The bimodal distribution of genic GC content is ancestral to monocot species

In grasses such as rice or maize, the distribution of genic GC content is well known to be bimodal. It is mainly driven by GC content at third codon positions (GC3 for short). This feature is thought to be specific to grasses as closely related species like banana have a unimodal GC3 distribution. GC3 is associated with numerous genomics features and uncovering the origin of this peculiar distribution will help understanding the potential roles and consequences of GC3 variations within and between genomes. Until recently, the origin of the peculiar GC3 distribution in grasses has remained unknown. Thanks to the recent publication of several complete genomes and transcriptomes of nongrass monocots, we studied more than 1,000 groups of one-to-one orthologous genes in seven grasses and three outgroup species (banana, palm tree, and yam). Using a maximum likelihood-based method, we reconstructed GC3 at several ancestral nodes. We found that the bimodal GC3 distribution observed in extant grasses is ancestral to both grasses and most monocot species, and that other species studied here have lost this peculiar structure. We also found that GC3 in grass lineages is globally evolving very slowly and that the decreasing GC3 gradient observed from 5' to 3' along coding sequences is also conserved and ancestral to monocots. This result strongly challenges the previous views on the specificity of grass genomes and we discuss its implications for the possible causes of the evolution of GC content in monocots.