Genomic basis of adaptation to serpentine soil in two Alyssum species shows convergence with Arabidopsis across 20 million years of divergence.

Background and aims: Serpentine outcrops, characterized by low nutrient availability, high heavy metal concentrations, propensity to drought, and island-like distributions, offer valuable systems to study parallelisms in repeated adaptation to extreme environments. While shared phenotypic manifestation of adaptation to serpentine environments has been investigated in many species, it is still unclear whether there may be a common genetic basis underlying such responses. Here we assess local adaptation to serpentine soil and infer the parallel genetic signatures of local adaptation to serpentine environments in two thus far unexplored closely related species, Alyssum gmelinii and Alyssum spruneri (Brassicaceae). Then we measure gene- and function-level convergence with the previously explored Arabidopsis arenosa, to reveal candidate shared adaptive strategies within Brassicaceae.

Methods: We tested for adaptation using a reciprocal substrate-transplant experiment in A. gmelinii. Then, after assembling a reference genome, we generated population-level sequencing data of four population pairs and performed genome scans for directional selection to infer serpentine adaptive candidate genes in Alyssum. Finally, we compared candidate gene lists with those inferred in similar experiments in Arabidopsis arenosa and used protein-protein interaction networks to discern functional convergence in serpentine adaptation.

Key results: Independent colonization of serpentine environments by Alyssum populations is associated with footprints of selection on genes related to ion transport and homeostasis, nutrient and water uptake, and life-history traits related to germination and reproduction. Reciprocal transplant experiments demonstrated that adapted plants germinate sooner and exhibit better growth in serpentine conditions while excluding heavy metals and increasing Ca uptake in their tissues. Finally, a significant fraction of such genes and molecular pathways is shared with Arabidopsis arenosa.

Conclusions: We show that genetic adaptation to the multi-factorial challenge imposed by serpentine environments involves key pathways that are shared not only between closely related species, but also between Brassicaceae tribes of ∼20 Mya divergence.