Thermal limits of leaf metabolism across biomes

Abstract

High-temperature tolerance in plants is important in a warming world, with extreme heat waves predicted to increase in frequency and duration, potentially leading to lethal heating of leaves. Global patterns of high-temperature tolerance are documented in animals, but generally not in plants, limiting our ability to assess risks associated with climate warming. To assess whether there are global patterns in high-temperature tolerance of leaf metabolism, we quantified T (high temperature where minimal chlorophyll a fluorescence rises rapidly and thus photosystem II is disrupted) and T (temperature where leaf respiration in darkness is maximal, beyond which respiratory function rapidly declines) in upper canopy leaves of 218 plant species spanning seven biomes. Mean site-based T values ranged from 41.5 °C in the Alaskan arctic to 50.8 °C in lowland tropical rainforests of Peruvian Amazon. For T , the equivalent values were 51.0 and 60.6 °C in the Arctic and Amazon, respectively. T and T followed similar biogeographic patterns, increasing linearly (˜8 °C) from polar to equatorial regions. Such increases in high-temperature tolerance are much less than expected based on the 20 °C span in high-temperature extremes across the globe. Moreover, with only modest high-temperature tolerance despite high summer temperature extremes, species in mid-latitude (~20-50°) regions have the narrowest thermal safety margins in upper canopy leaves; these regions are at the greatest risk of damage due to extreme heat-wave events, especially under conditions when leaf temperatures are further elevated by a lack of transpirational cooling. Using predicted heat-wave events for 2050 and accounting for possible thermal acclimation of T and T , we also found that these safety margins could shrink in a warmer world, as rising temperatures are likely to exceed thermal tolerance limits. Thus, increasing numbers of species in many biomes may be at risk as heat-wave events become more severe with climate change.

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

“…Ghouil et al () showed that Quercus suber seedlings subjected to a range of growth temperatures (10 to 40 °C) in a growth cabinet exhibited acclimation of P HT , with T crit acclimating approximately 0.3 °C per °C increase in growth temperature (Ghouil et al, ). More recently, O'Sullivan et al () reported seasonal variations in T crit at two sites (temperate woodland and a tropical rainforest) in Australia (three species at each site) consistent with thermal acclimation patterns, with the seasonal adjustments being similar to the biome‐to‐biome patterns of T crit values measured in summer at each site. Similar results were recently reported by Sastry and Barua () assessing seasonal variations in P HT at a dry tropical forest in India.…”

“…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.…”

“…Australia is noted for its unique flora and range of contrasting thermal and water‐supply environments (e.g., wet forests in tropical and temperate regions through to inland, arid, and semiarid woodlands); it is also experiencing rising air temperatures (CSIRO & Bureau of Meterology, ; Perkins & Alexander, ) and longer duration and severity of heatwaves (Cowan et al, ; Lewis & King, ; Steffen, ). By measuring T crit values at several field sites across Australia in two seasons (with a range of mean daily temperatures of 6.6 to 30.2 °C), and by growing plants in three different temperatures under controlled conditions, our study tested the following hypotheses: Photosynthetic heat tolerance ( P HT ) quantified as T crit : (a) varies seasonally in the field across biomes, being higher in summer than winter, (b) acclimates to sustained changes in growth temperature under controlled environment conditions; T crit values are inherently higher in species adapted to hot/dry environments than their cool/moist‐adapted counterparts, with inherent differences and acclimation of T crit both contributing to reported biogeographic patterns in P HT (O'Sullivan et al, ); Variations in T crit are associated with variations in leaf lipid physical properties, with hot‐adapted and/or warm‐acclimated plants exhibiting higher saturation level of FAs than their cool‐adapted/cool‐acclimated counterparts. …”

Photosynthetic acclimation to warming in tropical forest tree seedlings

“…Krause et al , 2010, 2013), and as such these T Max values are likely to reflect absolute thermal limits. O’Sullivan et al (2017) recently showed that the maximum temperature of PSII integrity was higher in the tropics (50.8 °C) than in high latitudes (41.5 °C in Alaska), but so far there is no experimental confirmation that high growth temperature can increase heat tolerance markedly above ~51 °C (Krause et al , 2013), with the exception of CAM succulents (Krause et al , 2016). …”

Relationships between climate of origin and photosynthetic responses to an episodic heatwave depend on growth CO2 concentration for Eucalyptus camaldulensis var. camaldulensis

“…during or following exposure to high temperature events Ball 1996a, 1996b), which can be driven, in some cases, by intraspecific variation within species (Drake et al 2015) or by environmental variation across species collection sites (Lewis et al 2011). The effects of eCO 2 on the heat or high-temperature stress tolerance of plants can act on several sites or processes within cells (Weis and Berry 1988;Murata et al 2007), which may help determine major distribution patterns (Osmond et al 1987;O'Sullivan et al 2017). Changes in A in response to eCO 2 can be related to membrane fatty acid saturation (Gombos et al 1994) or the activity of Rubisco (Law and Crafts-Brandner 1999;Salvucci and Crafts-Brandner 2004).…”