Natural genetic variation underlying the negative effect of elevated CO2 on ionome composition in Arabidopsis thaliana

Abstract The elevation of atmospheric CO 2 leads to a decline in the plant mineral content, which poses a major 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 CO 2 on plant mineral composition. Yet, several studies have shown a certain degree of diversity in the ionome’s response to elevated CO 2 , associated with genotypic variation. This suggests the existence of genetic factors controlling the effect of CO 2 on ionome composition. However, no large-scale studies have been carried out to date to explore the genetic diversity of the ionome responses to elevated CO 2 . Here, we used six hundred Arabidopsis thaliana accessions, representing geographical distributions ranging from worldwide to regional and local environments, to analyze the natural genetic variation underlying the negative effect of elevated CO 2 on the ionome composition in plants. We show that the growth under elevated CO 2 leads 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 CO 2 , 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 CO 2 . Using genome-wide association mapping on the response of each mineral element to elevated CO 2 or on integrative traits, we identified a large set of QTLs and genes associated with the ionome response to elevated CO 2 . Finally, we demonstrate that manipulating the function of one of these genes can mitigate the negative effect of elevated CO 2 on the plant mineral composition. Therefore, this resource will contribute to understand the genetic mechanisms underlying the negative effect of elevated CO 2 on the mineral composition of plants, and to the development of biofortified crops adapted to a high-CO 2 world.