Adaptation to toxic serpentine soils


Adaptation represents key evolutionary mechanism, which allows species and populations to succeed in a variable environment. Hostile serpentine (in a broader sense ultramafic) soils are among the strongest triggers for adaptation in plants. 

This chemically extreme substrate provides multiple challenges to plant life, including extremely low Ca:Mg ratio and elevated levels of toxic metals. Therefore, serpentine barrens provide a powerful model for studying multi-challenge adaptations. Moreover, the island-like distribution of serpentine soils can trigger parallel evolution at the level of both genome and phenotype.

We are using serpentine plants as models to study mechanisms underlying repeated adaptation in plants. In the ongoing ConAdapt project, we address mechanisms of serpentine adaptation and uncover their convergent genetic basis across European Brassicaceae species, with primary focus on Balkan peninsula. We collaborate with many colleagues focusing on serpentine flora and mechanisms of metal hyperaccumulation and ultramafic adaptation, in particular Sylvain Merlot (U Toulouse), Ute Krämer (Ruhr U Bochum), Mark Aarts and Anthony van der Ent (Wageningen U), Tomica Mišljenović (U Belgrade), Panayiotis Dimitrakopoulos (Aegean U, Lesbos) and Edita Tylová (Charles U Prague).


Serpentine adaptation in Arabidopsis arenosa

We assessed evolutionary sources of adaptive variation in lineages with doubled genomes, using autotetraploid Arabidopsis arenosa, which repeatedly adapted to naturally toxic serpentine soils. First, we combined demographic analysis and transplant experiments to demonstrate rapid parallel adaptation to five serpentine barrens. We identified shared  candidate genes for selection, functionally relevant to serpentines, e.g. genes, which are involved in dehydration tolerance and ion homeostasis. 

Then, we modelled parallel selection and infer dominant role of sampling from a shared pool of alleles across the variable tetraploid populations. However, we also discovered an exceptional locus with parallel de novo mutations! It encodes a central transporter TPC1 protein, shown to act as a global hub mediating stress signalling, with two distinct serpentine-specific mutations in otherwise conserved site at calcium selectivity gate.

Our finding demonstrates that large pool of pre-existing variation is the major source of adaptive alleles in autotetraploids. However, rapid selection on de novo mutations is still feasible, altogether indicating broad evolutionary flexibility of lineages with doubled genomes. Now we floow up on this research by targeted functional validations of importand gene canddiates, in collaboration with molecular geneticists and extend to other Arabidopsis (A. lyrata) and Brassicaceae to learn more about mechanisms underlying genetic convergence.