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Origins of a cyanobacterial 6-phosphogluconate dehydrogenase in plastid-lacking eukaryotes

BACKGROUND: Plastids have inherited their own genomes from a single cyanobacterial ancestor, but the majority of cyanobacterial genes, once retained in the ancestral plastid genome, have been lost or transferred into the eukaryotic host nuclear genome via endosymbiotic gene transfer. Although previo...

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Autores principales: Maruyama, Shinichiro, Misawa, Kazuharu, Iseki, Mineo, Watanabe, Masakatsu, Nozaki, Hisayoshi
Formato: Texto
Lenguaje:English
Publicado: BioMed Central 2008
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2416651/
https://www.ncbi.nlm.nih.gov/pubmed/18485228
http://dx.doi.org/10.1186/1471-2148-8-151
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author Maruyama, Shinichiro
Misawa, Kazuharu
Iseki, Mineo
Watanabe, Masakatsu
Nozaki, Hisayoshi
author_facet Maruyama, Shinichiro
Misawa, Kazuharu
Iseki, Mineo
Watanabe, Masakatsu
Nozaki, Hisayoshi
author_sort Maruyama, Shinichiro
collection PubMed
description BACKGROUND: Plastids have inherited their own genomes from a single cyanobacterial ancestor, but the majority of cyanobacterial genes, once retained in the ancestral plastid genome, have been lost or transferred into the eukaryotic host nuclear genome via endosymbiotic gene transfer. Although previous studies showed that cyanobacterial gnd genes, which encode 6-phosphogluconate dehydrogenase, are present in several plastid-lacking protists as well as primary and secondary plastid-containing phototrophic eukaryotes, the evolutionary paths of these genes remain elusive. RESULTS: Here we show an extended phylogenetic analysis including novel gnd gene sequences from Excavata and Glaucophyta. Our analysis demonstrated the patchy distribution of the excavate genes in the gnd gene phylogeny. The Diplonema gene was related to cytosol-type genes in red algae and Opisthokonta, while heterolobosean genes occupied basal phylogenetic positions with plastid-type red algal genes within the monophyletic eukaryotic group that is sister to cyanobacterial genes. Statistical tests based on exhaustive maximum likelihood analyses strongly rejected that heterolobosean gnd genes were derived from a secondary plastid of green lineage. In addition, the cyanobacterial gnd genes from phototrophic and phagotrophic species in Euglenida were robustly monophyletic with Stramenopiles, and this monophyletic clade was moderately separated from those of red algae. These data suggest that these secondary phototrophic groups might have acquired the cyanobacterial genes independently of secondary endosymbioses. CONCLUSION: We propose an evolutionary scenario in which plastid-lacking Excavata acquired cyanobacterial gnd genes via eukaryote-to-eukaryote lateral gene transfer or primary endosymbiotic gene transfer early in eukaryotic evolution, and then lost either their pre-existing or cyanobacterial gene.
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spelling pubmed-24166512008-06-07 Origins of a cyanobacterial 6-phosphogluconate dehydrogenase in plastid-lacking eukaryotes Maruyama, Shinichiro Misawa, Kazuharu Iseki, Mineo Watanabe, Masakatsu Nozaki, Hisayoshi BMC Evol Biol Research Article BACKGROUND: Plastids have inherited their own genomes from a single cyanobacterial ancestor, but the majority of cyanobacterial genes, once retained in the ancestral plastid genome, have been lost or transferred into the eukaryotic host nuclear genome via endosymbiotic gene transfer. Although previous studies showed that cyanobacterial gnd genes, which encode 6-phosphogluconate dehydrogenase, are present in several plastid-lacking protists as well as primary and secondary plastid-containing phototrophic eukaryotes, the evolutionary paths of these genes remain elusive. RESULTS: Here we show an extended phylogenetic analysis including novel gnd gene sequences from Excavata and Glaucophyta. Our analysis demonstrated the patchy distribution of the excavate genes in the gnd gene phylogeny. The Diplonema gene was related to cytosol-type genes in red algae and Opisthokonta, while heterolobosean genes occupied basal phylogenetic positions with plastid-type red algal genes within the monophyletic eukaryotic group that is sister to cyanobacterial genes. Statistical tests based on exhaustive maximum likelihood analyses strongly rejected that heterolobosean gnd genes were derived from a secondary plastid of green lineage. In addition, the cyanobacterial gnd genes from phototrophic and phagotrophic species in Euglenida were robustly monophyletic with Stramenopiles, and this monophyletic clade was moderately separated from those of red algae. These data suggest that these secondary phototrophic groups might have acquired the cyanobacterial genes independently of secondary endosymbioses. CONCLUSION: We propose an evolutionary scenario in which plastid-lacking Excavata acquired cyanobacterial gnd genes via eukaryote-to-eukaryote lateral gene transfer or primary endosymbiotic gene transfer early in eukaryotic evolution, and then lost either their pre-existing or cyanobacterial gene. BioMed Central 2008-05-17 /pmc/articles/PMC2416651/ /pubmed/18485228 http://dx.doi.org/10.1186/1471-2148-8-151 Text en Copyright ©2008 Maruyama et al; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Article
Maruyama, Shinichiro
Misawa, Kazuharu
Iseki, Mineo
Watanabe, Masakatsu
Nozaki, Hisayoshi
Origins of a cyanobacterial 6-phosphogluconate dehydrogenase in plastid-lacking eukaryotes
title Origins of a cyanobacterial 6-phosphogluconate dehydrogenase in plastid-lacking eukaryotes
title_full Origins of a cyanobacterial 6-phosphogluconate dehydrogenase in plastid-lacking eukaryotes
title_fullStr Origins of a cyanobacterial 6-phosphogluconate dehydrogenase in plastid-lacking eukaryotes
title_full_unstemmed Origins of a cyanobacterial 6-phosphogluconate dehydrogenase in plastid-lacking eukaryotes
title_short Origins of a cyanobacterial 6-phosphogluconate dehydrogenase in plastid-lacking eukaryotes
title_sort origins of a cyanobacterial 6-phosphogluconate dehydrogenase in plastid-lacking eukaryotes
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2416651/
https://www.ncbi.nlm.nih.gov/pubmed/18485228
http://dx.doi.org/10.1186/1471-2148-8-151
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