Plant Biology

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

Océane Cassan
Léa-Lou Pimparé
Timothy Mozzanino
Cécile Fizames
Sébastien Devidal
Fabrice Roux
Alexandru Milcu
Sophie Lèbre
Alain Gojon
Antoine Martin author has email address

IPSiM, Univ Montpellier, CNRS, INRAE, Institut Agro, 34060, Montpellier, France
Montpellier European Ecotron, Univ Montpellier, CNRS, Campus Baillarguet, 34980, Montferrier-sur-Lez, France
Laboratoire des Interactions Plantes-Microbes-Environnement, Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement, CNRS, Université de Toulouse, Castanet-Tolosan, France
CEFE, Univ Montpellier, CNRS, EPHE, IRD, 34293, Montpellier, France
IMAG, Univ Montpellier, CNRS, Montpellier, France

https://doi.org/10.7554/eLife.90170.2

Open access
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Figures and data

Elevated CO₂ negatively impacts the ionome content at the population-scale level in Arabidopsis thaliana.
A. Representation of the experimental design used in this study. The content of eight mineral elements was assessed for around 600 Arabidopsis thaliana accessions coming from the REGMAP (B), LANGUEDOC (C) and TOU-A (D) populations. Each dot represents the value of the content of a mineral element for one accession (yellow: ambient CO₂ (aCO₂, ∼420 ppm), blue: elevated CO₂ (eCO₂, 900 ppm). N (% of dry weight), Fe (µg.g^-1 dry weight), Zn (µg.g^-1 dry weight), Cu (µg.g^-1 dry weight), Mg (µg.g^-1 dry weight), Mn (µg.g^-1 dry weight), Na (µg.g^-1 dry weight), C (% of dry weight). Asterisks indicate significant differences (Paired Wilcoxson test; *, P < 0.05; **, P < 0.005; ***, P < 0.0005). ns; not significant.

Elevated CO₂ leads to high phenotypic diversity of ionome response in Arabidopsis thaliana.
Distributions of the relative change (%) of the content of 8 mineral elements between elevated CO₂ and ambient CO₂, in each population (A: REGMAP, B: LANGUEDOC, C: TOU-A). Each dot represents the value of the relative change of the content a mineral element for one accession. The name of the element appears in bold if the mean of the element in elevated CO₂ is significantly different from the mean of the element in ambient CO₂ (Paired wilcoxon test, significance threshold of 0.05).

Elevated CO₂ results in a general pattern of ionome variation common to most accessions constituting natural populations of Arabidopsis thaliana.
Principal Component Analysis (PCA) was performed using the variation of each element in response to elevated CO₂. A. Natural accessions were positioned on the PCA and colored based on population. B. Contribution of each element to the PCA axis.

Variation in the response of the ionome to elevated CO₂ identifies contrasting subpopulations inside the REGMAP panel.
K-means clustering was performed in the REGMAP accessions to identify different subpopulations. Each accession is represented by a dot, connected by a line between each element. Cluster 1:65 accessions. Cluster 2: 25 accessions. Cluster 3: 69 accessions.

Genetic architecture of the response of the ionome to elevated CO₂ in the REGMAP panel of Arabidopsis thaliana.
A. Manhadan plots for the content of eight mineral elements under elevated CO₂, or for the relative change of the content of mineral elements between elevated CO₂ and ambient CO₂. For each Manhadan plot, SNPs with the 50 most significant P-value, located above the horizontal line, are colored. Bar plots showing the number of SNPs identified by GWAs for traits under elevated CO₂ (B) or for the relative change of the content of mineral elements between elevated CO₂ and ambient CO₂ (C) that are unique to one element or shared between 2 or 3 traits.

Identification of genes detected by GWA mapping and differentially regulated by elevated CO₂.
Intersection between elevated CO₂-DEG in shoot (A) or root (B) and genes identified by GWA mapping. UpSet plots display the number of elevated CO₂-DEG that are associated to a locus identified for the content or the relative change of one or several mineral elements under elevated CO₂. Illustration of the padern of elevated CO₂-DEG in shoot (C) or root (D) also identified by GWA mapping.

Natural variation of the TIP2;2 gene is associated with improved responses of Zn content to elevated CO₂.
A. Manhattan plot of the relative change of Zn content between elevated CO₂ and ambient CO₂ showing the presence of a peak closed to the TIP2;2 locus. B. Comparison of haplotypes and their relative change of Zn content between elevated CO₂ and ambient CO₂. Three SNPs located at the TIP2;2 locus are associated to an improvement of Zn content under elevated CO₂ for accessions that possess them (haplotype 1) compared to the rest of the population (haplotype 0). C, D. Relative expression of TIP2;2 in the roots under ambient (C) or elevated (D) CO₂ for accessions belonging to haplotype 0 or haplotype 1. Relative expression levels were calculated based on UBQ10 as internal control. Horizontal black line represented the median of each group of haplotypes. ***P < 0,001, **P < 0,01, unpaired Mann-Whitney test. E. Shoot Zn content under ambient or elevated CO₂ for WT (Columbia) and tip2;2-1 mutant. Data are presented as the mean (with SD) of 5 and 6 biological repeats for the WT and tip2;2-1, respectively.**P < 0.01, unpaired Mann-Whitney test.

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