Significance: Are there biological constants unifying phenotypic diversity across scales? Metabolic scaling theory (MST) predicts mathematical regularity and constancy in the allometric scaling of growth rate with body size across species. Here we show that adaptation to climate inArabidopsis thalianais associated with local strains that substantially deviate from the values predicted by MST. This deviation can be linked to increased stress tolerance at the expense of seed production, and it occurs through selection on genes that are involved in the abiotic stress response and are geographically correlated with climatic conditions. This highlights the evolutionary role of allometric diversification and helps establish the physiological bases of plant adaptation to contrasting environments.

High temperature (HT) is a major limiting factor for plant productivity. Because some responses to HT, notably hyponasty, resemble those encountered in low light (LL), we hypothesized that plant responses to HT are under the control of carbon balance. We analysed the interactive effects of HT and irradiance level on hyponasty and a set of traits related to plant growth in natural accessions ofArabidopsis thalianaand mutants affected in heat dissipation through transpiration (NCED6‐OE,ost2) and starch metabolism (pgm). HT induced hyponasty, reduced plant growth and modified leaf structure. LL worsened the effects of HT, while increasing light restored trait values close to levels observed at control temperature. Leaf temperatureper sedid not play a major role in the observed responses. By contrast, a major role of carbon balance was supported by hyponastic growth ofpgm, as well as morphological, physiological (photosynthesis, sugar and starch contents) and transcriptional data. Carbon balance could be a common sensor of HT and LL, leading to responses specific of the shade avoidance syndrome. Hyponasty and associated changes in plant traits could be key traits conditioning plant performance under competition for light, particularly in warm environments.

Effects of abiotic and biotic stresses on plant photosynthetic performance lead to fitness and yield decrease. The maximum quantum efficiency of photosystem II (F v/F m) is a parameter of chlorophyll fluorescence (ChlF) classically used to track changes in photosynthetic performance. Despite recent technical and methodological advances in ChlF imaging, the spatio-temporal heterogeneity of F v/F m still awaits for standardized and accurate quantification. We developed a method to quantify the dynamics of spatial heterogeneity of photosynthetic efficiency through the distribution-based analysis of F v/F m values. The method was applied to Arabidopsis thaliana grown under well-watered and severe water deficit (survival rate of 40%). First, whole-plant F v/F m shifted from unimodal to bimodal distributions during plant development despite a constant mean F v/F m under well-watered conditions. The establishment of a bimodal distribution of F v/F m reflects the occurrence of two types of leaf regions with contrasted photosynthetic efficiency. The distance between the two modes (called S) quantified the whole-plant photosynthetic heterogeneity. The weighted contribution of the most efficient/healthiest leaf regions to whole-plant performance (called W max) quantified the spatial efficiency of a photosynthetically heterogeneous plant. Plant survival to water deficit was associated to high S values, as well as with strong and fast recovery of W max following soil rewatering. Hence, during stress surviving plants had higher, but more efficient photosynthetic heterogeneity compared to perishing plants. Importantly, S allowed the discrimination between surviving and perishing plants four days earlier than the mean F v/F m. A sensitivity analysis from simulated dynamics of F v/F m showed that parameters indicative of plant tolerance and/or stress intensity caused identifiable changes in S and W max. Finally, an independent comparison of six Arabidopsis accessions grown under well-watered conditions indicated that S and W max are related to the genetic variability of growth. The distribution-based analysis of ChlF provides an efficient tool for quantifying photosynthetic heterogeneity and performance. S and W max are good indicators to estimate plant survival under water stress. Our results suggest that the dynamics of photosynthetic heterogeneity are key components of plant growth and tolerance to stress.