Abstract
Gapless, chromosome-level assemblies provide unparalleled resolution for studying the architecture and evolution of genomes. We produced new telomere-to-telomere genome assemblies for five strains representing four species from the plant-pathogenic fungal genus Alternaria, focusing on section Alternaria. These new genomic resources were combined with seven previously published assemblies, allowing for detailed comparative analyses of genome architecture, chromosome structure and associated evolutionary dynamics. All strains possessed a stable complement of ten core chromosomes with highly conserved macrosynteny; only a few large-scale structural rearrangements were observed. Consensus genomic features, such as chromosome length, centromeres, subtelomeres, GC composition, gene density and repetitive content, were characterized in depth and were highly similar in most genomes. A metric for quantifying inter-genomic orthogroup retention revealed a consistent gradient of elevated homologue gain/loss toward chromosome ends. The increased rate of gene turnover is an inherent property of these dynamic regions and is not driven by the enrichment of certain functional classes of embedded genes. Despite the plasticity of chromosome ends, multiple complementary analyses found no evidence for physical or functional bipartite (or 'two-speed') compartmentalization as a whole. For example, candidate effector genes did not display biased localization to gene-sparse regions. Collectively, our results demonstrate that Alternaria section Alternaria has a conserved, stable genomic architecture yet retains evolutionarily dynamic regions localized to chromosomal termini. These gapless genomes provide a framework to support further studies on chromosomal evolution and pathogenicity-related diversification in this economically important fungal group.