Transmembrane transport and stress response genes play an important role in adaptation of Arabidopsis halleri to metalliferous soils

Abstract

When plants adapt to local environments, strong signatures of selection are expected in the genome, particularly in high-stress environments such as trace metal element enriched (metalliferous) soils. Using Arabidopsis halleri, a model species for metal homeostasis and adaptation to extreme environments, we identifid genes, gene variants, and pathways that are associated with soil properties and may thus contribute to adaptation to high concentrations of trace metal elements. We analysed whole-genome Pool-seq data from two metallicolous (from metalliferous soils) and two non-metallicolous populations (in total 119 individuals) and associated allele frequencies of the identified single-nucleotide polymorphisms (SNPs) with soil variables measured on site. Additionally, we accounted for polygenic adaptation by searching for gene pathways showing enrichment of signatures of selection. Out of >2.5 million SNPs, we identified 57 SNPs in 19 genes that were significantly associated with soil variables and are members of three enriched pathways. At least three of these candidate genes and pathways are involved in transmembrane transport and/or associated with responses to various stresses such as oxidative stress. We conclude that both allocation and detoxification processes play a crucial role in A. halleri for coping with these unfavourable conditions.

Genomic signatures of convergent adaptation to Alpine environments in three Brassicaceae species

“…For each population pool, we prepared Illumina paired-end libraries (2 × 100 bp) with an insertion size of ~250 bp. For the reference assembly of the highly outcrossing A. halleri, we made one Illumina paired-end library from leaf material from a single individual grown from a seed of low-polymorphism population Aha11 (for more details see Sailer et al, 2018).…”

“…Scaffolds below 200 bp in length were removed. The reference assembly of A. halleri (Ahalleri_CH_v2) was published in Sailer et al (2018) and done in a slightly different way (see above); quality trimmed paired-end and mate-pair reads were assembled together with VelVet 1.2.08.…”

Arabidopsis halleri: a perennial model system for studying population differentiation and local adaptation

“…As we have seen in the studies of altitudinal adaptation on Mt. Ibuki and in the Alps, a genome scan by whole-genome re-sequencing of population pools (Pool-Seq) was conducted to identify SNPs that associate with heavy metal concentration in natural habitats (Sailer et al 2018). They used two M and two NM populations ( N = 119 plants) and identified 57 SNPs in 19 genes significantly associated with soil adaptation.…”

Evolution of the metal hyperaccumulation and hypertolerance traits

“…However, advances in this field are still few and limited to those hyperaccumulators for which a closely related reference genome is available, such as A. halleri (Briskine et al, 2017). For example, whole-genome SNP comparisons between Polish metallicolous and non-metallicolous A. halleri populations identified 57 SNPs in 19 genes that were associated with edaphic conditions (Sailer et al, 2018). On the other hand, whole-genome scan analysis, comparing calamine and non-metallicolous populations of pseudo-metallophytes,…”

“…Similarly, genetic variation was found associated with soil metal concentration in an analysis comparing metallicolous and non-metallicolous populations of A. halleri from Poland. Considering the genes linked to adaptation to metallicolous soils, there was a significant enrichment of ion transport and stress response pathways (Sailer et al, 2018). On the other hand, the aforementioned A. halleri metallicolous populations, I16 and PL22, which belong to different phylogeographic units, have evolved distinct strategies to cope with Zn and Cd excess, involving the modulation of very different sets of genes for metal uptake and storage, mineral homeostasis and stress response (Corso et al, 2018;Schvartzman et al, 2018).…”