is a pressing need to move beyond gas exchange measurements in these types of studies. Many papers on thermal acclimation measure traits such as leaf nitrogen concentrations and specific leaf area, but future studies should delve more deeply into the biochemical and physiological mechanisms underlying photosynthetic (and respiratory) Box 1. Temperature response of net photosynthesis to increasing growth temperature The solid, blue line represents a cool-grown leaf and the dashed, red line represents a warm-grown leaf. Plants grown at higher temperatures usually exhibit an increased photosynthetic thermal optimum (T opt , shown as a point on each curve), but there is little data on how T max (the upper temperature at which net CO 2 assimilation rates are zero, i.e. carbon gain balances carbon loss) responds to warming. If T opt increases but T max remains constant, as in Slot and Winter (2017), the temperature response of net photosynthesis is 'squeezed' and becomes narrower.
Box 2. Increasing growth temperatures alter the high-temperature CO 2 compensation point Change in T max (∆ T max ) of net CO 2 assimilation rate as a function of the increase in growth temperature (∆ T growth ) in plant species from four plant functional types (see key). Each point plotted represents a comparison between cool and warm-grown plants from a single study (Table 1). The dotted line shows the regression for all data taken together (y=-1.29 + 0.40x; r 2 =0.13; P=0.0002).
acclimation. Recent studies in tropical tree species have highlighted the importance of within-leaf N allocation as a strong determinant of variation in photosynthetic capacity (Coste et al., 2005;Dusenge et al., 2015). Specifically, Scafaro et al. (2016) demonstrated that accounting for changes in N allocation to the CO 2 -fixing enzyme Rubisco in response to growth temperature explained the measured variation in photosynthetic capacity in a range of temperate and tropical species. Shifts in N allocation between the Calvin cycle and electron transport may represent a major theme for thermal acclimation of carbon gain (Hikosaka et al., 2006), but we still lack a predictive model of photosynthetic acclimation to temperature that could explain the variation we see between plant functional types (as described in Yamori et al., 2014, and. While this is not a problem unique to tropical systems, building such a model will require a much more extensive understanding of how changes in temperature affect photosynthesis in a broad range of species and ecosystems. This represents a significant challenge, but it would be an important step forward for predicting future carbon fluxes in vegetation.