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

Red seaweeds form part of an ancient lineage of eukaryotes that were one of the first to evolve multicellularity. Although red seaweeds share a common evolutionary origin with modern-day plants and display complex multicellular development, we still lack comprehensive genome data from the most highly-evolved groups. Here, we present a chromosome-level genome assembly of the complex red seaweed Bostrychia moritziana, a member of the largest and most diverse order of red algae called the Ceramiales. Contrary to the commonly held view that red algae generally have small genomes, we report significant genome size expansion in Bostrychia and other Ceramiales species, which we posit as one of at least three independent genome expansion events that occurred during red algal evolution. Our analyses suggest that these expansions do not involve polyploidy or ancient whole genome duplications, but in the case of Bostrychia appear to be largely driven by the dramatic proliferation of a single lineage of giant Plavaka DNA transposons. Consistent with increased genome size, we identify a substantial increase in gene content in Bostrychia that was shaped both by de novo gene emergence and by the amplification of gene families in common with other Ceramiales seaweeds, providing key insight into the genetic adaptations underpinning the evolutionary success of this species-rich order. Finally, our sex-specific assemblies enabled us to resolve the UV sex chromosomes in Bostrychia, which feature expanded gene-rich sex-linked regions. Notably, these sex-linked regions each harbour a distinct TALE-HD transcription factor orthologous to ancient regulators of haploid-diploid transitions in other multicellular lineages. Together, our findings offer unique perspectives into the genomic adaptations driving red algal diversity and demonstrate how this highly successful group of red seaweeds can provide insight into the evolutionary origins and common principles of complex multicellular plant life.

红海藻（red seaweeds）属于真核生物的古老演化支系，是最早演化出多细胞结构的类群之一。尽管红海藻与现代植物拥有共同的演化起源，且具备复杂的多细胞发育过程，但目前我们仍缺乏高度演化类群的完整基因组数据。本研究报道了复杂红藻莫氏串膜藻（Bostrychia moritziana）的染色体级基因组组装结果，该物种隶属于红藻中物种最丰富、多样性最高的仙菜目（Ceramiales）。与“红藻基因组普遍偏小”的主流观点相悖，本研究发现莫氏串膜藻及其他仙菜目物种存在显著的基因组大小扩张，我们推测这是红藻演化过程中至少三次独立的基因组扩张事件之一。分析表明，这些基因组扩张并非由多倍化或古老的全基因组复制事件导致，而就莫氏串膜藻而言，其基因组扩张主要由单个谱系的巨型Plavaka DNA转座子（Plavaka DNA transposons）的大规模增殖所驱动。与基因组增大的趋势一致，我们发现莫氏串膜藻的基因含量显著提升，这一过程由从头基因起源以及与其他仙菜目红藻共有的基因家族扩增共同塑造，为解析这个物种丰富的类群演化成功背后的遗传适应机制提供了关键见解。最后，本研究通过性别特异性组装，解析了莫氏串膜藻的UV性染色体，其特征为扩增的富含基因的性连锁区域。值得注意的是，这两个性连锁区域各自携带一个独特的TALE-HD转录因子（TALE-HD transcription factor），其与其他多细胞类群中单倍体-二倍体转换的古老调控因子互为同源基因。综上，本研究的发现为解析驱动红藻多样性的基因组适应机制提供了独特视角，并证明这类高度成功的红海藻类群，能够为复杂多细胞植物生命的演化起源及共性原则提供研究参考。