Plant competition cues activate a singlet oxygen signaling pathway in Arabidopsis thaliana.

Oxidative stress responses of Arabidopsis to reflected low red to far-red signals (R:FR ≈ 0.3) generated by neighboring weeds or an artificial source of FR light were compared with a weed-free control (R:FR ≈1.6). In the low R:FR treatments, induction of the shade avoidance responses (SAR) coincided with increased leaf production of singlet oxygen (1O2). This 1O2 increase was not due to protochlorophyllide accumulation and did not cause cell death. Chemical treatments, however, with 5-aminolevulinic acid (the precursor of tetrapyrrole biosynthesis) and glutathione (a quinone A reductant) enhanced cell death and growth inhibition. RNA sequencing revealed that transcriptome responses to the reflected low R:FR light treatments minimally resembled previously known Arabidopsis 1O2 generating systems that rapidly generate 1O2 following a dark to light transfer. The upregulation of only a few early 1O2 responsive genes (6 out of 1931) in the reflected low R:FR treatments suggested specificity of the 1O2 signaling. Moreover, increased expression of two enzyme genes, the SULFOTRANSFERASE ST2A (ST2a) and the early 1O2-responsive IAA-LEUCINE RESISTANCE (ILR)-LIKE6 (ILL6), which negatively regulate jasmonate level, suggested that repression of bioactive JAs may promote the shade avoidance (versus defense) and 1O2 acclimation (versus cell death) responses to neighboring weeds.

Caught between two states: The compromise in acclimation of photosynthesis, transpiration and mesophyll conductance to different amplitudes of fluctuating irradiance.

While dynamic regulation of photosynthesis in fluctuating light is increasingly recognized as an important driver of carbon uptake, acclimation to realistic irradiance fluctuations is still largely unexplored. We subjected Arabidopsis thaliana (L.) wild-type and jac1 mutants to irradiance fluctuations with distinct amplitudes and average irradiance. We examined how irradiance fluctuations affected leaf structure, pigments and physiology. A wider amplitude of fluctuations produced a stronger acclimation response. Large reductions of leaf mass per area under fluctuating irradiance framed our interpretation of changes in photosynthetic capacity and mesophyll conductance as measured by three separate methods, in that photosynthetic investment increased markedly on a mass basis, but only a little on an area basis. Moreover, thermal imagery showed that leaf transpiration was four times higher under fluctuating irradiance. Leaves growing under fluctuating irradiance, although thinner, maintained their photosynthetic capacity, as measured through light- and CO2-response curves; suggesting their photosynthesis may be more cost-efficient than those under steady light, but overall may incur increased maintenance costs. This is especially relevant for plant performance globally because naturally fluctuating irradiance creates conflicting acclimation cues for photosynthesis and transpiration that may hinder progress towards ensuring food security under climate-related extremes of water stress.

Acclimation capacity to global warming of amphibians and freshwater fishes: Drivers, patterns, and data limitations.

Amphibians and fishes play a central role in shaping the structure and function of freshwater environments. These organisms have a limited capacity to disperse across different habitats and the thermal buffer offered by freshwater systems is small. Understanding determinants and patterns of their physiological sensitivity across life history is, therefore, imperative to predicting the impacts of climate change in freshwater systems. Based on a systematic literature review including 345 experiments with 998 estimates on 96 amphibian (Anura/Caudata) and 93 freshwater fish species (Teleostei), we conducted a quantitative synthesis to explore phylogenetic, ontogenetic, and biogeographic (thermal adaptation) patterns in upper thermal tolerance (CTmax) and thermal acclimation capacity (acclimation response ratio, ARR) as well as the influence of the methodology used to assess these thermal traits using a conditional inference tree analysis. We found globally consistent patterns in CTmax and ARR, with phylogeny (taxa/order), experimental methodology, climatic origin, and life stage as significant determinants of thermal traits. The analysis demonstrated that CTmax does not primarily depend on the climatic origin but on experimental acclimation temperature and duration, and life stage. Higher acclimation temperatures and longer acclimation times led to higher CTmax values, whereby Anuran larvae revealed a higher CTmax than older life stages. The ARR of freshwater fishes was more than twice that of amphibians. Differences in ARR between life stages were not significant. In addition to phylogenetic differences, we found that ARR also depended on acclimation duration, ramping rate, and adaptation to local temperature variability. However, the amount of data on early life stages is too small, methodologically inconsistent, and phylogenetically unbalanced to identify potential life cycle bottlenecks in thermal traits. We, therefore, propose methods to improve the robustness and comparability of CTmax/ARR data across species and life stages, which is crucial for the conservation of freshwater biodiversity under climate change.

Thermal tolerance and acclimation capacity in the European common frog (Rana temporaria) change throughout ontogeny.

Phenotypic plasticity may allow ectotherms with complex life histories such as amphibians to cope with climate-driven changes in their environment. Plasticity in thermal tolerance (i.e., shifts of thermal limits via acclimation to higher temperatures) has been proposed as a mechanism to cope with warming and extreme thermal events. However, thermal tolerance and, hence, acclimation capacity, is known to vary with life stage. Using the common frog (Rana temporaria) as a model species, we measured the capacity to adjust lower (CTmin ) and upper (CTmax ) critical thermal limits at different acclimation temperatures. We calculated the acclimation response ratio as a metric to assess the stage-specific acclimation capacity at each of seven consecutive ontogenetic stages and tested whether acclimation capacity was influenced by body mass and/or age. We further examined how acclimation temperature, body mass, age, and ontogenetic stage influenced CTmin and CTmax . In the temperate population of R. temporaria that we studied, thermal tolerance and acclimation capacity were affected by the ontogenetic stage. However, acclimation capacity at both thermal limits was well below 100% at all life stages tested. The lowest and highest acclimation capacity in thermal limits was observed in young and late larvae, respectively. The relatively low acclimation capacity of young larvae highlights a clear risk of amphibian populations to ongoing climate change. Ignoring stage-specific differences in thermal physiology may drastically underestimate the climate vulnerability of species, which will hamper successful conservation actions.

Interindividual plasticity in metabolic and thermal tolerance traits from populations subjected to recent anthropogenic heating.

To better understand temperature's role in the interaction between local evolutionary adaptation and physiological plasticity, we investigated acclimation effects on metabolic performance and thermal tolerance among natural Fundulus heteroclitus (small estuarine fish) populations from different thermal environments. Fundulus heteroclitus populations experience large daily and seasonal temperature variations, as well as local mean temperature differences across their large geographical cline. In this study, we use three populations: one locally heated (32°C) by thermal effluence (TE) from the Oyster Creek Nuclear Generating Station, NJ, and two nearby reference populations that do not experience local heating (28°C). After acclimation to 12 or 28°C, we quantified whole-animal metabolic (WAM) rate, critical thermal maximum (CTmax) and substrate-specific cardiac metabolic rate (CaM, substrates: glucose, fatty acids, lactate plus ketones plus ethanol, and endogenous (i.e. no added substrates)) in approximately 160 individuals from these three populations. Populations showed few significant differences due to large interindividual variation within populations. In general, for WAM and CTmax, the interindividual variation in acclimation response (log2 ratio 28/12°C) was a function of performance at 12°C and order of acclimation (12-28°C versus 28-12°C). CTmax and WAM were greater at 28°C than 12°C, although WAM had a small change (2.32-fold) compared with the expectation for a 16°C increase in temperature (expect 3- to 4.4-fold). By contrast, for CaM, the rates when acclimatized and assayed at 12 or 28°C were nearly identical. The small differences in CaM between 12 and 28°C temperature were partially explained by cardiac remodeling where individuals acclimatized to 12°C had larger hearts than individuals acclimatized to 28°C. Correlation among physiological traits was dependent on acclimation temperature. For example, WAM was negatively correlated with CTmax at 12°C but positively correlated at 28°C. Additionally, glucose substrate supported higher CaM than fatty acid, and fatty acid supported higher CaM than lactate, ketones and alcohol (LKA) or endogenous. However, these responses were highly variable with some individuals using much more FA than glucose. These findings suggest interindividual variation in physiological responses to temperature acclimation and indicate that additional research investigating interindividual may be relevant for global climate change responses in many species.

Climate vulnerability of South American freshwater fish: Thermal tolerance and acclimation.

Freshwater fish are restricted by their physiology to rivers and lakes, and are generally limited in their capacity to disperse across basins. As a result, there is often a close match between the evolutionary history of river basins and their natural history. Thus, the regional landscape and ecological features, such as temperature, have shaped the evolution and adaptation of local fish assemblages. Climate change is expected to affect fish diversity and increase extinction, especially in low latitudes, and it has been suggested that species that inhabit low latitude species are more susceptible since they live close to their maximum thermal limits and have low capacity for acclimation. To understand the mechanisms of variation in thermal tolerance across a broad-scale of South American fishes is fundamental to be able to assess the vulnerability of species and habitat to global warming. Herein, we present the first attempt to analyze the vulnerability of South American freshwater fish species, based on the review of upper thermal limits of 106 species from a broad range of latitudinal habitats. Our findings show that upper thermal limits decrease with latitude, while the thermal safety margin (TSM) increase. Furthermore, the latitude has little effects on the acclimation response ratio, and the TSM decreased with rising temperatures. These data suggest that thermal phenotypic acclimation has low potential for mitigating global warming. These results indicate that South American fish species living in tropical areas are more susceptible to global warming since they are already living close to their maximum habitat temperature.

TMEA: A Thermodynamically Motivated Framework for Functional Characterization of Biological Responses to System Acclimation.

The objective of gene set enrichment analysis (GSEA) in modern biological studies is to identify functional profiles in huge sets of biomolecules generated by high-throughput measurements of genes, transcripts, metabolites, and proteins. GSEA is based on a two-stage process using classical statistical analysis to score the input data and subsequent testing for overrepresentation of the enrichment score within a given functional coherent set. However, enrichment scores computed by different methods are merely statistically motivated and often elusive to direct biological interpretation. Here, we propose a novel approach, called Thermodynamically Motivated Enrichment Analysis (TMEA), to account for the energy investment in biological relevant processes. Therefore, TMEA is based on surprisal analysis, which offers a thermodynamic-free energy-based representation of the biological steady state and of the biological change. The contribution of each biomolecule underlying the changes in free energy is used in a Monte Carlo resampling procedure resulting in a functional characterization directly coupled to the thermodynamic characterization of biological responses to system perturbations. To illustrate the utility of our method on real experimental data, we benchmark our approach on plant acclimation to high light and compare the performance of TMEA with the most frequently used method for GSEA.

Effects of developmental acclimation on fitness costs differ between two aphid species.

Most ectotherms are able to increase their tolerance to heat stress via the acclimation response. However, there is ongoing debate about whether the acclimation response is associated with fitness costs, and what factors can affect the consequences of acclimation are still unclear. To elucidate this, we sought to determine whether fitness costs varied with acclimation conditions in two cereal aphids, Sitobion avenae and Rhopalosiphum padi. Thus, the basal and inducible thermal tolerances (maximum critical temperature [CTmax]) and fitness traits (proportion of adult emergence, adult longevity, fecundity, and population parameters) of adult aphids were measured under three conditions of developmental acclimation: 1) 22 °C constant temperature (no acclimation), 2) 22 °C + 34 °C for 2 h per day (low daytime temperature), and 3) 22 °C + 38 °C for 2 h per day (high daytime temperature). We found that the thermal tolerances of both species were significantly higher following developmental acclimations, where higher basal and inducible thermal tolerances were observed in R. padi than in S. avenae. Low daytime temperature acclimation conditions (34 °C) resulted in negligible reproductive costs and improved the intrinsic rates of population increase in both species. In contrast, substantial fitness costs were detected in both species in response to high daytime temperature acclimation (38 °C), especially for S. avenae. Our results indicate that the effects of acclimation conditions on fitness costs differ between the two aphid species. These findings will not only enhance our understanding of species dynamics in the context of climate change but could also potentially improve pest control efforts.

An Arabidopsis soluble chloroplast proteomic analysis reveals the participation of the Executer pathway in response to increased light conditions.

The Executer1 and Executer2 proteins have a fundamental role in the signalling pathway mediated by singlet oxygen in chloroplast; nonetheless, not much is known yet about their specific activity and features. Herein, we have followed a differential-expression proteomics approach to analyse the impact of Executer on the soluble chloroplast protein abundance in Arabidopsis. Because singlet oxygen plays a significant role in signalling the oxidative response of plants to light, our analysis also included the soluble chloroplast proteome of plants exposed to a moderate light intensity in the time frame of hours. A number of light- and genotype-responsive proteins were detected, and mass-spectrometry identification showed changes in abundance of several photosynthesis- and carbon metabolism-related proteins as well as proteins involved in plastid mRNA processing. Our results support the participation of the Executer proteins in signalling and control of chloroplast metabolism, and in the regulation of plant response to environmental changes.