Natural genetic variation underlying the negative effect of elevated CO₂on ionome composition inArabidopsis thaliana

The elevation of atmospheric CO₂leads to a decline in the plant mineral content, which might pose a significant threat to food security in the coming decades. To date, very few genes have been identified as having a role in the negative effect of elevated CO₂on plant mineral composition. Yet, several studies have shown a certain degree of diversity in the ionome’s response to elevated CO₂, associated with genotypic variation. This suggests the existence of genetic factors controlling the effect of CO₂on ionome composition. However, no large-scale studies have been carried out to date to explore the genetic diversity of the ionome responses to elevated CO₂. Here, we used six hundredArabidopsis thalianaaccessions, representing geographical distributions ranging from worldwide to regional and local environments, to analyze the natural genetic variation underlying the negative effect of elevated CO₂on the ionome composition in plants. We show that the growth under elevated CO₂leads to a global and important decrease of the ionome content whatever the geographic distribution of the population. We also observed a high range of genetic diversity in the response of the ionome composition to elevated CO₂, and we identified sub-populations, showing effects on their ionome ranging from the most pronounced to resilience or even to a benefit in response to elevated CO₂. Using genome-wide association mapping on the response of each mineral element to elevated CO₂or on integrative traits, we identified a large set of QTLs and genes associated with the ionome response to elevated CO₂. Finally, we demonstrate that the function of one of these genes is associated to the negative effect of elevated CO₂on the plant mineral composition. This resource will contribute to understand the genetic mechanisms underlying the negative effect of elevated CO₂on plant mineral nutrition, and could help towards the development of crops adapted to a high-CO₂world.