A segmental duplication in the common ancestor of Brassicaceae is responsible for the origin of the paralogs KCS6-KCS5, which are not shared with other angiosperms

Abstract

Novel morphological structures allowed adaptation to dry conditions in early land plants. The cuticle, one such novelty, plays diverse roles in tolerance to abiotic and biotic stresses and plant development. Cuticular waxes represent a major constituent of the cuticle and are comprised of an assortment of chemicals that include, among others, very long chain fatty acids (VLCFAs). Members of the β-ketoacyl coenzyme A synthases (KCS) gene family code for enzymes that are essential for fatty acid biosynthesis. The gene KCS6 (CUT1) is known to be a key player in the production of VLCFA precursors essential for the synthesis of cuticular waxes in the model plant Arabidopsis thaliana (Brassicaceae). Despite its functional importance, relatively little is known about the evolutionary history of KCS6 or its paralog KCS5 in Brassicaceae or beyond. This lacuna becomes important when we extrapolate understanding of mechanisms gained from the model plant to its containing clades Brassicaceae, flowering plants, or beyond. The Brassicaceae, with several sequenced genomes and a known history of paleoploidy, mesopolyploidy and neopolyploidy, offer a system in which to study the evolution and diversification of the KCS6-KCS5 paralogy. Our phylogenetic analyses across green plants, combined with comparative genomic, microsynteny and evolutionary rates analyses across nine genomes of Brassicaceae, reveal that (1) the KCS6-KCS5 paralogy arose as the result of a large segmental duplication in the ancestral Brassicaceae, (2) the KCS6-KCS5 lineage is represented by a single copy in other flowering plant lineages, (3) the duplicated segments undergo different degrees of retention and loss, and (4) most of the genes in the KCS6 and KCS5 gene blocks (including KCS6 and KCS5 themselves) are under purifying selection. The last also true for most members of the KCS gene family in Brassicaceae, except for KCS8, KCS9 and KCS17, which are under positive selection and may be undergoing functional evolution, meriting further investigation. Overall, our results clearly establish that the ancestral KCS6/5 gene duplicated in the Brassicaceae lineage. It is possible that any specialized functions of KCS5 found in Brassicaceae are either part of a set of KCS6/5 gene functions in the rest of the flowering plants, or unique to Brassicaceae.