A comparative analysis of photosynthetic recovery from thermal stress: a desert plant case study

Abstract

Our understanding of the effects of heat stress on plant photosynthesis has progressed rapidly in recent years through the use of chlorophyll a fluorescence techniques. These methods frequently involve the treatment of leaves for several hours in dark conditions to estimate declines in maximum quantum yield of photsystem II (F(V)/F(M)), rarely accounting for the recovery of effective quantum yield (ΔF/F(M')) after thermally induced damage occurs. Exposure to high temperature extremes, however, can occur over minutes, rather than hours, and recent studies suggest that light influences damage recovery. Also, the current focus on agriculturally important crops may lead to assumptions about average stress responses and a poor understanding about the variation among species' thermal tolerance. We present a chlorophyll a fluorescence protocol incorporating subsaturating light to address whether species' thermal tolerance thresholds (T 50) are related to the ability to recover from short-term heat stress in 41 Australian desert species. We found that damage incurred by 15-min thermal stress events was most strongly negatively correlated with the capacity of species to recover after a stress event of 50 °C in summer. Phylogenetically independent contrast analyses revealed that basal divergences partially explain this relationship. Although T 50 and recovery capacity were positively correlated, the relationship was weaker for species with high T 50 values (>51 °C). Results highlight that, even within a single desert biome, species vary widely in their physiological response to high temperature stress and recovery metrics provide more comprehensive information than damage metrics alone.

Trees tolerate an extreme heatwave via sustained transpirational cooling and increased leaf thermal tolerance

“…T 50 was derived using a Weibull function fit to the F v / F m using the “fitplc” r package; tree‐level estimates of T 50 were obtained by fitting this function to the final overnight data collected for each tree on each date. As described previously for a range of plants (Curtis et al., ), the initial and overnight F v / F m values of leaf discs exposed to the 24°C control treatment were equivalently high (~0.8), indicating that there were no methodological artifacts related to sample handling.…”

“…Leaves rapidly increased their high‐temperature tolerance in response to the heatwave. The high‐temperature threshold of photosynthetic integrity (Curtis et al., ; T 50 ) was high (~48.5°C) across all treatments prior to the heatwave (minimum p > .1), including trees designated for the control and heatwave treatment (Tukey post hoc test; p > .1). This is consistent with a large thermal safety margin (O'Sullivan et al., ).…”

“…We used a measurement of the high-temperature thermal threshold of photosystem II integrity (T 50 ) as an index of leaf thermal tolerance. We measured T 50 with an established laboratory protocol (Curtis, Knight, Petrou, & Leigh, 2014) based on the ratio of darkadapted variable fluorescence relative to maximal fluorescence (F v / F m ). T 50 is the temperature at which dark-adapted F v /F m declines to 50% of its healthy unstressed value (Curtis et al, 2014).…”

Plasticity of photosynthetic heat tolerance in plants adapted to thermally contrasting biomes

“…Under these heatwave and drought conditions, where adaptive and acclimation dependent changes would be expected to maximize heat tolerance, T crit rarely exceeded 55 °C, with most species exhibiting maximum T crit values near 50 °C. Two other studies on Australian desert plant species during summer (Curtis et al, ; Curtis et al, ) also found the highest thermal tolerance indicated by T 50 of photosynthetic efficiency (50% decline in the maximum quantum yield of PSII of dark‐adapted leaves)—was below 55 °C. Similar results were also reported in studies of 35 desert species of P HT in the USA (Downton et al, ) and 24 savanna woody species in China (Zhang et al, ).…”

“…Quantification of the temperature response of F o (i.e., F o ‐T curves)—or similar methods that assess PSII functionality (e.g., temperature dependence of the maximum quantum yield of PSII of dark‐adapted leaves)—therefore provides insights into the heat sensitivity of PSII (Bilger, Schreiber, & Lange, ; Curtis, Gollan, Murray, & Leigh, ; Curtis, Knight, Petrou, & Leigh, ; Krause et al, ; Krause & Weis, ; Krause, Winter, Krause, & Virgo, ; Schreiber & Berry, ; Schreiber, Colbow, & Vidaver, ; Zhang, Poorter, Hao, & Cao, ). Using such approaches, advances have been made in our understanding of the physiological mechanisms (Hüve, Bichele, Rasulov, & Niinemets, ; Hüve, Bichele, Tobias, & Niinemets, ; Yamane, Kashino, Koike, & Satoh, ), broader ecological patterns, and significance of photosynthetic heat tolerance ( P HT ) (Curtis et al, ; Downton, Berry, & Seemann, ; Ghouil et al, ; Knight & Ackerly, ; Knight & Ackerly, ; Knight & Ackerly, ; Krause et al, ; O'Sullivan et al, ; Seemann, Downton, & Berry, ; Zhang et al, ). What is less clear, however, is the extent to which there are inherent differences in P HT among species adapted to contrasting habitats.…”