Quantifying spatial heterogeneity of chlorophyll fluorescence during plant growth and in response to water stress

Background: 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. Results: 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 Wmax 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 Wmax are related to the genetic variability of growth. Conclusions: 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.