The RJL family of small GTPases is an ancient eukaryotic invention probably functionally associated with the flagellar apparatus

Marek Elias; John M. Archibald

doi:10.1016/j.gene.2009.04.011

The RJL family of small GTPases is an ancient eukaryotic invention probably functionally associated with the flagellar apparatus

Marek Elias, John M. Archibald

Producción científica: Contribución a una revista › Artículo › revisión exhaustiva

27 Citas (Scopus)

Resumen

A patchily distributed gene family is often taken as evidence for horizontal gene transfer (HGT) events, but it may also result solely from multiple gene losses. The RJL family of uncharacterised Ras-like GTPases was previously suggested to have undergone HGT events between protists and deuterostome metazoans, owing to the apparent absence of RJL in intermediate groups (Nepomuceno-Silva, J.L., de Melo, L.D., Mendonca, S.M., Paixao, J.C., Lopes, U.G., 2004. RJLs: a new family of Ras-related GTP-binding proteins. Gene 327, 221-232). We have reanalysed the phylogenetic distribution and phylogeny of the RJL family, taking advantage of the recent expansion of sequence data available from diverse eukaryotes. We found that RJL orthologs are much more widely distributed than previously assumed. At least one representative encoding an RJL protein could be identified for each of the six major eukaryotic "supergroups" (Opisthokonta, Amoebozoa, Excavata, Archaeplastida, Chromalveolata, and Rhizaria) as well as for a species of Apusomonadida, a deep lineage that may not be specifically related to any of the recognized supergroups. Phylogenetic analyses do not support HGT of RJL genes between the major eukaryotic lineages, indicating that the RJL family was present in the last eukaryotic common ancestor and was lost several times over the course of eukaryotic evolution. Interestingly, RJL was lost from all taxa lacking flagellated cells and from a few lineages that build structurally unusual or reduced flagella, raising the intriguing possibility that RJL proteins are functionally associated with the flagellar apparatus. The RJL GTPase domain has been fused with the DnaJ domain on two separate occasions: in the Holozoa (before the split of Metazoa and choanoflagellates), giving rise to the previously known Rbj type of RJL with the DnaJ domain at the C-terminus, and independently in Alveolata resulting in novel proteins with the DnaJ domain at the N-terminus. These independent fusions suggest that RJL proteins may generally function via regulating the DnaJ-Hsp70 module.

Idioma original	English
Páginas (desde-hasta)	63-72
Número de páginas	10
Publicación	Gene
Volumen	442
N.º	1-2
DOI	https://doi.org/10.1016/j.gene.2009.04.011
Estado	Published - ago. 1 2009
Publicado de forma externa	Sí

Nota bibliográfica

Funding Information:
We highly appreciate constructive comments of two anonymous reviewers on the original version of the manuscript. We thank the Joint Genome Institute's Community Sequencing Program ( http://www.jgi.doe.gov/sequencing/why/50026.html ) for their on-going efforts to sequence the nuclear genomes of Guillardia theta and Bigelowiella natans, K. Barry and E. Lindquist of the JGI for project management and data availability, and M.W. Gray, P. Keeling, G.I. McFadden and C.E. Lane for their contributions to the project. We are also indebted to Andreas Schmidt-Rhaesa (Biozentrum Grindel/Zoological Museum, Hamburg) and Peter von Dassow (Station Biologique de Roscoff) for the discussions on flagella in Ecdysozoa and Emiliania, respectively. Genome sequence data from Babesia bigemina, Eimeria tenella and Schistosoma mansoni, were provided by the Wellcome Trust Sanger Institute ( http://www.sanger.ac.uk/ ). Genome sequence data from Physarum polycephalum were produced by the Genome Sequencing Center at Washington University School of Medicine in St. Louis (GSC WUSTL) and can be obtained from http://genome.wustl.edu/pub/organism/ . Genome sequence data from Aureococcus anophagefferens, Ciona intestinalis, Lottia gigantea, Naegleria gruberi, and Takifugu rubripes were produced by the US Department of Energy Joint Genome Institute, http://www.jgi.doe.gov/ and are provided for use in this publication only. Genome sequence data from Acanthamoeba castellanii were generated and provided by the Human Genome Sequencing Center at Baylor College of Medicine ( http://www.hgsc.bcm.tmc.edu/ ). Sequence data from Galdieria sulphuraria were obtained from the Michigan State University Galdieria Database ( http://genomics.msu.edu/galdieria ). We also greatly acknowledge the opportunity to use unassembled WGS sequencing reads from Amphimedon queenslandica (=Reniera sp.) and Spironucleus vortens produced by DOE JGI, from Ectocarpus siliculosus produced by Genoscope, from Sterkiella histriomuscorum (=Oxytricha trifallax) produced by GSC WUSTL, and from Spizellomyces punctatus, Allomyces macrogynus, Amastigomonas sp. ATCC 50062, and Proterospongia sp. ATCC 50818 produced by the Broad Institute. ME was supported by research project no. 0021620858 of Czech Ministry of Education. JMA was supported by a Special Research Opportunities grant from the Natural Sciences and Engineering Research Council of Canada. JMA is Associate Director and Scholar of the Canadian Institute for Advanced Research, Program in Integrated Microbial Biodiversity, and a Canadian Institutes of Health Research New Investigator.

ASJC Scopus Subject Areas

Genetics

PubMed: MeSH publication types

Journal Article
Research Support, Non-U.S. Gov't

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10.1016/j.gene.2009.04.011

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title = "The RJL family of small GTPases is an ancient eukaryotic invention probably functionally associated with the flagellar apparatus",

abstract = "A patchily distributed gene family is often taken as evidence for horizontal gene transfer (HGT) events, but it may also result solely from multiple gene losses. The RJL family of uncharacterised Ras-like GTPases was previously suggested to have undergone HGT events between protists and deuterostome metazoans, owing to the apparent absence of RJL in intermediate groups (Nepomuceno-Silva, J.L., de Melo, L.D., Mendonca, S.M., Paixao, J.C., Lopes, U.G., 2004. RJLs: a new family of Ras-related GTP-binding proteins. Gene 327, 221-232). We have reanalysed the phylogenetic distribution and phylogeny of the RJL family, taking advantage of the recent expansion of sequence data available from diverse eukaryotes. We found that RJL orthologs are much more widely distributed than previously assumed. At least one representative encoding an RJL protein could be identified for each of the six major eukaryotic {"}supergroups{"} (Opisthokonta, Amoebozoa, Excavata, Archaeplastida, Chromalveolata, and Rhizaria) as well as for a species of Apusomonadida, a deep lineage that may not be specifically related to any of the recognized supergroups. Phylogenetic analyses do not support HGT of RJL genes between the major eukaryotic lineages, indicating that the RJL family was present in the last eukaryotic common ancestor and was lost several times over the course of eukaryotic evolution. Interestingly, RJL was lost from all taxa lacking flagellated cells and from a few lineages that build structurally unusual or reduced flagella, raising the intriguing possibility that RJL proteins are functionally associated with the flagellar apparatus. The RJL GTPase domain has been fused with the DnaJ domain on two separate occasions: in the Holozoa (before the split of Metazoa and choanoflagellates), giving rise to the previously known Rbj type of RJL with the DnaJ domain at the C-terminus, and independently in Alveolata resulting in novel proteins with the DnaJ domain at the N-terminus. These independent fusions suggest that RJL proteins may generally function via regulating the DnaJ-Hsp70 module.",

author = "Marek Elias and Archibald, {John M.}",

note = "Funding Information: We highly appreciate constructive comments of two anonymous reviewers on the original version of the manuscript. We thank the Joint Genome Institute's Community Sequencing Program ( http://www.jgi.doe.gov/sequencing/why/50026.html ) for their on-going efforts to sequence the nuclear genomes of Guillardia theta and Bigelowiella natans, K. Barry and E. Lindquist of the JGI for project management and data availability, and M.W. Gray, P. Keeling, G.I. McFadden and C.E. Lane for their contributions to the project. We are also indebted to Andreas Schmidt-Rhaesa (Biozentrum Grindel/Zoological Museum, Hamburg) and Peter von Dassow (Station Biologique de Roscoff) for the discussions on flagella in Ecdysozoa and Emiliania, respectively. Genome sequence data from Babesia bigemina, Eimeria tenella and Schistosoma mansoni, were provided by the Wellcome Trust Sanger Institute ( http://www.sanger.ac.uk/ ). Genome sequence data from Physarum polycephalum were produced by the Genome Sequencing Center at Washington University School of Medicine in St. Louis (GSC WUSTL) and can be obtained from http://genome.wustl.edu/pub/organism/ . Genome sequence data from Aureococcus anophagefferens, Ciona intestinalis, Lottia gigantea, Naegleria gruberi, and Takifugu rubripes were produced by the US Department of Energy Joint Genome Institute, http://www.jgi.doe.gov/ and are provided for use in this publication only. Genome sequence data from Acanthamoeba castellanii were generated and provided by the Human Genome Sequencing Center at Baylor College of Medicine ( http://www.hgsc.bcm.tmc.edu/ ). Sequence data from Galdieria sulphuraria were obtained from the Michigan State University Galdieria Database ( http://genomics.msu.edu/galdieria ). We also greatly acknowledge the opportunity to use unassembled WGS sequencing reads from Amphimedon queenslandica (=Reniera sp.) and Spironucleus vortens produced by DOE JGI, from Ectocarpus siliculosus produced by Genoscope, from Sterkiella histriomuscorum (=Oxytricha trifallax) produced by GSC WUSTL, and from Spizellomyces punctatus, Allomyces macrogynus, Amastigomonas sp. ATCC 50062, and Proterospongia sp. ATCC 50818 produced by the Broad Institute. ME was supported by research project no. 0021620858 of Czech Ministry of Education. JMA was supported by a Special Research Opportunities grant from the Natural Sciences and Engineering Research Council of Canada. JMA is Associate Director and Scholar of the Canadian Institute for Advanced Research, Program in Integrated Microbial Biodiversity, and a Canadian Institutes of Health Research New Investigator. ",

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doi = "10.1016/j.gene.2009.04.011",

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T1 - The RJL family of small GTPases is an ancient eukaryotic invention probably functionally associated with the flagellar apparatus

AU - Elias, Marek

AU - Archibald, John M.

N1 - Funding Information: We highly appreciate constructive comments of two anonymous reviewers on the original version of the manuscript. We thank the Joint Genome Institute's Community Sequencing Program ( http://www.jgi.doe.gov/sequencing/why/50026.html ) for their on-going efforts to sequence the nuclear genomes of Guillardia theta and Bigelowiella natans, K. Barry and E. Lindquist of the JGI for project management and data availability, and M.W. Gray, P. Keeling, G.I. McFadden and C.E. Lane for their contributions to the project. We are also indebted to Andreas Schmidt-Rhaesa (Biozentrum Grindel/Zoological Museum, Hamburg) and Peter von Dassow (Station Biologique de Roscoff) for the discussions on flagella in Ecdysozoa and Emiliania, respectively. Genome sequence data from Babesia bigemina, Eimeria tenella and Schistosoma mansoni, were provided by the Wellcome Trust Sanger Institute ( http://www.sanger.ac.uk/ ). Genome sequence data from Physarum polycephalum were produced by the Genome Sequencing Center at Washington University School of Medicine in St. Louis (GSC WUSTL) and can be obtained from http://genome.wustl.edu/pub/organism/ . Genome sequence data from Aureococcus anophagefferens, Ciona intestinalis, Lottia gigantea, Naegleria gruberi, and Takifugu rubripes were produced by the US Department of Energy Joint Genome Institute, http://www.jgi.doe.gov/ and are provided for use in this publication only. Genome sequence data from Acanthamoeba castellanii were generated and provided by the Human Genome Sequencing Center at Baylor College of Medicine ( http://www.hgsc.bcm.tmc.edu/ ). Sequence data from Galdieria sulphuraria were obtained from the Michigan State University Galdieria Database ( http://genomics.msu.edu/galdieria ). We also greatly acknowledge the opportunity to use unassembled WGS sequencing reads from Amphimedon queenslandica (=Reniera sp.) and Spironucleus vortens produced by DOE JGI, from Ectocarpus siliculosus produced by Genoscope, from Sterkiella histriomuscorum (=Oxytricha trifallax) produced by GSC WUSTL, and from Spizellomyces punctatus, Allomyces macrogynus, Amastigomonas sp. ATCC 50062, and Proterospongia sp. ATCC 50818 produced by the Broad Institute. ME was supported by research project no. 0021620858 of Czech Ministry of Education. JMA was supported by a Special Research Opportunities grant from the Natural Sciences and Engineering Research Council of Canada. JMA is Associate Director and Scholar of the Canadian Institute for Advanced Research, Program in Integrated Microbial Biodiversity, and a Canadian Institutes of Health Research New Investigator.

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N2 - A patchily distributed gene family is often taken as evidence for horizontal gene transfer (HGT) events, but it may also result solely from multiple gene losses. The RJL family of uncharacterised Ras-like GTPases was previously suggested to have undergone HGT events between protists and deuterostome metazoans, owing to the apparent absence of RJL in intermediate groups (Nepomuceno-Silva, J.L., de Melo, L.D., Mendonca, S.M., Paixao, J.C., Lopes, U.G., 2004. RJLs: a new family of Ras-related GTP-binding proteins. Gene 327, 221-232). We have reanalysed the phylogenetic distribution and phylogeny of the RJL family, taking advantage of the recent expansion of sequence data available from diverse eukaryotes. We found that RJL orthologs are much more widely distributed than previously assumed. At least one representative encoding an RJL protein could be identified for each of the six major eukaryotic "supergroups" (Opisthokonta, Amoebozoa, Excavata, Archaeplastida, Chromalveolata, and Rhizaria) as well as for a species of Apusomonadida, a deep lineage that may not be specifically related to any of the recognized supergroups. Phylogenetic analyses do not support HGT of RJL genes between the major eukaryotic lineages, indicating that the RJL family was present in the last eukaryotic common ancestor and was lost several times over the course of eukaryotic evolution. Interestingly, RJL was lost from all taxa lacking flagellated cells and from a few lineages that build structurally unusual or reduced flagella, raising the intriguing possibility that RJL proteins are functionally associated with the flagellar apparatus. The RJL GTPase domain has been fused with the DnaJ domain on two separate occasions: in the Holozoa (before the split of Metazoa and choanoflagellates), giving rise to the previously known Rbj type of RJL with the DnaJ domain at the C-terminus, and independently in Alveolata resulting in novel proteins with the DnaJ domain at the N-terminus. These independent fusions suggest that RJL proteins may generally function via regulating the DnaJ-Hsp70 module.

AB - A patchily distributed gene family is often taken as evidence for horizontal gene transfer (HGT) events, but it may also result solely from multiple gene losses. The RJL family of uncharacterised Ras-like GTPases was previously suggested to have undergone HGT events between protists and deuterostome metazoans, owing to the apparent absence of RJL in intermediate groups (Nepomuceno-Silva, J.L., de Melo, L.D., Mendonca, S.M., Paixao, J.C., Lopes, U.G., 2004. RJLs: a new family of Ras-related GTP-binding proteins. Gene 327, 221-232). We have reanalysed the phylogenetic distribution and phylogeny of the RJL family, taking advantage of the recent expansion of sequence data available from diverse eukaryotes. We found that RJL orthologs are much more widely distributed than previously assumed. At least one representative encoding an RJL protein could be identified for each of the six major eukaryotic "supergroups" (Opisthokonta, Amoebozoa, Excavata, Archaeplastida, Chromalveolata, and Rhizaria) as well as for a species of Apusomonadida, a deep lineage that may not be specifically related to any of the recognized supergroups. Phylogenetic analyses do not support HGT of RJL genes between the major eukaryotic lineages, indicating that the RJL family was present in the last eukaryotic common ancestor and was lost several times over the course of eukaryotic evolution. Interestingly, RJL was lost from all taxa lacking flagellated cells and from a few lineages that build structurally unusual or reduced flagella, raising the intriguing possibility that RJL proteins are functionally associated with the flagellar apparatus. The RJL GTPase domain has been fused with the DnaJ domain on two separate occasions: in the Holozoa (before the split of Metazoa and choanoflagellates), giving rise to the previously known Rbj type of RJL with the DnaJ domain at the C-terminus, and independently in Alveolata resulting in novel proteins with the DnaJ domain at the N-terminus. These independent fusions suggest that RJL proteins may generally function via regulating the DnaJ-Hsp70 module.

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The RJL family of small GTPases is an ancient eukaryotic invention probably functionally associated with the flagellar apparatus

Resumen

Nota bibliográfica

ASJC Scopus Subject Areas

PubMed: MeSH publication types

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