Summary Leaf mineral composition, the leaf ionome, reflects the complex interaction between a plant and its environment including local soil composition, an influential factor that can limit species distribution and plant productivity. Here we addressed within‐species variation in plant–soil interactions and edaphic adaptation using Arabidopsis halleri, a well‐suited model species as a facultative metallophyte and metal hyperaccumulator.We conducted multi‐element analysis of 1972 paired leaf and soil samples from 165 European populations of A. halleri, at individual resolution to accommodate soil heterogeneity. Results were further confirmed under standardized conditions upon cultivation of 105 field‐collected genotypes on an artificially metal‐contaminated soil in growth chamber experiments.Soil‐independent between‐ and within‐population variation set apart leaf accumulation of zinc, cadmium and lead from all other nutrient and nonessential elements, concurring with differential hypothesized ecological roles in either biotic interaction or nutrition. For these metals, soil–leaf relationships were element‐specific, differed between metalliferous and nonmetalliferous soils and were geographically structured both in the field and under standardized growth conditions, implicating complex scenarios of recent ecological adaptation.Our study provides an example and a reference for future related work and will serve as a basis for the molecular–genetic dissection and ecological analysis of the observed phenotypic variation.

AbstractHeavy metal-rich toxic soils and ordinary soils are both natural habitats of Arabidopsis halleri, different from closely related plant species such as A. thaliana. Here we demonstrate enhanced Cd hypertolerance and attenuated Cd accumulation in plants originating from the most highly heavy metal-contaminated A. halleri site in Europe Ponte Nossa (Noss/IT), compared to A. halleri from non-metalliferous (NM) sites at both a small and a larger geographic distance. In the two populations from NM sites, hundreds of Cd-responsive transcripts mostly reflect the activation of Fe deficiency responses, whereas no single transcript responded to the same Cd treatment in plants from the metalliferous (M) site Noss. Instead, in Noss, thousands of transcripts exhibited an altered abundance irrespective of Cd exposure, with the highest enrichment for Gene Ontology Term “meiotic cell cycle”. Levels of ARGONAUTE 9 (AGO9) and the synaptonemal complex transverse filament protein-encoding ZYP1a/b transcripts, which are pre-meiosis- and meiosis-specific in A. thaliana, respectively, were strongly elevated in vegetative tissues of Noss, alongside transcripts with known additional functions in somatic genome integrity maintenance. Increased AGO9 transcript abundance was shared by individuals from M sites in Poland and Germany. Expression of IRON-REGULATED TRANSPORTER 1 (IRT1) was very low and of HEAVY METAL ATPASE 2 (HMA2) strongly elevated in Noss compared to both NM populations, largely explaining physiological differences in Cd handling. In summary, adaptation of Noss to extreme abiotic stress is associated with globally enhanced somatic genome integrity maintenance, as well as a small number of constitutive alterations in stress-specific functional networks.

Heavy metal-rich toxic soils and ordinary soils are both natural habitats of Arabidopsis halleri, a diploid perennial and obligate outcrosser in the sister clade of the genetic model plant Arabidopsis thaliana. The molecular divergence underlying survival in sharply contrasting environments is unknown. Here we comparatively address metal physiology and transcriptomes of A. halleri originating from the most highly heavy metal-contaminated soil in Europe, Ponte Nossa, Italy (Noss), and from non-metalliferous (NM) soils. Plants from Noss exhibit enhanced hypertolerance and attenuated accumulation of cadmium (Cd), and their transcriptomic Cd responsiveness is decreased, compared to plants of NM soil origin. Among the conditionindependent transcriptome characteristics of Noss, the most highly overrepresented functional class of 'meiotic cell cycle' comprises 21 transcripts with elevated abundance in vegetative tissues, in particular Argonaute 9 (AGO9) and the synaptonemal complex transverse filament protein-encoding ZYP1a/b. Increased AGO9 transcript levels in Noss are accompanied by decreased long terminal repeat retrotransposon expression. Similar to Noss, plants from other highly metalliferous sites in Poland and Germany share elevated somatic AGO9 transcript levels in comparison to plants originating from NM soils in their respective geographic regions. Transcript levels of Iron-Regulated Transporter 1 (IRT1) are very low and transcript levels of Heavy Metal ATPase 2 (HMA2) are strongly elevated in Noss, which can account for its altered Cd handling. We conclude that in plants adapted to the most extreme abiotic stress, broadly enhanced functions comprise genes with likely roles in somatic genome integrity maintenance, accompanied by few alterations in stress-specific functional networks.

Freezing tolerance is likely to be an important adaptation for both natural populations and crop cultivars like winter wheat (Triticum aestivum L.). In the United States, winter wheat represents 80% of the total wheat production. Understanding the genetic basis of freezing tolerance in wheat furthers our knowledge of abiotic stress tolerance in plants and may inform breeding programs aimed at adjusting the level of freezing tolerance for a given region. We examined freezing tolerance in a 267-line panel of elite soft red winter wheat that has previously been used for genome-wide association study (GWAS) on agronomically important traits. We were specifically interested in determining the extent of genetic variation for freezing tolerance within the panel, what the genetic basis of that variation is, and if there are correlations between freezing tolerance and other agronomically important traits. We found significant variation in freezing tolerance among the lines, measured as survival through three total days at −8 ˚C. We performed a GWAS on freezing tolerance and identified 13 candidate loci, with nearby candidate genes involved in different functions potentially associated with freezing tolerance. In addition, we found significant correlations between freezing tolerance and seven previously published yield related traits. In summary, we found considerable variation in freezing tolerance in this panel that is associated with yield related traits. Thus, these lines may be useful for breeding programs seeking to optimize freezing tolerance for present and future climatic conditions. INTRODUCTIONWheat (Triticum aestivum L.) is one of the most important crops worldwide. It is cultivated in ∼200 million ha (http: //www.fao.org/faostat/en/#data/QC/visualize) (Zhao et al., 2013) and provided about 20% of all dietary calories consumed globally (