Chromatin dynamics of a large-sized genome provides insights into polyphenism and X0 dosage compensation of locusts

Locusts are characterized by a large genome size, polyphenism and an X0 sex determination system. Here we generated chromosome-level genomes for both desert and migratory locusts, as well as a comprehensive chromatin map for the latter. We found that genome enlargement is associated with an increased number of enhancers in expanded intronic regions. To explore the function of expanded enhancers, we identified a distal enhancer that contributes to behavioral differences between solitary and gregarious locusts. In the X0 sex system, H4K16ac enrichment and H4K20me1 depletion maintain balanced X-linked expression in male soma. Notably, the distance-dependent H4K16ac enrichment diminishes gradually in intergenic regions, revealing a special dosage compensation mechanism in large genomes. Furthermore, the distance-dependent H4K16ac results in a lag in the evolution of dosage compensation for the X-linked genes translocated recently from autosomes. Therefore, expanded intronic and intergenic regions shape a distinct chromatin regulation landscape in large genomes. Chromosome-level genome assemblies of migratory and desert locusts, coupled with epigenomic profiling of migratory locusts, reveal chromatin dynamics underlying polyphenism and X-linked dosage compensation following autosomal gene translocation.