Cited by 13Protist diversity and phylogenyMarine and coastal plant biologyChromosomal and Genetic Variations

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

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Ochiai, Kanta K., Hanawa, Daiki, Ogawa, Harumi A., Tanaka, Hiroyuki, Uesaka, Kazuma, Edzuka, Tomoya, Shirae‐Kurabayashi, Maki, Toyoda, Atsushi +2 more·2024·The Plant Journal

Abstract

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.

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Crossref · 10.1111/tpj.16764

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  • Canonical anterograde organelle transporters known in plants and animals (kinesin-1, kinesin-3, and kinesin-ARK) are missing in Bryopsis.

    “Furthermore, canonical anterograde organelle transporters known in plants and animals (kinesin‐1, kinesin‐3, and kinesin‐ARK) are missing in Bryopsis, although chloroplasts”

    From <scp>RNAi</scp> reveals a unique set of kinesins mediating chloroplast motility in the giant cytoplasm of <i>Bryopsis</i> (Ulvophyceae), a coenocytic green alga (2026) · cites this paper as Ochiai et al., 2024

    The Kinesin-ARK section says that orthologous genes for candidate anterograde transporters are missing in Bryopsidales, which includes Bryopsis. It identifies kinesin-1 as an animal transporter but does not state that kinesin-1 or kinesin-3 is missing in Bryopsis; a search for kinesin-3 found no such statement. The claim's full three-part list is therefore not supported by our copy. (LLM, conf=0.82)

    Experimental — accuracy not yet measured
  • Actin appears dispensable for chloroplast motility in at least some Bryopsis strains.

    “In land plants, actin generally plays a dominant role in organelle transport; however, a kinesin‐like protein (KAC), which is critical for actin‐based chloroplast motility in land plants, is absent from the Bryopsis genome, and actin appears to be dispensable for chloroplast motility, at least in some Bryopsis strains (Mizukami & Wada, 1981; Ochiai et al., 2024; Suetsugu et al., 2010).”
  • Coenocytic green algae possess kinesin genes that are thought to be specialized for cytokinesis in land plants despite lacking cytokinesis.

    “Surprisingly, comparative genomic analysis of motor proteins revealed that despite the lack of cytokinesis, coenocytic green algae possess kinesin genes that are thought to be specialized for cytokinesis in land plants.”
  • The kinesin-like protein KAC, critical for actin-based chloroplast motility in land plants, is absent from the Bryopsis genome.

    “In land plants, actin generally plays a dominant role in organelle transport; however, a kinesin‐like protein (KAC), which is critical for actin‐based chloroplast motility in land plants, is absent from the Bryopsis genome, and actin appears to be dispensable for chloroplast motility, at least in some Bryopsis strains (Mizukami & Wada, 1981; Ochiai et al., 2024; Suetsugu et al., 2010).”

    From <scp>RNAi</scp> reveals a unique set of kinesins mediating chloroplast motility in the giant cytoplasm of <i>Bryopsis</i> (Ulvophyceae), a coenocytic green alga (2026) · cites this paper as Ochiai et al., 2024

    The Kinesin-ARK section says that ARK-like orthologous genes are missing in Bryopsidales, but it does not identify them as KAC. The chloroplast-motility section reports actin-independent movement in Bryopsis; neither section says KAC is absent from its genome or describes KAC’s role in land plants (searched: KAC and kinesin-like protein KAC). (LLM, conf=0.76)

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Cites

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Research works printed but not linked: 19

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Authors
Ochiai, K. K., Hanawa, D., Ogawa, H. A., Tanaka, H., Uesaka, K., Edzuka, T., Shirae‐Kurabayashi, M., Toyoda, A., Itoh, T., & Goshima, G.
Affiliations
  • Nagoya University (JP)
  • Tokyo Institute of Technology (JP)
  • Center for Gene Research, Nagoya University (JP)
  • National Institute of Genetics (JP)
Corresponding author
  • Itoh, Takehiko
  • Goshima, Gohta
Venue
The Plant Journal
Publisher
Wiley
Published
2024-04-20
Volume
119
Issue
2
Pages
1091-1111
ISSN
  • 0960-7412 (ISSN-L)
  • 1365-313X
OpenAlex
W4394974440
Cited by
13
References
4
Citations by year
2026: 4 · 2025: 8 · 2024: 1
FWCI
1.77
Type
journal article
Language
en
Open access
Locations
  • The Plant Journal (publishedVersion)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc)
  • PubMed (publishedVersion)
  • Tokyo Tech Research Repository (Tokyo Institute of Technology) (submittedVersion)
Funders
Japan Society for the Promotion of Science (16H06279, 22K19308, 22H04717, 22H02644)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protist diversity and phylogeny
  • Physical Sciences › Earth and Planetary Sciences › Oceanography › Marine and coastal plant biology
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
Keywords
Bryopsis, Bryopsidales, regeneration, nuclear genome assembly, genome annotation, kinesin, myosin, microtubules, comparative genomics, Ulvophyceae
MeSH terms
Chlorophyta, Myosins, Phylogeny, Regeneration, Kinesins, Genome, Plant, Bryopsida

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