Cargando…

Comparative genome and transcriptome analyses of the social amoeba Acytostelium subglobosum that accomplishes multicellular development without germ-soma differentiation

BACKGROUND: Social amoebae are lower eukaryotes that inhabit the soil. They are characterized by the construction of a starvation-induced multicellular fruiting body with a spore ball and supportive stalk. In most species, the stalk is filled with motile stalk cells, as represented by the model orga...

Descripción completa

Detalles Bibliográficos
Autores principales: Urushihara, Hideko, Kuwayama, Hidekazu, Fukuhara, Kensuke, Itoh, Takehiko, Kagoshima, Hiroshi, Shin-I, Tadasu, Toyoda, Atsushi, Ohishi, Kazuyo, Taniguchi, Tateaki, Noguchi, Hideki, Kuroki, Yoko, Hata, Takashi, Uchi, Kyoko, Mohri, Kurato, King, Jason S, Insall, Robert H, Kohara, Yuji, Fujiyama, Asao
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4334915/
https://www.ncbi.nlm.nih.gov/pubmed/25758444
http://dx.doi.org/10.1186/s12864-015-1278-x
_version_ 1782358250939744256
author Urushihara, Hideko
Kuwayama, Hidekazu
Fukuhara, Kensuke
Itoh, Takehiko
Kagoshima, Hiroshi
Shin-I, Tadasu
Toyoda, Atsushi
Ohishi, Kazuyo
Taniguchi, Tateaki
Noguchi, Hideki
Kuroki, Yoko
Hata, Takashi
Uchi, Kyoko
Mohri, Kurato
King, Jason S
Insall, Robert H
Kohara, Yuji
Fujiyama, Asao
author_facet Urushihara, Hideko
Kuwayama, Hidekazu
Fukuhara, Kensuke
Itoh, Takehiko
Kagoshima, Hiroshi
Shin-I, Tadasu
Toyoda, Atsushi
Ohishi, Kazuyo
Taniguchi, Tateaki
Noguchi, Hideki
Kuroki, Yoko
Hata, Takashi
Uchi, Kyoko
Mohri, Kurato
King, Jason S
Insall, Robert H
Kohara, Yuji
Fujiyama, Asao
author_sort Urushihara, Hideko
collection PubMed
description BACKGROUND: Social amoebae are lower eukaryotes that inhabit the soil. They are characterized by the construction of a starvation-induced multicellular fruiting body with a spore ball and supportive stalk. In most species, the stalk is filled with motile stalk cells, as represented by the model organism Dictyostelium discoideum, whose developmental mechanisms have been well characterized. However, in the genus Acytostelium, the stalk is acellular and all aggregated cells become spores. Phylogenetic analyses have shown that it is not an ancestral genus but has lost the ability to undergo cell differentiation. RESULTS: We performed genome and transcriptome analyses of Acytostelium subglobosum and compared our findings to other available dictyostelid genome data. Although A. subglobosum adopts a qualitatively different developmental program from other dictyostelids, its gene repertoire was largely conserved. Yet, families of polyketide synthase and extracellular matrix proteins have not expanded and a serine protease and ABC transporter B family gene, tagA, and a few other developmental genes are missing in the A. subglobosum lineage. Temporal gene expression patterns are astonishingly dissimilar from those of D. discoideum, and only a limited fraction of the ortholog pairs shared the same expression patterns, so that some signaling cascades for development seem to be disabled in A. subglobosum. CONCLUSIONS: The absence of the ability to undergo cell differentiation in Acytostelium is accompanied by a small change in coding potential and extensive alterations in gene expression patterns. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-015-1278-x) contains supplementary material, which is available to authorized users.
format Online
Article
Text
id pubmed-4334915
institution National Center for Biotechnology Information
language English
publishDate 2015
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-43349152015-02-21 Comparative genome and transcriptome analyses of the social amoeba Acytostelium subglobosum that accomplishes multicellular development without germ-soma differentiation Urushihara, Hideko Kuwayama, Hidekazu Fukuhara, Kensuke Itoh, Takehiko Kagoshima, Hiroshi Shin-I, Tadasu Toyoda, Atsushi Ohishi, Kazuyo Taniguchi, Tateaki Noguchi, Hideki Kuroki, Yoko Hata, Takashi Uchi, Kyoko Mohri, Kurato King, Jason S Insall, Robert H Kohara, Yuji Fujiyama, Asao BMC Genomics Research Article BACKGROUND: Social amoebae are lower eukaryotes that inhabit the soil. They are characterized by the construction of a starvation-induced multicellular fruiting body with a spore ball and supportive stalk. In most species, the stalk is filled with motile stalk cells, as represented by the model organism Dictyostelium discoideum, whose developmental mechanisms have been well characterized. However, in the genus Acytostelium, the stalk is acellular and all aggregated cells become spores. Phylogenetic analyses have shown that it is not an ancestral genus but has lost the ability to undergo cell differentiation. RESULTS: We performed genome and transcriptome analyses of Acytostelium subglobosum and compared our findings to other available dictyostelid genome data. Although A. subglobosum adopts a qualitatively different developmental program from other dictyostelids, its gene repertoire was largely conserved. Yet, families of polyketide synthase and extracellular matrix proteins have not expanded and a serine protease and ABC transporter B family gene, tagA, and a few other developmental genes are missing in the A. subglobosum lineage. Temporal gene expression patterns are astonishingly dissimilar from those of D. discoideum, and only a limited fraction of the ortholog pairs shared the same expression patterns, so that some signaling cascades for development seem to be disabled in A. subglobosum. CONCLUSIONS: The absence of the ability to undergo cell differentiation in Acytostelium is accompanied by a small change in coding potential and extensive alterations in gene expression patterns. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-015-1278-x) contains supplementary material, which is available to authorized users. BioMed Central 2015-02-14 /pmc/articles/PMC4334915/ /pubmed/25758444 http://dx.doi.org/10.1186/s12864-015-1278-x Text en © Urushihara et al.; licensee BioMed Central. 2015 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Urushihara, Hideko
Kuwayama, Hidekazu
Fukuhara, Kensuke
Itoh, Takehiko
Kagoshima, Hiroshi
Shin-I, Tadasu
Toyoda, Atsushi
Ohishi, Kazuyo
Taniguchi, Tateaki
Noguchi, Hideki
Kuroki, Yoko
Hata, Takashi
Uchi, Kyoko
Mohri, Kurato
King, Jason S
Insall, Robert H
Kohara, Yuji
Fujiyama, Asao
Comparative genome and transcriptome analyses of the social amoeba Acytostelium subglobosum that accomplishes multicellular development without germ-soma differentiation
title Comparative genome and transcriptome analyses of the social amoeba Acytostelium subglobosum that accomplishes multicellular development without germ-soma differentiation
title_full Comparative genome and transcriptome analyses of the social amoeba Acytostelium subglobosum that accomplishes multicellular development without germ-soma differentiation
title_fullStr Comparative genome and transcriptome analyses of the social amoeba Acytostelium subglobosum that accomplishes multicellular development without germ-soma differentiation
title_full_unstemmed Comparative genome and transcriptome analyses of the social amoeba Acytostelium subglobosum that accomplishes multicellular development without germ-soma differentiation
title_short Comparative genome and transcriptome analyses of the social amoeba Acytostelium subglobosum that accomplishes multicellular development without germ-soma differentiation
title_sort comparative genome and transcriptome analyses of the social amoeba acytostelium subglobosum that accomplishes multicellular development without germ-soma differentiation
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4334915/
https://www.ncbi.nlm.nih.gov/pubmed/25758444
http://dx.doi.org/10.1186/s12864-015-1278-x
work_keys_str_mv AT urushiharahideko comparativegenomeandtranscriptomeanalysesofthesocialamoebaacytosteliumsubglobosumthataccomplishesmulticellulardevelopmentwithoutgermsomadifferentiation
AT kuwayamahidekazu comparativegenomeandtranscriptomeanalysesofthesocialamoebaacytosteliumsubglobosumthataccomplishesmulticellulardevelopmentwithoutgermsomadifferentiation
AT fukuharakensuke comparativegenomeandtranscriptomeanalysesofthesocialamoebaacytosteliumsubglobosumthataccomplishesmulticellulardevelopmentwithoutgermsomadifferentiation
AT itohtakehiko comparativegenomeandtranscriptomeanalysesofthesocialamoebaacytosteliumsubglobosumthataccomplishesmulticellulardevelopmentwithoutgermsomadifferentiation
AT kagoshimahiroshi comparativegenomeandtranscriptomeanalysesofthesocialamoebaacytosteliumsubglobosumthataccomplishesmulticellulardevelopmentwithoutgermsomadifferentiation
AT shinitadasu comparativegenomeandtranscriptomeanalysesofthesocialamoebaacytosteliumsubglobosumthataccomplishesmulticellulardevelopmentwithoutgermsomadifferentiation
AT toyodaatsushi comparativegenomeandtranscriptomeanalysesofthesocialamoebaacytosteliumsubglobosumthataccomplishesmulticellulardevelopmentwithoutgermsomadifferentiation
AT ohishikazuyo comparativegenomeandtranscriptomeanalysesofthesocialamoebaacytosteliumsubglobosumthataccomplishesmulticellulardevelopmentwithoutgermsomadifferentiation
AT taniguchitateaki comparativegenomeandtranscriptomeanalysesofthesocialamoebaacytosteliumsubglobosumthataccomplishesmulticellulardevelopmentwithoutgermsomadifferentiation
AT noguchihideki comparativegenomeandtranscriptomeanalysesofthesocialamoebaacytosteliumsubglobosumthataccomplishesmulticellulardevelopmentwithoutgermsomadifferentiation
AT kurokiyoko comparativegenomeandtranscriptomeanalysesofthesocialamoebaacytosteliumsubglobosumthataccomplishesmulticellulardevelopmentwithoutgermsomadifferentiation
AT hatatakashi comparativegenomeandtranscriptomeanalysesofthesocialamoebaacytosteliumsubglobosumthataccomplishesmulticellulardevelopmentwithoutgermsomadifferentiation
AT uchikyoko comparativegenomeandtranscriptomeanalysesofthesocialamoebaacytosteliumsubglobosumthataccomplishesmulticellulardevelopmentwithoutgermsomadifferentiation
AT mohrikurato comparativegenomeandtranscriptomeanalysesofthesocialamoebaacytosteliumsubglobosumthataccomplishesmulticellulardevelopmentwithoutgermsomadifferentiation
AT kingjasons comparativegenomeandtranscriptomeanalysesofthesocialamoebaacytosteliumsubglobosumthataccomplishesmulticellulardevelopmentwithoutgermsomadifferentiation
AT insallroberth comparativegenomeandtranscriptomeanalysesofthesocialamoebaacytosteliumsubglobosumthataccomplishesmulticellulardevelopmentwithoutgermsomadifferentiation
AT koharayuji comparativegenomeandtranscriptomeanalysesofthesocialamoebaacytosteliumsubglobosumthataccomplishesmulticellulardevelopmentwithoutgermsomadifferentiation
AT fujiyamaasao comparativegenomeandtranscriptomeanalysesofthesocialamoebaacytosteliumsubglobosumthataccomplishesmulticellulardevelopmentwithoutgermsomadifferentiation