Pinaceae show elevated rates of gene duplication and gene loss that are robust to incomplete gene annotation

Abstract

Gene duplications and gene losses are major determinants of genome evolution and phenotypic diversity. The frequency of gene turnover (gene gains and gene losses combined) is known to vary between organisms. Comparative genomic analyses of gene families can highlight such variation; however, estimates of gene turnover rates may be biased when using highly fragmented genome assemblies resulting in poor gene annotations. Here, we address potential biases introduced by gene annotation errors in estimates of gene turnover frequencies in a dataset including both well-annotated angiosperm genomes and the incomplete gene sets of four Pinaceae including two pine species, Norway spruce and Douglas-fir. Previous studies have shown low overall substitution rates, but higher levels of adaptive substitutions, in genes from Pinaceae and other gymnosperms compared to angiosperms. Conversely, our analysis suggests that pines experienced higher gene turnover rates than angiosperm lineages lacking recent whole-genome duplications. This finding is robust to both known major issues in Pinaceae gene sets: missing gene models and erroneous annotation of pseudogenes. A separate analysis limited to the four Pinaceae gene sets confirmed an accelerated gene turnover rate in pines compared to Norway spruce and Douglas-fir. Our results indicate that gene turnover significantly contributes to genome variation and possibly to adaptation and speciation in Pinaceae. Moreover, these findings indicate that reliable estimates of gene turnover frequencies can be discerned in incomplete and potentially inaccurate gene sets.