The link between ancient whole-genome duplications and cold adaptations in the Caryophyllaceae.

Premise: The Caryophyllaceae (the carnation family) have undergone multiple transitions into colder climates and convergence on cushion plant adaptation, indicating that they may provide a natural system for cold adaptation research. Previous research has suggested that putative ancient whole-genome duplications (WGDs) are correlated with niche shifts into colder climates across the Caryophyllales. Here, we explored the genomic changes potentially involved in one of these discovered shifts in the Caryophyllaceae.

Methods: We constructed a data set combining 26 newly generated transcriptomes with 45 published transcriptomes, including 11 cushion plant species across seven genera. With this data set, we inferred a dated phylogeny for the Caryophyllaceae and mapped ancient WGDs and gene duplications onto the phylogeny. We also examined functional groups enriched for gene duplications related to the climatic shift.

Results: The ASTRAL topology was mostly congruent with the current consensus of relationships within the family. We inferred 15 putative ancient WGDs in the family, including eight that have not been previously published. The oldest ancient WGD (ca. 64.4-56.7 million years ago), WGD1, was found to be associated with a shift into colder climates by previous research. Gene regions associated with ubiquitination were overrepresented in gene duplications retained after WGD1 and those convergently retained by cushion plants in Colobanthus and Eremogone, along with other functional annotations.

Conclusions: Gene family expansions induced by ancient WGDs may have contributed to the shifts to cold climatic niches in the Caryophyllaceae. Transcriptomic data are crucial resources that help unravel heterogeneity in deep-time evolutionary patterns in plants.