Evolution of Cold Acclimation and Its Role in Niche Transition in the Temperate Grass Subfamily Pooideae

Abstract

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.

Gene expression analysis of Cyanophora paradoxa reveals conserved abiotic stress responses between basal algae and flowering plants

“…This observation is also supported by the analysis of the most conserved families operating upon stress (Figs 6d, S9), in which we find several, mostly down-regulated photosynthesis and primary metabolism-related families. Similar trends have been found in grasses, where the various members of the family Pooideae showed highly diverse transcriptomic responses to cold stress, but a common down-regulation of transcripts involved in photosynthesis and metabolism (Schubert et al, 2019). Analysis of photosynthesis parameters during salt stress revealed that this is reflected by a decrease in the total performance index of photosynthesis in multiple species (Pavlovi c et al, 2019), showing a correlation between the transcript responses and plant phenotype.…”

“…5d). Similar trends have been found in grasses, where the various members of the family Pooideae showed highly diverse transcriptomic responses to cold stress, but a common down-regulation of transcripts involved in photosynthesis and metabolism (Schubert et al, 2019). Similar trends have been found in grasses, where the various members of the family Pooideae showed highly diverse transcriptomic responses to cold stress, but a common down-regulation of transcripts involved in photosynthesis and metabolism (Schubert et al, 2019).…”

The grass subfamily Pooideae: Cretaceous–Palaeocene origin and climate‐driven Cenozoic diversification

“…In a study of three Pooideae species, Zhong, Robbett, Poire, & Preston () identified several gene clusters exhibiting conserved cold response, many of which had previously been characterized as ancient stress response genes. Another study found 16 cold‐responsive genes that exhibited conserved expression in five distantly related Pooideae species (Schubert, Grønvold, Sandve, Hvidsten, & Fjellheim, ). Interestingly, most of these genes were induced in response to short‐term cold and are known to be stress responsive in other angiosperms.…”

“…Our findings corroborate recent studies of molecular evolution of cold adaptation. Although all species from distantly related Pooideae lineages are able to acclimatize to cold, most of the cold-responsive genes identified by Schubert et al, (2019) were differentially expressed in only one of five investigated species representing different tribes.…”

“…Nonetheless, our ASRs of these (extrinsic) traits are not able to distinguish convergent and parallel evolution, which increases the uncertainty of inferred states on ancestral nodes. The abundance of frost-experiencing taxa in all tribes suggests, however, that their ancestors possessed features that allowed them to evolve cold adaptation, which is supported by the 16 cold-responsive genes shared by five distantly related Pooideae species identified by Schubert et al (2019).…”