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

  1. Oceane Cassan
  2. Lea-Lou Pimpare
  3. Timothy Mozzanino
  4. Cecile Fizames
  5. Sebastien Devidal
  6. Fabrice Roux
  7. Alexandru Milcu
  8. Sophie Lebre
  9. Alain Gojon
  10. Antoine Martin  Is a corresponding author
  1. IPSiM, Univ Montpellier, CNRS, INRAE, Institut Agro, France
  2. Montpellier European Ecotron, Univ Montpellier, CNRS, Campus Baillarguet, France
  3. Laboratoire des Interactions Plantes-Microbes-Environnement, Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement, CNRS, Université de Toulouse, France
  4. CEFE, Univ Montpellier, CNRS, EPHE, IRD, France
  5. IMAG, Univ Montpellier, CNRS, France
8 figures and 2 additional files

Figures

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.

Figure 4 with 1 supplement
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.

Figure 4—figure supplement 1
Geographic distribution of accessions for each cluster identified within the REGMAP panel.

(A) Full distribution. (B) Zoom into European accessions. (C) Zoom into North-American accessions.

Figure 5 with 3 supplements
Genetic architecture of the response of the ionome to elevated CO2 in the REGMAP panel of Arabidopsis thaliana.

(A) Manhattan 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 Manhattan 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 two or three traits.

Figure 5—figure supplement 1
Snapshots of the Manhattan plots of Na content (A) and N content (B) under ambient CO2 in the REGMAP panel.

Peaks of high p-values are observed at the HKT1 locus for the Na content (A) and at the NIA1 locus for the N content (B).

Figure 5—figure supplement 2
Qqplots from the GWAs corresponding to data for the level of each mineral under ambient and under elevated CO2, as well as for the percentage of change between ambient and elevated CO2 for each element.
Figure 5—figure supplement 3
Manhattan plots made from the GWAs corresponding to data for the level of each mineral under elevated CO2, as well as for the percentage of change between ambient and elevated CO2 for each element.
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 pattern 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.

Author response image 1

Additional files

Supplementary file 1

Clustering of the REGMAP population and expression data in response to CO2.

(a) List of accessions per clusters identified by k-means approach in the REGMAP panel. (b) List of top 50 SNPs identified by GWAs for the content of each element under eCO2. "snp": coordinates of the SNP identified. "shared": number of traits for which the SNP is identified in the top 50 list. "element": element for which the SNP has been identified in the top 50 list. "chrom": chromosome number on which the SNP is positionned. "position": position of the SNP in the chromosome. "AGIs": list of genes located at -/+25 kb from the SNP. (c) List of top 50 SNPs identified by GWAs for the relative change of each element between eCO2 and aCO2. "snp": coordinates of the SNP identified. "shared": number of traits for which the SNP is identified in the top 50 list. "element": element for which the SNP has been identified in the top 50 list. "chrom": chromosome number on which the SNP is positionned. "position": position of the SNP in the chromosome. "AGIs": list of genes located at -/+25 kb from the SNP. (d) List of genes differentially expressed by eCO2 in shoot or root. (e) List of genes identified by GWAs for each element that are differentially expressed by eCO2 in shoot or root. (f) List of primers used for qRT-PCR. (g) Number of outliers removed from each dataset.

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  1. Oceane Cassan
  2. Lea-Lou Pimpare
  3. Timothy Mozzanino
  4. Cecile Fizames
  5. Sebastien Devidal
  6. Fabrice Roux
  7. Alexandru Milcu
  8. Sophie Lebre
  9. Alain Gojon
  10. Antoine Martin
(2024)
Natural genetic variation underlying the negative effect of elevated CO2 on ionome composition in Arabidopsis thaliana
eLife 12:RP90170.
https://doi.org/10.7554/eLife.90170.3