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

Christian Sailer,Stefan Zoller,Alicja Babst-Kostecka,Martin C Fischer,Alex Widmer,Pierre Vollenweider,Felix Gugerli,Christian Rellstab

doi:10.1038/s41598-018-33938-2

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.

Highlights

Local adaptation is a key evolutionary process allowing plants to cope with environmental changes and/or to colonize new and selective habitats
Under experimentally controlled conditions, when all plants are exposed to the same elevated metal concentrations, non-metallicolous populations often accumulate higher amounts of trace metal elements (TMEs) compared to metallicolous populations, reaching the threshold concentration for hyperaccumulation[20,21,22]
We searched for adaptive genetic changes that have evolved to allow the Brassicaceae Arabidopsis halleri to grow on M soils that were polluted with TMEs by mining since the late medieval times or more recently (

Summary

Introduction

Local adaptation is a key evolutionary process allowing plants to cope with environmental changes and/or to colonize new and selective habitats. Metalliferous (M) habitats exert a strong selection pressure on plant communities from high and potentially toxic concentrations of some trace metal elements (TMEs) in soils (Thlaspi caerulescens[4], Biscutella laevigata[5]) Such high concentrations of TMEs can occur naturally, for example in rare serpentine soils[6], or can result from anthropogenic activities (e.g. mining). Genome scans[11,23] and quantitative genetic studies[24,25] have shown the involvement of genomic regions and genes that underlie processes of internal metal transport, homeostasis and/or detoxification in leaves of hyperaccumulating plants Still, these studies are based on genomic information and categorical assignment (e.g. M or NM soils) only and lack associations with quantitative environmental variables that characterize e.g. soil metal content. The existing analyses and interpretations are often gene-focused and offer only limited insight into the genetic basis of adaptation to environmental stress, despite increasing evidence suggesting that such adaptation is polygenic[26]

Methods

Results

Conclusion