Genome sequence and cell biological toolbox of the highly regenerative, coenocytic green feather alga Bryopsis

• Published in: The Plant journal : for cell and molecular biology Vol. 119; no. 2; pp. 1091 - 1111
• Main Authors: Ochiai, Kanta K., Hanawa, Daiki, Ogawa, Harumi A., Tanaka, Hiroyuki, Uesaka, Kazuma, Edzuka, Tomoya, Shirae‐Kurabayashi, Maki, Toyoda, Atsushi, Itoh, Takehiko, Goshima, Gohta
• Format: Journal Article
• Language: English
• Published: England Blackwell Publishing Ltd 01-07-2024
• Subjects: Actin; Algae; Annotations; Aquatic plants; Biology; Bryopsis; Chemical analysis; chloroplast transport; Chloroplasts; coenocyte; Cytokinesis; Cytoplasm; Experimental research; Feathers; Gene duplication; Genes; Genomes; Genomic analysis; Kinesin; lectin; marine macroalgae; Microtubules; Myosin; Nuclear division; Nucleotide sequence; Physical characteristics; Protoplasts; Regeneration; Seawater; SNAP receptors; Thallus; Water analysis; marine macroalgae; regeneration; kinesin; lectin; chloroplast transport; Bryopsis; coenocyte
• ISSN: 0960-7412; 1365-313X; 1365-313X
• DOI: 10.1111/tpj.16764

SUMMARY
Green feather algae (Bryopsidales) undergo a unique life cycle in which a single cell repeatedly executes nuclear division without cytokinesis, resulting in the development of a thallus (>100 mm) with characteristic morphology called coenocyte. Bryopsis is a representative coenocytic alga that has exceptionally high regeneration ability: extruded cytoplasm aggregates rapidly in seawater, leading to the formation of protoplasts. However, the genetic basis of the unique cell biology of Bryopsis remains poorly understood. Here, we present a high‐quality assembly and annotation of the nuclear genome of Bryopsis sp. (90.7 Mbp, 27 contigs, N50 = 6.7 Mbp, 14 034 protein‐coding genes). Comparative genomic analyses indicate that the genes encoding BPL‐1/Bryohealin, the aggregation‐promoting lectin, are heavily duplicated in Bryopsis, whereas homologous genes are absent in other ulvophyceans, suggesting the basis of regeneration capability of Bryopsis. Bryopsis sp. possesses >30 kinesins but only a single myosin, which differs from other green algae that have multiple types of myosin genes. Consistent with this biased motor toolkit, we observed that the bidirectional motility of chloroplasts in the cytoplasm was dependent on microtubules but not actin in Bryopsis sp. Most genes required for cytokinesis in plants are present in Bryopsis, including those in the SNARE or kinesin superfamily. Nevertheless, a kinesin crucial for cytokinesis initiation in plants (NACK/Kinesin‐7II) is hardly expressed in the coenocytic part of the thallus, possibly underlying the lack of cytokinesis in this portion. The present genome sequence lays the foundation for experimental biology in coenocytic macroalgae.
Significance Statement
The exceptionally coenocytic body and remarkable regeneration ability of Bryopsis have attracted biologists for years. However, molecular biological tools remain underdeveloped, partly due to the lack of genome information. Here, we report high‐quality assembly and annotation of the genome, providing a crucial resource for experimental biology and genomics studies of Bryopsis. Furthermore, comparative genomic analysis reveals a unique gene repertoire that possibly underlies the highly regenerative coenocytic body.