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Whole genome duplication (WGD) events have played a major role in eukaryotic genome evolution, but the consequence of these extreme events in adaptive genome evolution is still not well understood. To address this knowledge gap we used a comparative phylogenetic model and transcriptomic data from seven species to infer selection on gene expression in duplicated genes (ohnologs) following the salmonid WGD 80-100 million years ago. We find rare cases of tissue-specific expression evolution but pervasive expression evolution affecting many tissues, reflecting strong selection on maintenance of genome stability following genome doubling. Although ohnolog expression levels have evolved mostly asymmetrically, by diverting one ohnolog copy down a path towards pseudogenization, strong evolutionary constraints have frequently also favoured symmetric shifts in gene dosage of both copies, likely to achieve gene dose reduction while avoiding accumulation of ‘toxic mutations’. Mechanistically, ohnolog regulatory divergence is dictated by the number of bound transcription factors in promoters, with transposable elements being one source of novel binding sites driving tissue-specific gains in expression. Our results imply pervasive adaptive expression evolution following WGD to overcome the immediate challenges posed by genome doubling and to exploit the long-term genetic opportunities for novel phenotype evolution.

The grass subfamily Pooideae dominates the grass floras in cold temperate regions and has evolved complex physiological adaptations to cope with extreme environmental conditions like frost, winter, and seasonality. One such adaptation is cold acclimation, wherein plants increase their frost tolerance in response to gradually falling temperatures and shorter days in the autumn. However, understanding how complex traits like cold acclimation evolve remains a major challenge in evolutionary biology. Here, we investigated the evolution of cold acclimation in Pooideae and found that a phylogenetically diverse set of Pooideae species displayed cold acclimation capacity. However, comparing differential gene expression after cold treatment in transcriptomes of five phylogenetically diverse species revealed widespread species-specific responses of genes with conserved sequences. Furthermore, we studied the correlation between gene family size and number of cold-responsive genes as well as between selection pressure on coding sequences of genes and their cold responsiveness. We saw evidence of protein-coding and regulatory sequence evolution as well as the origin of novel genes and functions contributing toward evolution of a cold response in Pooideae. Our results reflect that selection pressure resulting from global cooling must have acted on already diverged lineages. Nevertheless, conservation of cold-induced gene expression of certain genes indicates that the Pooideae ancestor may have possessed some molecular machinery to mitigate cold stress. Evolution of adaptations to seasonally cold climates is regarded as particularly difficult. How Pooideae evolved to transition from tropical to temperate biomes sheds light on how complex traits evolve in the light of climate changes.

In the past 50 million years climate cooling has triggered the expansion of temperate biomes. During this period, many extant plant lineages in temperate biomes evolved from tropical ancestors and adapted to seasonality and cool conditions. Among the Poaceae (grass family), one of the subfamilies that successfully shifted from tropical to temperate biomes is the Pooideae (temperate grasses). Subfamily Pooideae contains the most important crops cultivated in the temperate regions including wheat (Triticum aestivum) and barley (Hordeum vulgare). Due to the need of well-adapted cultivars, extensive research has produced a large body of knowledge about the mechanisms underlying cold adaptation in cultivated Pooideae species. Especially cold acclimation, a process which increases the frost tolerance during a period of non-freezing cold, plays an important role. Because cold adaptation is largely unexplored in lineages that diverged early in the evolution of the Pooideae, little is known about the evolutionary history of cold acclimation in the Pooideae. Here we test if several species of early diverging lineages exhibit increased frost tolerance after a period of cold acclimation. We further investigate the conservation of five well-studied gene families that are known to be involved in the cold acclimation of Pooideae crop species. Our results indicate that cold acclimation exists in early diverging lineages, but that genes involved in regulation of cold acclimation are not conserved. The investigated gene families show signs of lineage-specific evolution and support the hypothesis that gene family expansion is an important mechanism in adaptive evolution.