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Premetazoan genome evolution and the regulation of cell differentiation in the choanoflagellate Salpingoeca rosetta

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Fairclough, Stephen R, Chen, Zehua, Kramer, Eric, Zeng, Qiandong, Young, Sarah, Robertson, Hugh M, Begovic, Emina, Richter, Daniel J, Russ, Carsten, Westbrook, M Jody, Manning, Gerard, Lang, B Franz, Haas, Brian, Nusbaum, Chad, King, Nicole·2013·Genome Biology

Abstract

Background: Metazoan multicellularity is rooted in mechanisms of cell adhesion, signaling, and differentiation that first evolved in the progenitors of metazoans. To reconstruct the genome composition of metazoan ancestors, we sequenced the genome and transcriptome of the choanoflagellate Salpingoeca rosetta, a close relative of metazoans that forms rosette-shaped colonies of cells. Results: A comparison of the 55 Mb S. rosetta genome with genomes from diverse opisthokonts suggests that the origin of metazoans was preceded by a period of dynamic gene gain and loss. The S. rosetta genome encodes homologs of cell adhesion, neuropeptide, and glycosphingolipid metabolism genes previously found only in metazoans and expands the repertoire of genes inferred to have been present in the progenitors of metazoans and choanoflagellates. Transcriptome analysis revealed that all four S. rosetta septins are upregulated in colonies relative to single cells, suggesting that these conserved cytokinesis proteins may regulate incomplete cytokinesis during colony development. Furthermore, genes shared exclusively by metazoans and choanoflagellates were disproportionately upregulated in colonies and the single cells from which they develop. Conclusions: The S. rosetta genome sequence refines the catalog of metazoan-specific genes while also extending the evolutionary history of certain gene families that are central to metazoan biology. Transcriptome data suggest that conserved cytokinesis genes, including septins, may contribute to S. rosetta colony formation and indicate that the initiation of colony development may preferentially draw upon genes shared with metazoans, while later stages of colony maturation are likely regulated by genes unique to S. rosetta.

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Metadata

Authors
Fairclough, S. R., Chen, Z., Kramer, E., Zeng, Q., Young, S., Robertson, H. M., Begovic, E., Richter, D. J., Russ, C., Westbrook, M. J., Manning, G., Lang, B. F., Haas, B., Nusbaum, C., & King, N.
Venue
Genome Biology
Published
2013-02-18
Volume
14
Issue
2
Pages
R15-R15
ISSN
  • 1465-6906 (ISSN-L)
  • 1474-760X
OpenAlex
W2140304975
Cited by
287
References
16
FWCI
17.10
Type
journal article
Language
en
Open access
gold
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CoChat. (2026). Citation check: Premetazoan genome evolution and the regulation of cell differentiation in the choanoflagellate Salpingoeca rosetta. https://app.cochat.ai/papers/10.1186/gb-2013-14-2-r15
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Fairclough, S. R., Chen, Z., Kramer, E., Zeng, Q., Young, S., Robertson, H. M., Begovic, E., Richter, D. J., Russ, C., Westbrook, M. J., Manning, G., Lang, B. F., Haas, B., Nusbaum, C., & King, N. (2013). Premetazoan genome evolution and the regulation of cell differentiation in the choanoflagellate Salpingoeca rosetta. Genome Biology. https://doi.org/10.1186/gb-2013-14-2-r15

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