Network-based microsynteny analysis identifies major differences and genomic outliers in mammalian and angiosperm genomes

A comprehensive analysis of relative gene order, or microsynteny, can provide valuable information for understanding the evolutionary history of genes and genomes, and ultimately traits and species, across broad phylogenetic groups and divergence times. We have used our network-based phylogenomic synteny analysis pipeline to first analyze the overall patterns and major differences between 87 mammalian and 107 angiosperm genomes. These two important groups have both evolved and radiated over the last ∼170 MYR. Secondly, we identified the genomic outliers or “rebel genes” within each clade. We theorize that rebel genes potentially have influenced trait and lineage evolution. Microsynteny networks use genes as nodes and syntenic relationships between genes as edges. Networks were decomposed into clusters using the Infomap algorithm, followed by phylogenomic copy-number profiling of each cluster. The differences in syntenic properties of all annotated gene families, including BUSCO genes, between the two clades are striking: most genes are single copy and syntenic across mammalian genomes, whereas most genes are multicopy and/or have lineage-specific distributions for angiosperms. We propose microsynteny scores as an alternative and complementary metric to BUSCO for assessing genome assemblies. We further found that the rebel genes are different between the two groups: lineage-specific gene transpositions are unusual in mammals, whereas single-copy highly syntenic genes are rare for flowering plants. We illustrate several examples of mammalian transpositions, such as brain-development genes in primates, and syntenic conservation across angiosperms, such as single-copy genes related to photosynthesis. Future experimental work can test if these are indeed rebels with a cause.