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Genome sequencing of the multicellular alga Astrephomene provides insights into convergent evolution of germ-soma differentiation

Germ-soma differentiation evolved independently in many eukaryotic lineages and contributed to complex multicellular organizations. However, the molecular genetic bases of such convergent evolution remain unresolved. Two multicellular volvocine green algae, Volvox and Astrephomene, exhibit convergen...

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Autores principales: Yamashita, Shota, Yamamoto, Kayoko, Matsuzaki, Ryo, Suzuki, Shigekatsu, Yamaguchi, Haruyo, Hirooka, Shunsuke, Minakuchi, Yohei, Miyagishima, Shin-ya, Kawachi, Masanobu, Toyoda, Atsushi, Nozaki, Hisayoshi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8608804/
https://www.ncbi.nlm.nih.gov/pubmed/34811380
http://dx.doi.org/10.1038/s41598-021-01521-x
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author Yamashita, Shota
Yamamoto, Kayoko
Matsuzaki, Ryo
Suzuki, Shigekatsu
Yamaguchi, Haruyo
Hirooka, Shunsuke
Minakuchi, Yohei
Miyagishima, Shin-ya
Kawachi, Masanobu
Toyoda, Atsushi
Nozaki, Hisayoshi
author_facet Yamashita, Shota
Yamamoto, Kayoko
Matsuzaki, Ryo
Suzuki, Shigekatsu
Yamaguchi, Haruyo
Hirooka, Shunsuke
Minakuchi, Yohei
Miyagishima, Shin-ya
Kawachi, Masanobu
Toyoda, Atsushi
Nozaki, Hisayoshi
author_sort Yamashita, Shota
collection PubMed
description Germ-soma differentiation evolved independently in many eukaryotic lineages and contributed to complex multicellular organizations. However, the molecular genetic bases of such convergent evolution remain unresolved. Two multicellular volvocine green algae, Volvox and Astrephomene, exhibit convergent evolution of germ-soma differentiation. The complete genome sequence is now available for Volvox, while genome information is scarce for Astrephomene. Here, we generated the de novo whole genome sequence of Astrephomene gubernaculifera and conducted RNA-seq analysis of isolated somatic and reproductive cells. In Volvox, tandem duplication and neofunctionalization of the ancestral transcription factor gene (RLS1/rlsD) might have led to the evolution of regA, the master regulator for Volvox germ-soma differentiation. However, our genome data demonstrated that Astrephomene has not undergone tandem duplication of the RLS1/rlsD homolog or acquisition of a regA-like gene. Our RNA-seq analysis revealed the downregulation of photosynthetic and anabolic gene expression in Astrephomene somatic cells, as in Volvox. Among genes with high expression in somatic cells of Astrephomene, we identified three genes encoding putative transcription factors, which may regulate somatic cell differentiation. Thus, the convergent evolution of germ-soma differentiation in the volvocine algae may have occurred by the acquisition of different regulatory circuits that generate a similar division of labor.
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spelling pubmed-86088042021-11-24 Genome sequencing of the multicellular alga Astrephomene provides insights into convergent evolution of germ-soma differentiation Yamashita, Shota Yamamoto, Kayoko Matsuzaki, Ryo Suzuki, Shigekatsu Yamaguchi, Haruyo Hirooka, Shunsuke Minakuchi, Yohei Miyagishima, Shin-ya Kawachi, Masanobu Toyoda, Atsushi Nozaki, Hisayoshi Sci Rep Article Germ-soma differentiation evolved independently in many eukaryotic lineages and contributed to complex multicellular organizations. However, the molecular genetic bases of such convergent evolution remain unresolved. Two multicellular volvocine green algae, Volvox and Astrephomene, exhibit convergent evolution of germ-soma differentiation. The complete genome sequence is now available for Volvox, while genome information is scarce for Astrephomene. Here, we generated the de novo whole genome sequence of Astrephomene gubernaculifera and conducted RNA-seq analysis of isolated somatic and reproductive cells. In Volvox, tandem duplication and neofunctionalization of the ancestral transcription factor gene (RLS1/rlsD) might have led to the evolution of regA, the master regulator for Volvox germ-soma differentiation. However, our genome data demonstrated that Astrephomene has not undergone tandem duplication of the RLS1/rlsD homolog or acquisition of a regA-like gene. Our RNA-seq analysis revealed the downregulation of photosynthetic and anabolic gene expression in Astrephomene somatic cells, as in Volvox. Among genes with high expression in somatic cells of Astrephomene, we identified three genes encoding putative transcription factors, which may regulate somatic cell differentiation. Thus, the convergent evolution of germ-soma differentiation in the volvocine algae may have occurred by the acquisition of different regulatory circuits that generate a similar division of labor. Nature Publishing Group UK 2021-11-22 /pmc/articles/PMC8608804/ /pubmed/34811380 http://dx.doi.org/10.1038/s41598-021-01521-x Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Yamashita, Shota
Yamamoto, Kayoko
Matsuzaki, Ryo
Suzuki, Shigekatsu
Yamaguchi, Haruyo
Hirooka, Shunsuke
Minakuchi, Yohei
Miyagishima, Shin-ya
Kawachi, Masanobu
Toyoda, Atsushi
Nozaki, Hisayoshi
Genome sequencing of the multicellular alga Astrephomene provides insights into convergent evolution of germ-soma differentiation
title Genome sequencing of the multicellular alga Astrephomene provides insights into convergent evolution of germ-soma differentiation
title_full Genome sequencing of the multicellular alga Astrephomene provides insights into convergent evolution of germ-soma differentiation
title_fullStr Genome sequencing of the multicellular alga Astrephomene provides insights into convergent evolution of germ-soma differentiation
title_full_unstemmed Genome sequencing of the multicellular alga Astrephomene provides insights into convergent evolution of germ-soma differentiation
title_short Genome sequencing of the multicellular alga Astrephomene provides insights into convergent evolution of germ-soma differentiation
title_sort genome sequencing of the multicellular alga astrephomene provides insights into convergent evolution of germ-soma differentiation
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8608804/
https://www.ncbi.nlm.nih.gov/pubmed/34811380
http://dx.doi.org/10.1038/s41598-021-01521-x
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