Genomic Architecture and Evolution of the Gene Superfamily As Revealed by Phylogenomic Analysis

The superfamily synthesizes cellulose and different hemicellulosic polysaccharides in plant cell walls. While much has been discovered about the evolution and function of these genes, their genomic architecture and relationship with gene (sub-)functionalization and evolution remains unclear. By using 242 genomes covering plant evolution from green algae to eudicots, we performed a large-scale analysis of synteny, phylogenetic, and functional data of the superfamily. Results revealed considerable gene copy number variation across species and gene families, and also two patterns - singletons vs. tandem arrays - in chromosomic gene arrangement. Synteny analysis revealed exceptional conservation of gene architecture across species, but also lineage-specific patterns across gene (sub-)families. Synteny patterns correlated with gene sub-functionalization into primary and secondary and distinct CslD functional isoforms. Furthermore, a genomic context shift of a group of cotton secondary was associated with peculiar properties of cotton fiber synthesis. Finally, phylogenetics suggested that primary sequences appeared before the secondary , while phylogenomic analyses unveiled the genomic trace of the duplication that initiated the family. Our results describe in detail the genomic architecture of the superfamily in plants, highlighting its crucial relevance for gene diversification and sub-functionalization, and for understanding their evolution.