Strong acclimation effect of temperature and humidity on heat tolerance of the Arctic collembolan Megaphorura arctica.

The Arctic is a highly variable environment in which extreme daily and seasonal temperature fluctuations can occur. With climate change, an increase in the occurrence of extreme high temperatures and drought events is expected. While the effects of cold and dehydration stress on polar arthropods are well studied in combination, little is known about how these species respond to the combined effects of heat and dehydration stress. In this paper, we investigated how the heat tolerance of the Arctic collembola Megaphorura arctica is affected by combinations of different temperature and humidity acclimation regimes under controlled laboratory conditions. The effect of acclimation temperature was complex and highly dependent on both acclimation time and temperature, and was found to have a positive, negative or no effect depending on experimental conditions. Further, we found marked effects of the interaction between temperature and humidity on heat tolerance, with lower humidity severely decreasing heat tolerance when the acclimation temperature was increased. This effect was more pronounced with increasing acclimation time. Lastly, the effect of acclimation on heat tolerance under a fluctuating temperature regime was dependent on acclimation temperature and time, as well as humidity levels. Together, these results show that thermal acclimation alone has moderate or no effect on heat tolerance, but that drought events, likely to be more frequent in the future, in combination with high temperature stress can have large negative impacts on heat tolerance of some Arctic arthropods.

The temperature sensor TWA1 is required for thermotolerance in Arabidopsis.

Plants exposed to incidences of excessive temperatures activate heat-stress responses to cope with the physiological challenge and stimulate long-term acclimation1,2. The mechanism that senses cellular temperature for inducing thermotolerance is still unclear3. Here we show that TWA1 is a temperature-sensing transcriptional co-regulator that is needed for basal and acquired thermotolerance in Arabidopsis thaliana. At elevated temperatures, TWA1 changes its conformation and allows physical interaction with JASMONATE-ASSOCIATED MYC-LIKE (JAM) transcription factors and TOPLESS (TPL) and TOPLESS-RELATED (TPR) proteins for repressor complex assembly. TWA1 is a predicted intrinsically disordered protein that has a key thermosensory role functioning through an amino-terminal highly variable region. At elevated temperatures, TWA1 accumulates in nuclear subdomains, and physical interactions with JAM2 and TPL appear to be restricted to these nuclear subdomains. The transcriptional upregulation of the heat shock transcription factor A2 (HSFA2) and heat shock proteins depended on TWA1, and TWA1 orthologues provided different temperature thresholds, consistent with the sensor function in early signalling of heat stress. The identification of the plant thermosensors offers a molecular tool for adjusting thermal acclimation responses of crops by breeding and biotechnology, and a sensitive temperature switch for thermogenetics.

Pollen thermotolerance of a widespread plant, Lotus corniculatus, in response to climate warming: possible local adaptation of populations from different elevations.

One of the most vulnerable phases in the plant life cycle is sexual reproduction, which depends on effective pollen transfer, but also on the thermotolerance of pollen grains. Pollen thermotolerance is temperature-dependent and may be reduced by increasing temperature associated with global warming. A growing body of research has focused on the effect of increased temperature on pollen thermotolerance in crops to understand the possible impact of temperature extremes on yield. Yet, little is known about the effects of temperature on pollen thermotolerance of wild plant species. To fill this gap, we selected Lotus corniculatus s.l. (Fabaceae), a species common to many European habitats and conducted laboratory experiments to test its pollen thermotolerance in response to artificial increase in temperature. To test for possible local adaptation of pollen thermal tolerance, we compared data from six lowland (389-451 m a.s.l.) and six highland (841-1,030 m a.s.l.) populations. We observed pollen germination in vitro at 15 °C, 25 °C, 30 °C, and 40 °C. While lowland plants maintained a stable germination percentage across a broad temperature range (15-30 °C) and exhibited reduced germination only at extremely high temperatures (40 °C), highland plants experienced reduced germination even at 30 °C-temperatures commonly exceeded in lowlands during warm summers. This suggests that lowland populations of L. corniculatus may be locally adapted to higher temperature for pollen germination. On the other hand, pollen tube length decreased with increasing temperature in a similar way in lowland and highland plants. The overall average pollen germination percentage significantly differed between lowland and highland populations, with highland populations displaying higher germination percentage. On the other hand, the average pollen tube length was slightly smaller in highland populations. In conclusion, we found that pollen thermotolerance of L. corniculatus is reduced at high temperature and that the germination of pollen from plant populations growing at higher elevations is more sensitive to increased temperature, which suggests possible local adaptation of pollen thermotolerance.

Multi-scale analysis of heat stress acclimation in Arabidopsis seedlings highlights the primordial contribution of energy-transducing organelles.

Much progress has been made in understanding the molecular mechanisms of plant adaptation to heat stress. However, the great diversity of models and stress conditions, and the fact that analyses are often limited to a small number of approaches, complicate the picture. We took advantage of a liquid culture system in which Arabidopsis seedlings are arrested in their development, thus avoiding interference with development and drought stress responses, to investigate through an integrative approach seedlings' global response to heat stress and acclimation. Seedlings perfectly tolerate a noxious heat shock (43°C) when subjected to a heat priming treatment at a lower temperature (38°C) the day before, displaying a thermotolerance comparable to that previously observed for Arabidopsis. A major effect of the pre-treatment was to partially protect energy metabolism under heat shock and favor its subsequent rapid recovery, which was correlated with the survival of seedlings. Rapid recovery of actin cytoskeleton and mitochondrial dynamics were another landmark of heat shock tolerance. The omics confirmed the role of the ubiquitous heat shock response actors but also revealed specific or overlapping responses to priming, heat shock, and their combination. Since only a few components or functions of chloroplast and mitochondria were highlighted in these analyses, the preservation and rapid recovery of their bioenergetic roles upon acute heat stress do not require extensive remodeling of the organelles. Protection of these organelles is rather integrated into the overall heat shock response, thus allowing them to provide the energy required to elaborate other cellular responses toward acclimation.

Evolution of avian heat tolerance: The role of atmospheric humidity.

The role of atmospheric humidity in the evolution of endotherms' thermoregulatory performance remains largely unexplored, despite the fact that elevated humidity is known to impede evaporative cooling capacity. Using a phylogenetically informed comparative framework, we tested the hypothesis that pronounced hyperthermia tolerance among birds occupying humid lowlands evolved to reduce the impact of humidity-impeded scope for evaporative heat dissipation by comparing heat tolerance limits (HTLs; maximum tolerable air temperature), maximum body temperatures (Tbmax), and associated thermoregulatory variables in humid (19.2 g H2O m-3) versus dry (1.1 g H2O m-3) air among 30 species from three climatically distinct sites (arid, mesic montane, and humid lowland). Humidity-associated decreases in evaporative water loss and resting metabolic rate were 27%-38% and 21%-27%, respectively, and did not differ significantly between sites. Decreases in HTLs were significantly larger among arid-zone (mean ± SD = 3.13 ± 1.12°C) and montane species (2.44 ± 1.0°C) compared to lowland species (1.23 ± 1.34°C), with more pronounced hyperthermia among lowland (Tbmax = 46.26 ± 0.48°C) and montane birds (Tbmax = 46.19 ± 0.92°C) compared to arid-zone species (45.23 ± 0.24°C). Our findings reveal a functional link between facultative hyperthermia and humidity-related constraints on evaporative cooling, providing novel insights into how hygric and thermal environments interact to constrain avian performance during hot weather. Moreover, the macrophysiological patterns we report provide further support for the concept of a continuum from thermal specialization to thermal generalization among endotherms, with adaptive variation in body temperature correlated with prevailing climatic conditions.

Application of the thermal death time model in predicting thermal damage accumulation in plants.

The thermal death time (TDT) model suggests that the duration for which an organism can tolerate thermal stress decreases exponentially as the intensity of the temperature becomes more extreme. This model has been used to predict damage accumulation in ectothermic animals and plants under fluctuating thermal conditions. However, the critical assumption of the TDT model, which is additive damage accumulation, remains unverified for plants. We assessed thermal damage in Thymus vulgaris under different heat and cold treatments, and used TDT models to predict time to thermal failure of PSII. Additionally, thermal tolerance estimates from previous studies were used to create TDT models to assess the applicability of this framework in plants. We show that thermal damage is additive between 44 °C and 47 °C and between -6.5 °C and -8 °C, and that the TDT model can predict damage accumulation at both temperature extremes. Data from previous studies indicate a broad applicability of this approach across plant species and traits. The TDT framework reveals a thermal tolerance landscape describing the relationship between exposure duration, stress intensity, and percentage damage accumulation. The extreme thermal sensitivity of plants emphasizes that even a 1 °C increase in future extreme temperatures could impact their mortality and distribution.

Glucose-G protein signaling plays a crucial role in tomato resilience to high temperature and elevated CO2.

Global climate change is accompanied by carbon dioxide (CO2) enrichment and high temperature (HT) stress; however, how plants adapt to the combined environments and the underlying mechanisms remain largely unclear. In this study, we show that elevated CO2 alleviated plant sensitivity to HT stress, with significantly increased apoplastic glucose (Glc) levels in tomato (Solanum lycopersicum) leaves. Exogenous Glc treatment enhanced tomato resilience to HT stress under ambient CO2 conditions. Cell-based biolayer interferometry, subcellular localization, and Split-luciferase assays revealed that Glc bound to the tomato regulator of G protein signaling 1 (RGS1) and induced RGS1 endocytosis and thereby RGS1-G protein α subunit (GPA1) dissociation in a concentration-dependent manner. Using rgs1 and gpa1 mutants, we found that RGS1 negatively regulated thermotolerance and was required for elevated CO2-Glc-induced thermotolerance. GPA1 positively regulated the elevated CO2-Glc-induced thermotolerance. A combined transcriptome and chlorophyll fluorescence parameter analysis further revealed that GPA1 integrated photosynthesis- and photoprotection-related mechanisms to regulate thermotolerance. These results demonstrate that Glc-RGS1-GPA1 signaling plays a crucial role in the elevated CO2-induced thermotolerance in tomato. This information enhances our understanding of the Glc-G protein signaling function in stress resilience in response to global climate change and will be helpful for genetic engineering approaches to improve plant resilience.

Are tropical forests approaching critical temperature thresholds?

There is growing concern about the fate of tropical forests in the face of rising global temperatures. Doughty et al. (2023) suggest that an increase in air temperature beyond ∼4 °C will result in massive death of tropical forest leaves and potentially tree death. However, this prediction relies on assumptions that likely underestimate the heat tolerance of tropical leaves.

Variation in leaf carbon economics, energy balance, and heat tolerance traits highlights differing timescales of adaptation and acclimation.

Multivariate leaf trait correlations are hypothesized to originate from natural selection on carbon economics traits that control lifetime leaf carbon gain, and energy balance traits governing leaf temperatures, physiological rates, and heat injury. However, it is unclear whether macroevolution of leaf traits primarily reflects selection for lifetime carbon gain or energy balance, and whether photosynthetic heat tolerance is coordinated along these axes. To evaluate these hypotheses, we measured carbon economics, energy balance, and photosynthetic heat tolerance traits for 177 species (157 families) in a common garden that minimizes co-variation of taxa and climate. We observed wide variation in carbon economics, energy balance, and heat tolerance traits. Carbon economics and energy balance (but not heat tolerance) traits were phylogenetically structured, suggesting macroevolution of leaf mass per area and leaf dry matter content reflects selection on carbon gain rather than energy balance. Carbon economics and energy balance traits varied along a common axis orthogonal to heat tolerance traits. Our results highlight a fundamental mismatch in the timescales over which morphological and heat tolerance traits respond to environmental variation. Whereas carbon economics and energy balance traits are constrained by species' evolutionary histories, photosynthetic heat tolerance traits are not and can acclimate readily to leaf microclimates.

Transcription factor CaHDZ15 promotes pepper basal thermotolerance by activating HEAT SHOCK FACTORA6a.

High temperature stress (HTS) is a serious threat to plant growth and development and to crop production in the context of global warming, and plant response to HTS is largely regulated at the transcriptional level by the actions of various transcription factors (TFs). However, whether and how homeodomain-leucine zipper (HD-Zip) TFs are involved in thermotolerance are unclear. Herein, we functionally characterized a pepper (Capsicum annuum) HD-Zip I TF CaHDZ15. CaHDZ15 expression was upregulated by HTS and abscisic acid in basal thermotolerance via loss- and gain-of-function assays by virus-induced gene silencing in pepper and overexpression in Nicotiana benthamiana plants. CaHDZ15 acted positively in pepper basal thermotolerance by directly targeting and activating HEAT SHOCK FACTORA6a (HSFA6a), which further activated CaHSFA2. In addition, CaHDZ15 interacted with HEAT SHOCK PROTEIN 70-2 (CaHsp70-2) and glyceraldehyde-3-phosphate dehydrogenase1 (CaGAPC1), both of which positively affected pepper thermotolerance. CaHsp70-2 and CaGAPC1 promoted CaHDZ15 binding to the promoter of CaHSFA6a, thus enhancing its transcription. Furthermore, CaHDZ15 and CaGAPC1 were protected from 26S proteasome-mediated degradation by CaHsp70-2 via physical interaction. These results collectively indicate that CaHDZ15, modulated by the interacting partners CaGAPC1 and CaHsp70-2, promotes basal thermotolerance by directly activating the transcript of CaHSFA6a. Thus, a molecular linkage is established among CaHsp70-2, CaGAPC1, and CaHDZ15 to transcriptionally modulate CaHSFA6a in pepper thermotolerance.

The Heat Shock Transcription Factor HsfA Plays a Role in Membrane Lipids Biosynthesis Connecting Thermotolerance and Unsaturated Fatty Acid Metabolism in Aspergillus fumigatus.

Thermotolerance is a remarkable virulence attribute of Aspergillus fumigatus, but the consequences of heat shock (HS) to the cell membrane of this fungus are unknown, although this structure is one of the first to detect changes in ambient temperature that imposes on the cell a prompt adaptative response. Under high-temperature stress, fungi trigger the HS response controlled by heat shock transcription factors, such as HsfA, which regulates the expression of heat shock proteins. In yeast, smaller amounts of phospholipids with unsaturated fatty acid (FA) chains are synthesized in response to HS, directly affecting plasma membrane composition. The addition of double bonds in saturated FA is catalyzed by Δ9-fatty acid desaturases, whose expression is temperature-modulated. However, the relationship between HS and saturated/unsaturated FA balance in membrane lipids of A. fumigatus in response to HS has not been investigated. Here, we found that HsfA responds to plasma membrane stress and has a role in sphingolipid and phospholipid unsaturated biosynthesis. In addition, we studied the A. fumigatus Δ9-fatty acid desaturase sdeA and discovered that this gene is essential and required for unsaturated FA biosynthesis, although it did not directly affect the total levels of phospholipids and sphingolipids. sdeA depletion significantly sensitizes mature A. fumigatus biofilms to caspofungin. Also, we demonstrate that hsfA controls sdeA expression, while SdeA and Hsp90 physically interact. Our results suggest that HsfA is required for the adaptation of the fungal plasma membrane to HS and point out a sharp relationship between thermotolerance and FA metabolism in A. fumigatus. IMPORTANCE Aspergillus fumigatus causes invasive pulmonary aspergillosis, a life-threatening infection accounting for high mortality rates in immunocompromised patients. The ability of this organism to grow at elevated temperatures is long recognized as an essential attribute for this mold to cause disease. A. fumigatus responds to heat stress by activating heat shock transcription factors and chaperones to orchestrate cellular responses that protect the fungus against damage caused by heat. Concomitantly, the cell membrane must adapt to heat and maintain physical and chemical properties such as the balance between saturated/unsaturated fatty acids. However, how A. fumigatus connects these two physiological responses is unclear. Here, we explain that HsfA affects the synthesis of complex membrane lipids such as phospholipids and sphingolipids and controls the enzyme SdeA, which produces monounsaturated fatty acids, raw material for membrane lipids. These findings suggest that forced dysregulation of saturated/unsaturated fatty acid balance might represent novel strategies for antifungal therapy.

Brain dysfunction during warming is linked to oxygen limitation in larval zebrafish.

Understanding the physiological mechanisms that limit animal thermal tolerance is crucial in predicting how animals will respond to increasingly severe heat waves. Despite their importance for understanding climate change impacts, these mechanisms underlying the upper thermal tolerance limits of animals are largely unknown. It has been hypothesized that the upper thermal tolerance in fish is limited by the thermal tolerance of the brain and is ultimately caused by a global brain depolarization. In this study, we developed methods for measuring the upper thermal limit (CTmax) in larval zebrafish (Danio rerio) with simultaneous recordings of brain activity using GCaMP6s calcium imaging in both free-swimming and agar-embedded fish. We discovered that during warming, CTmax precedes, and is therefore not caused by, a global brain depolarization. Instead, the CTmax coincides with a decline in spontaneous neural activity and a loss of neural response to visual stimuli. By manipulating water oxygen levels both up and down, we found that oxygen availability during heating affects locomotor-related neural activity, the neural response to visual stimuli, and CTmax. Our results suggest that the mechanism limiting the upper thermal tolerance in zebrafish larvae is insufficient oxygen availability causing impaired brain function.

The effect of thermal microenvironment in upper thermal tolerance plasticity in tropical tadpoles. Implications for vulnerability to climate warming.

Current climate change is generating accelerated increase in extreme heat events and organismal plastic adjustments in upper thermal tolerances, (critical thermal maximum -CTmax ) are recognized as the quicker mitigating mechanisms. However, current research casts doubt on the actual mitigating role of thermal acclimation to face heat impacts, due to its low magnitude and weak environmental signal. Here, we examined these drawbacks by first estimating maximum extent of thermal acclimation by examining known sources of variation affecting CTmax expression, such as daily thermal fluctuation and heating rates. Second, we examined whether the magnitude and pattern of CTmax plasticity is dependent of the thermal environment by comparing the acclimation responses of six species of tropical amphibian tadpoles inhabiting thermally contrasting open and shade habitats and, finally, estimating their warming tolerances (WT = CTmax - maximum temperatures) as estimator of heating risk. We found that plastic CTmax responses are improved in tadpoles exposed to fluctuating daily regimens. Slow heating rates implying longer duration assays determined a contrasting pattern in CTmax plastic expression, depending on species environment. Shade habitat species suffer a decline in CTmax whereas open habitat tadpoles greatly increase it, suggesting an adaptive differential ability of hot exposed species to quick hardening adjustments. Open habitat tadpoles although overall acclimate more than shade habitat species, cannot capitalize this beneficial increase in CTmax, because the maximum ambient temperatures are very close to their critical limits, and this increase may not be large enough to reduce acute heat stress under the ongoing global warming.

Reduced physiological plasticity in a fish adapted to stable temperatures.

Plasticity can allow organisms to maintain consistent performance across a wide range of environmental conditions. However, it remains largely unknown how costly plasticity is and whether a trade-off exists between plasticity and performance under optimal conditions. Biological rates generally increase with temperature, and to counter that effect, fish use physiological plasticity to adjust their biochemical and physiological functions. Zebrafish in the wild encounter large daily and seasonal temperature fluctuations, suggesting they should display high physiological plasticity. Conversely, laboratory zebrafish have been at optimal temperatures with low thermal fluctuations for over 150 generations. We treated this domestication as an evolution experiment and asked whether this has reduced the physiological plasticity of laboratory fish compared to their wild counterparts. We measured a diverse range of phenotypic traits, from gene expression through physiology to behavior, in wild and laboratory zebrafish acclimated to 15 temperatures from 10 °C to 38 °C. We show that adaptation to the laboratory environment has had major effects on all levels of biology. Laboratory fish show reduced plasticity and are thus less able to counter the direct effects of temperature on key traits like metabolic rates and thermal tolerance, and this difference is detectable down to gene expression level. Rapid selection for faster growth in stable laboratory environments appears to have carried with it a trade-off against physiological plasticity in captive zebrafish compared with their wild counterparts.

Genome-wide association mapping for high temperature tolerance in wheat through 90k SNP array using physiological and yield traits.

Dissecting the genetic basis of physiological and yield traits against tolerance to heat stress is an essential in wheat breeding programs to boost up the wheat yield for sustainable food security. Herein, a genome-wide association study (GWAS) was performed to reveal the genetic basis of heat tolerance using high-density Illumina 90K Infinium SNPs array through physiological and yield indices. These indices were phenotyped on a diverse panel of foreign and domestic genotypes of Pakistan, grown in normal and heat-stressed environments. Based on STRUCTURE analysis, the studied germplasm clustered into four sub-population. Highly significant variations with a range of moderate (58.3%) to high (77.8%) heritability was observed under both conditions. Strong positive correlation existed among physiological and yield related attributes. A total of 320 significant (-log10 P ≥ 3) marker-trait associations (MTAs) were identified for the observed characters. Out of them 169 and 151 MTAs were recorded in normal and heat stress environments, respectively. Among the MTA loci, three (RAC875_c103017_302, Tdurum_contig42087_1199, and Tdurum_contig46877_488 on chromosomes 4B, 6B, and 7B respectively), two (BobWhite_c836_422 and BS00010616_51) and three (Kukri_rep_c87210_361, D_GA8KES401BNLTU_253 and Tdurum_contig1015_131) on chromosomes 5A, 1B, and 3D at the positions 243.59cM, 77.82cM and 292.51cM) showed pleiotropic effects in studied traits under normal, heat-stressed and both conditions respectively. The present study not only authenticated the numerous previously reported MTAs for examined attributes but also revealed novel MTAs under heat-stressed conditions. Identified SNPs will be beneficial in determining the novel genes in wheat to develop the heat tolerant and best yielded genotypes to fulfill the wheat requirement for the growing population.

Mechanisms of temperature-regulated growth and thermotolerance in crop species.

Temperature is a major environmental factor affecting the development and productivity of crop species. The ability to cope with periods of high temperatures, also known as thermotolerance, is becoming an increasingly indispensable trait for the future of agriculture owing to the current trajectory of average global temperatures. From temperature sensing to downstream transcriptional changes, here, we review recent findings involving the thermal regulation of plant growth and the effects of heat on hormonal pathways, reactive oxygen species, and epigenetic regulation. We also highlight recent approaches and strategies that could be integrated to confront the challenges in sustaining crop productivity in future decades.

Short-term warming does not affect intrinsic thermotolerance but induces strong sustaining photoprotection in tropical evergreen citrus genotypes.

Consequences of warming and postwarming events on photosynthetic thermotolerance (PT ) and photoprotective responses in tropical evergreen species remain elusive. We chose Citrus to answer some of the emerging questions related to tropical evergreen species' PT behaviour including (i) how wide is the genotypic variation in PT ? (ii) how does PT respond to short-term warming and (iii) how do photosynthesis and photoprotective functions respond over short-term warming and postwarming events? A study on 21 genotypes revealed significant genotypic differences in PT , though these were not large. We selected five genotypes with divergent PT and simulated warming events: Tmax 26/20°C (day-time highest maximum/night-time lowest maximum) (Week 1) < Tmax 33/30°C (Week 2) < Tmax 36/32°C (Week 3) followed by Tmax 26/16°C (Week 4, recovery). The PT of all genotypes remained unaltered despite strong leaf megathermy (leaf temperature > air temperature) during warming events. Though moderate warming showed genotype-specific stimulation in photosynthesis, higher warming unequivocally led to severe loss in net photosynthesis and induced higher nonphotochemical quenching. Even after a week of postwarming, photoprotective mechanisms strongly persisted. Our study points towards a conservative PT in evergreen citrus genotypes and their need for sustaining higher photoprotection during warming as well as postwarming recovery conditions.