Evolution of a distinct chromatin regulatory landscape in brown algae

Abstract Chromatin structure plays a central role in regulating transcription, genome stability and epigenetic inheritance in eukaryotes. Much of our understanding of chromatin architecture and histone post-translational modifications (hPTMs) comes from a narrow set of animal and plant models, but emerging data from non-model lineages are challenging canonical views of how chromatin functions across the tree of life. Brown algae are complex multicellular eukaryotes that provide a unique perspective on chromatin evolution given their independent origin of complex multicellularity. Here we compile the chromatin toolkit of brown algae and show that canonical silencing systems involving DNA cytosine methylation and Polycomb repressive complex 2 (PRC2)-mediated histone H3 lysine 27 (H3K27) methylation were lost early in their evolution. By generating hPTM profiles from diverse brown algal clades, we resolve the nature and regulatory roles of chromatin states in this lineage and show how H3 lysine 79 (H3K79) methylation emerged and diversified as a repressive system. We further uncover sex-specific reconfigurations in species with varying degrees of sexual dimorphism and reconstruct the ancestral regulatory landscape that probably preceded the emergence of brown algae. Together, our findings illuminate the dynamic evolution of chromatin regulation in a distinct multicellular lineage and challenge assumptions about the universality of chromatin-based mechanisms across eukaryotes.