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Evidence for lateral gene transfer (LGT) in the evolution of eubacteria-derived small GTPases in plant organelles

The genomes of free-living bacteria frequently exchange genes via lateral gene transfer (LGT), which has played a major role in bacterial evolution. LGT also played a significant role in the acquisition of genes from non-cyanobacterial bacteria to the lineage of “primary” algae and land plants. Smal...

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Autores principales: Suwastika, I. Nengah, Denawa, Masatsugu, Yomogihara, Saki, Im, Chak Han, Bang, Woo Young, Ohniwa, Ryosuke L., Bahk, Jeong Dong, Takeyasu, Kunio, Shiina, Takashi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4263083/
https://www.ncbi.nlm.nih.gov/pubmed/25566271
http://dx.doi.org/10.3389/fpls.2014.00678
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author Suwastika, I. Nengah
Denawa, Masatsugu
Yomogihara, Saki
Im, Chak Han
Bang, Woo Young
Ohniwa, Ryosuke L.
Bahk, Jeong Dong
Takeyasu, Kunio
Shiina, Takashi
author_facet Suwastika, I. Nengah
Denawa, Masatsugu
Yomogihara, Saki
Im, Chak Han
Bang, Woo Young
Ohniwa, Ryosuke L.
Bahk, Jeong Dong
Takeyasu, Kunio
Shiina, Takashi
author_sort Suwastika, I. Nengah
collection PubMed
description The genomes of free-living bacteria frequently exchange genes via lateral gene transfer (LGT), which has played a major role in bacterial evolution. LGT also played a significant role in the acquisition of genes from non-cyanobacterial bacteria to the lineage of “primary” algae and land plants. Small GTPases are widely distributed among prokaryotes and eukaryotes. In this study, we inferred the evolutionary history of organelle-targeted small GTPases in plants. Arabidopsis thaliana contains at least one ortholog in seven subfamilies of OBG-HflX-like and TrmE-Era-EngA-YihA-Septin-like GTPase superfamilies (together referred to as Era-like GTPases). Subcellular localization analysis of all Era-like GTPases in Arabidopsis revealed that all 30 eubacteria-related GTPases are localized to chloroplasts and/or mitochondria, whereas archaea-related DRG and NOG1 are localized to the cytoplasm and nucleus, respectively, suggesting that chloroplast- and mitochondrion-localized GTPases are derived from the ancestral cyanobacterium and α-proteobacterium, respectively, through endosymbiotic gene transfer (EGT). However, phylogenetic analyses revealed that plant organelle GTPase evolution is rather complex. Among the eubacterium-related GTPases, only four localized to chloroplasts (including one dual targeting GTPase) and two localized to mitochondria were derived from cyanobacteria and α-proteobacteria, respectively. Three other chloroplast-targeted GTPases were related to α-proteobacterial proteins, rather than to cyanobacterial GTPases. Furthermore, we found that four other GTPases showed neither cyanobacterial nor α-proteobacterial affiliation. Instead, these GTPases were closely related to clades from other eubacteria, such as Bacteroides (Era1, EngB-1, and EngB-2) and green non-sulfur bacteria (HflX). This study thus provides novel evidence that LGT significantly contributed to the evolution of organelle-targeted Era-like GTPases in plants.
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spelling pubmed-42630832015-01-06 Evidence for lateral gene transfer (LGT) in the evolution of eubacteria-derived small GTPases in plant organelles Suwastika, I. Nengah Denawa, Masatsugu Yomogihara, Saki Im, Chak Han Bang, Woo Young Ohniwa, Ryosuke L. Bahk, Jeong Dong Takeyasu, Kunio Shiina, Takashi Front Plant Sci Plant Science The genomes of free-living bacteria frequently exchange genes via lateral gene transfer (LGT), which has played a major role in bacterial evolution. LGT also played a significant role in the acquisition of genes from non-cyanobacterial bacteria to the lineage of “primary” algae and land plants. Small GTPases are widely distributed among prokaryotes and eukaryotes. In this study, we inferred the evolutionary history of organelle-targeted small GTPases in plants. Arabidopsis thaliana contains at least one ortholog in seven subfamilies of OBG-HflX-like and TrmE-Era-EngA-YihA-Septin-like GTPase superfamilies (together referred to as Era-like GTPases). Subcellular localization analysis of all Era-like GTPases in Arabidopsis revealed that all 30 eubacteria-related GTPases are localized to chloroplasts and/or mitochondria, whereas archaea-related DRG and NOG1 are localized to the cytoplasm and nucleus, respectively, suggesting that chloroplast- and mitochondrion-localized GTPases are derived from the ancestral cyanobacterium and α-proteobacterium, respectively, through endosymbiotic gene transfer (EGT). However, phylogenetic analyses revealed that plant organelle GTPase evolution is rather complex. Among the eubacterium-related GTPases, only four localized to chloroplasts (including one dual targeting GTPase) and two localized to mitochondria were derived from cyanobacteria and α-proteobacteria, respectively. Three other chloroplast-targeted GTPases were related to α-proteobacterial proteins, rather than to cyanobacterial GTPases. Furthermore, we found that four other GTPases showed neither cyanobacterial nor α-proteobacterial affiliation. Instead, these GTPases were closely related to clades from other eubacteria, such as Bacteroides (Era1, EngB-1, and EngB-2) and green non-sulfur bacteria (HflX). This study thus provides novel evidence that LGT significantly contributed to the evolution of organelle-targeted Era-like GTPases in plants. Frontiers Media S.A. 2014-12-11 /pmc/articles/PMC4263083/ /pubmed/25566271 http://dx.doi.org/10.3389/fpls.2014.00678 Text en Copyright © 2014 Suwastika, Denawa, Yomogihara, Im, Bang, Ohniwa, Bahk, Takeyasu and Shiina. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Suwastika, I. Nengah
Denawa, Masatsugu
Yomogihara, Saki
Im, Chak Han
Bang, Woo Young
Ohniwa, Ryosuke L.
Bahk, Jeong Dong
Takeyasu, Kunio
Shiina, Takashi
Evidence for lateral gene transfer (LGT) in the evolution of eubacteria-derived small GTPases in plant organelles
title Evidence for lateral gene transfer (LGT) in the evolution of eubacteria-derived small GTPases in plant organelles
title_full Evidence for lateral gene transfer (LGT) in the evolution of eubacteria-derived small GTPases in plant organelles
title_fullStr Evidence for lateral gene transfer (LGT) in the evolution of eubacteria-derived small GTPases in plant organelles
title_full_unstemmed Evidence for lateral gene transfer (LGT) in the evolution of eubacteria-derived small GTPases in plant organelles
title_short Evidence for lateral gene transfer (LGT) in the evolution of eubacteria-derived small GTPases in plant organelles
title_sort evidence for lateral gene transfer (lgt) in the evolution of eubacteria-derived small gtpases in plant organelles
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4263083/
https://www.ncbi.nlm.nih.gov/pubmed/25566271
http://dx.doi.org/10.3389/fpls.2014.00678
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