Analysis of Pinaceae Gene Family Evolution Suggests Accelerated Gene Turnover in Pine Trees

Gene duplications and losses are major determinants of evolutionary change. Comparative genome-wide analyses of gene family evolution are often applied to infer patterns of gene turnover, i.e. gene gains and losses, across a range of species. Such investigations rely on gene annotations, which are often incomplete and partially inaccurate in draft genomes and transcriptomes. This issue is particularly relevant in species with large genomes (>10 Gb), including conifers. In this work we analyze gene family evolution in draft genomes of four conifers (loblolly and sugar pine, Norway spruce and Douglas-fir) using the likelihood framework implemented in the CAFE software, which allows estimating gene turnover rates and patterns in a species phylogeny. After grouping all annotated genes in orthogroups with OrthoFinder, we selected 16,118 gene families (~24,000-28,000 genes per species) occurring in at least two species for downstream analysis. The CAFE analyses indicated that gene turnover is at least twice as high in the two pines (~110 gene gains and/or losses per million years) compared to Norway spruce and Douglas-fir, even after correcting for possible annotation errors and for the presence of multiple pine species in our dataset. We also identified 1,192 gene families with significant expansion or contraction changes, and a high proportion of gene duplications vs. gene losses in Douglas-fir. Overall, our results indicate that no less than 1/5 of all gene families experienced gains and/or losses during the evolution of these Pinaceae. This extensive gene turnover has likely played a major role in conifer genome evolution and adaptation.