Contrasting cadmium resistance strategies in two metallicolous populations of Arabidopsis halleri

Abstract

While cadmium (Cd) tolerance is a constitutive trait in the Arabidopsis halleri species, Cd accumulation is highly variable. Recent adaptation to anthropogenic metal stress has occurred independently within the genetic units of A. halleri and the evolution of different mechanisms involved in Cd tolerance and accumulation has been suggested. To gain a better understanding of the mechanisms underlying Cd tolerance and accumulation in A. halleri, ionomic inductively coupled plasma mass spectrometry (ICP-MS), transcriptomic (RNA sequencing) and metabolomic (high-performance liquid chromatography-mass spectrometry) profiles were analysed in two A. halleri metallicolous populations from different genetic units (PL22 from Poland and I16 from Italy). The PL22 and I16 populations were both hypertolerant to Cd, but PL22 hyperaccumulated Cd while I16 behaved as an excluder both in situ and when grown hydroponically. The observed hyperaccumulator vs excluder behaviours were paralleled by large differences in the expression profiles of transporter genes. Flavonoid-related transcripts and metabolites were strikingly more abundant in PL22 than in I16 shoots. The role of novel A. halleri candidate genes possibly involved in Cd hyperaccumulation or exclusion was supported by the study of corresponding A. thaliana knockout mutants. Taken together, our results are suggestive of the evolution of divergent strategies for Cd uptake, transport and detoxification in different genetic units of A. halleri.

Protein lysine methylation contributes to modulating the response of sensitive and tolerant Arabidopsis species to cadmium stress

“…Then, the expression of KMT genes was analysed in the I16 and PL22 populations challenged with Cd. After 4 weeks of acclimatization in hydroponic growth medium, plants were treated with 5 μM CdSO 4 for 10 days and transcriptomic analysis was performed in root and shoot samples using RNA sequencing (Corso et al, ). Genes coding KMTs were retrieved from the RNAseq data and their expression was analysed.…”

“…The effect of the treatment (Cd vs. CM) was less important, accounting for 34 and 19% of the variance in roots and shoots, respectively (Figure a). DEGs were then identified in two pairwise comparisons to estimate the effect of the genetic unit and the treatment ( p < .05, threshold set at 1.4‐fold change) (Corso et al, ). In agreement with the PCA, the PL22/I16 comparison identified 16 DEGs in roots and 10 DEGs in shoots (Figure b), whereas the Cd/control comparison yielded only four DEGs in PL22 and none in I16 (Figure c).…”

“…Relative expression levels of KMT genes were retrieved from the different experiments, the ratio between Cd and control conditions were calculated from pairwise comparisons, and a non‐parametric Student's t test was performed on log2 ratio to determine differentially expressed genes (DEGs, with p ‐value <.05) and the threshold was set at twofold (−1 ≤ log2 fold change ≥1). Finally, we used the RNA‐seq data we obtained to analyse the tolerance strategies to Cd of two metallicolous populations of A. halleri (BioProject PRJNA388549) (Corso et al, ). In this experiment, gene expression in the I16 and PL22 populations was analysed after 10 days of treatment with 5 μM Cd in hydroponics.…”

“…Arabidopsis halleri , a close relative of A. thaliana and A. lyrata , is a model species for studying tolerance and accumulation of cadmium (Cd), one of the most toxic metal for living organisms (for reviews, see Kramer, ; DalCorso, Fasani, & Furini, ; Verbruggen, Juraniec, Baliardini, & Meyer, ; Moulis, Bourguignon, & Catty, ). While Cd and zinc tolerance seems to be constitutive in A. halleri , populations originating from different genetic units and from metallicolous or non‐metallicolous soils display important variability in terms of Cd accumulation (Corso et al, ; Meyer et al, ; Schvartzman et al, ; Stein et al, ). This intraspecific variability suggests adaptation at the local scale and, possibly, the involvement of different molecular mechanisms to account for metal accumulation and tolerance traits.…”

“…To test this hypothesis, we analysed the expression of the two main players involved in protein Lys methylation, that is, Lys‐methylated proteins and genes coding KMTs, in three Arabidopsis species challenged with Cd. We used A. thaliana and A. lyrata non‐tolerant plants and three populations of A. halleri from different genetic units and showing contrasting tolerance and accumulation of Cd (Corso et al, ; Meyer et al, ; Schvartzman et al, ). First, we showed that some non‐histone proteins are differentially methylated at Lys residues in response to Cd and we identified one of these proteins by MS/MS.…”