Enhanced genome integrity maintenance and few directly stress-mitigating alterations in extreme habitat-adapted Arabidopsis halleri

Abstract Heavy 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.