The expanded Bostrychia moritziana genome unveils evolution in the most diverse and complex order of red algae.

Abstract

Red algae are an ancient eukaryotic lineage that were among the first to evolve multicellularity. Although they share a common origin with modern-day plants and display complex multicellular development, comprehensive genome data from the most highly evolved red algal groups remain scarce. Here, we present a chromosome-level genome assembly of Bostrychia moritziana, a complex red seaweed in the Rhodomelaceae family of the Ceramiales-the largest and most diverse order of red algae. Contrary to the view that red algal genomes are typically small, we report significant genome size expansion in Bostrychia and other Ceramiales, which represents one of at least three independent expansion events in red algal evolution. Our analyses suggest that these expansions do not involve polyploidy or ancient whole-genome duplications, but in Bostrychia rather stem from the proliferation of a single lineage of giant Plavaka DNA transposons. Consistent with its enlarged genome, Bostrychia has an increased gene content shaped by de novo gene emergence and amplified gene families in common with other Ceramiales, providing insight into the genetic adaptations underpinning this successful and species-rich order. Finally, our sex-specific assemblies resolve the UV sex chromosomes in Bostrychia, which feature expanded gene-rich sex-linked regions. Notably, each sex chromosome harbors a three amino acid loop extension homeodomain (TALE-HD) transcription factor orthologous to ancient regulators of haploid-diploid transitions in other multicellular lineages. Together, our findings offer a unique perspective of the genomic adaptations driving red algal diversity and demonstrate how this red seaweed lineage can provide insight into the evolutionary origins and universal principles underpinning complex multicellularity.