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Horizontal gene transfer in eukaryotic evolution
Abstract
Horizontal gene transfer (HGT; also known as lateral gene transfer) has had an important role in eukaryotic genome evolution, but its importance is often overshadowed by the greater prevalence and our more advanced understanding of gene transfer in prokaryotes. Recurrent endosymbioses and the generally poor sampling of most nuclear genes from diverse lineages have also complicated the search for transferred genes. Nevertheless, the number of well-supported cases of transfer from both prokaryotes and eukaryotes, many with significant functional implications, is now expanding rapidly. Major recent trends include the important role of HGT in adaptation to certain specialized niches and the highly variable impact of HGT in different lineages.
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“In multicellular lineages, convincing cases of HGT are rarer but include gene acquisitions in bdelloid rotifers, fungi, and even vertebrate genomes [33,34].”
From Origin and Evolution of Genes in Eukaryotes: Mechanisms, Dynamics, and Functional Implications (2025) · cites this paper as [33]
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Pérez-Martínez, X., Antaramián, A., Vázquez-Acevedo, M., Funes, S., Tolkunova, E., d'Alayer, J., Claros, M., Davidson, E., King, M., & González-Halphen, D. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m010244200 · Cited by 105
Kavanaugh, L. A., Fraser, J. A., & Dietrich, F. S. (2006) · Molecular Biology and Evolution · doi:10.1093/molbev/msl070 · Cited by 105
How do mitochondrial genes get into the nucleus?
Henze, K. (2001) · Trends in Genetics · doi:10.1016/s0168-9525(01)02312-5 · Cited by 104
The difference between organelles and endosymbionts
Theißen, U., & Martin, W. F. (2006) · Current Biology · doi:10.1016/j.cub.2006.11.020 · Cited by 103
Andersson, J. O., Hirt, R. P., Foster, P. G., & Roger, A. J. (2006) · BMC Evolutionary Biology · doi:10.1186/1471-2148-6-27 · Cited by 103
Andersson, J. O., Sjögren, Å. M., Horner, D. S., Murphy, C. A., Dyal, P. L., Svärd, S. G., Logsdon, J. M., Jr., Ragan, M. A., Hirt, R. P., & Roger, A. J. (2007) · BMC Genomics · doi:10.1186/1471-2164-8-51 · Cited by 103
Andersson, J. O., Doolittle, W. F., & Nesbø, C. L. (2001) · Science · doi:10.1126/science.1062241 · Cited by 96
High rate of horizontal transfer of transposable elements in Drosophila
Sánchez‐Gracia, A., Maside, X., & Charlesworth, B. (2005) · Trends in Genetics · doi:10.1016/j.tig.2005.02.001 · Cited by 95
Keeling, P. J., & Inagaki, Y. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0404505101 · Cited by 93
Self-citationSlamovits, C. H., Saldarriaga, J. F., Larocque, A., & Keeling, P. J. (2007) · Journal of Molecular Biology · doi:10.1016/j.jmb.2007.06.085 · Cited by 93
Self-citationPlastid endosymbiosis, genome evolution and the origin of green plants.
Stiller, J. (2007) · Trends in Plant Science · doi:10.1016/j.tplants.2007.08.002 · Cited by 92
Lateral Gene Transfer and Metabolic Adaptation in the Human Parasite Trichomonas vaginalis
de Koning, A. P., Brinkman, F. S. L., Jones, S. J. M., & Keeling, P. J. (2000) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a026275 · Cited by 91
Self-citationEndosymbiosis: Lessons in Conflict Resolution
Wernegreen, J. J. (2004) · PLoS Biology · doi:10.1371/journal.pbio.0020068 · Cited by 90
Funes, S., Davidson, E., Claros, M. G., van Lis, R., Pérez-Martı́nez, X., Vázquez‐Acevedo, M., King, M. P., & González‐Halphen, D. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m109993200 · Cited by 88
Waller, R. F., Slamovits, C. H., & Keeling, P. J. (2006) · Molecular Biology and Evolution · doi:10.1093/molbev/msl008 · Cited by 84
Self-citationHorizontal Gene Transfer and the Evolution of Parasitic Protozoa
Richards, T. A., Hirt, R. P., Williams, B., & Embley, T. M. (2003) · Protist · doi:10.1078/143446103764928468 · Cited by 83
Roelofs, J., & Haastert, P. J. M. V. (2001) · Nature · doi:10.1038/35082627 · Cited by 80
Do different surrogate methods detect lateral genetic transfer events of different relative ages?
Ragan, M. A., Harlow, T. J., & Beiko, R. G. (2005) · Trends in Microbiology · doi:10.1016/j.tim.2005.11.004 · Cited by 80
Lateral transfer at the gene and subgenic levels in the evolution of eukaryotic enolase
Keeling, P. J., & Palmer, J. D. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.191337098 · Cited by 79
Self-citationIn vitro assembly and GTP hydrolysis by bacterial tubulins BtubA and BtubB
Sontag, C. A., Staley, J. T., & Erickson, H. (2005) · The Journal of Cell Biology · doi:10.1083/jcb.200410027 · Cited by 79
Endosymbiosis in protozoa of the Trypanosomatidae family
de Souza, W., & Motta, M. C. M. (1999) · FEMS Microbiology Letters · doi:10.1016/s0378-1097(99)00005-1 · Cited by 79
Ancient horizontal gene transfer can benefit phylogenetic reconstruction.
Huang, J.-L., & Gogarten, J. (2006) · Trends in Genetics · doi:10.1016/j.tig.2006.05.004 · Cited by 78
Interspecific evolution: microbial symbiosis, endosymbiosis and gene transfer
Hoffmeister, M., & Martin, W. F. (2003) · Environmental Microbiology · doi:10.1046/j.1462-2920.2003.00454.x · Cited by 75
Daley, D. O., Clifton, R., & Whelan, J. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.122354399 · Cited by 73
Slamovits, C. H., & Keeling, P. J. (2006) · Eukaryotic Cell · doi:10.1128/ec.5.1.148-154.2006 · Cited by 71
Self-citationFukami, H., Chen, C. A., Chiou, C.-Y., & Knowlton, N. (2007) · Journal of Molecular Evolution · doi:10.1007/s00239-006-0279-4 · Cited by 70
Lateral Transfer and Recompartmentalization of Calvin Cycle Enzymes of Plants and Algae
Rogers, M. B., & Keeling, P. J. (2004) · Journal of Molecular Evolution · doi:10.1007/s00239-003-2558-7 · Cited by 68
Self-citationWhy genes persist in organelle genomes
Daley, D. O., & Whelan, J. (2005) · Genome Biology · doi:10.1186/gb-2005-6-5-110 · Cited by 66
Invasion and Persistence of a Selfish Gene in the Cnidaria
Goddard, M. R., Leigh, J., Roger, A. J., & Pemberton, A. J. (2006) · PLoS ONE · doi:10.1371/journal.pone.0000003 · Cited by 62
Gene Transfers from Nanoarchaeota to an Ancestor of Diplomonads and Parabasalids
Andersson, J. O. (2004) · Molecular Biology and Evolution · doi:10.1093/molbev/msh254 · Cited by 60
Horizontal gene transfer of two cytoskeletal elements from a eukaryote to a cyanobacterium
Guljamow, A., Jenke‐Kodama, H., Saumweber, H., Quillardet, P., Frangeul, L., Castets, A. M., Bouchier, C., de Marsac, N. T., & Dittmann, E. (2007) · Current Biology · doi:10.1016/j.cub.2007.06.063 · Cited by 58
Gamieldien, J., Ptitsyn, A. A., & Hide, W. (2002) · Trends in Genetics · doi:10.1016/s0168-9525(01)02529-x · Cited by 56
Henze, K., Horner, D. S., Suguri, S., Moore, D. V., Sánchez, L. B., Müller, M., & Embley, T. M. (2001) · Gene · doi:10.1016/s0378-1119(01)00773-9 · Cited by 56
Archibald, J. M. (2005) · IUBMB Life · doi:10.1080/15216540500167732 · Cited by 52
Patterns of Bacterial Gene Movement
Hao, W. (2004) · Molecular Biology and Evolution · doi:10.1093/molbev/msh129 · Cited by 52
What tangled web: barriers to rampant horizontal gene transfer
Kurland, C. G. (2005) · BioEssays · doi:10.1002/bies.20258 · Cited by 51
Energy transduction anchors genes in organelles
Allen, J. F., Puthiyaveetil, S., Ström, J., & Allen, C. A. (2005) · BioEssays · doi:10.1002/bies.20194 · Cited by 49
A complex and punctate distribution of three eukaryotic genes derived by lateral gene transfer
Rogers, M. B., Watkins, R. F., Harper, J., Durnford, D. G., Gray, M. W., & Keeling, P. J. (2007) · BMC Evolutionary Biology · doi:10.1186/1471-2148-7-89 · Cited by 48
Self-citationThe Presence of a Haloarchaeal Type Tyrosyl-tRNA Synthetase Marks the Opisthokonts as Monophyletic
Huang, J., Xu, Y. C., & Gogarten, J. P. (2005) · Molecular Biology and Evolution · doi:10.1093/molbev/msi221 · Cited by 47
Andersson, J. O., & Roger, A. J. (2002) · Eukaryotic Cell · doi:10.1128/ec.1.2.304-310.2002 · Cited by 47
Forces maintaining organellar genomes: is any as strong as genetic code disparity or hydrophobicity?
de Grey, A. D. N. J. (2005) · BioEssays · doi:10.1002/bies.20209 · Cited by 45
The Chloroplast Genome of Dinoflagellates ? A Reduced Instruction Set?
Green, B. R. (2004) · Protist · doi:10.1078/1434461000161 · Cited by 39
Complex distribution of EFL and EF-1α proteins in the green algal lineage
Noble, G. P., Rogers, M. B., & Keeling, P. (2007) · BMC Evolutionary Biology · doi:10.1186/1471-2148-7-82 · Cited by 38
Self-citationLedent, V., & Vervoort, M. (2006) · BMC Biology · doi:10.1186/1741-7007-4-24 · Cited by 33
The glycolytic pathway of Trimastix pyriformis is an evolutionary mosaic.
Stechmann, A., Baumgärtner, M., Silberman, J. D., & Roger, A. J. (2006) · BMC Evolutionary Biology · doi:10.1186/1471-2148-6-101 · Cited by 32
Waller, R. F., Patron, N. J., & Keeling, P. J. (2006) · INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY · doi:10.1099/ijs.0.64061-0 · Cited by 32
Self-citationSimpson, A. G. B., Perley, T. A., & Lara, E. (2007) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2007.11.035 · Cited by 31
Horizontal transfer of a eukaryotic plastid-targeted protein gene to cyanobacteria
Rogers, M. B., Patron, N. J., & Keeling, P. J. (2007) · BMC Biology · doi:10.1186/1741-7007-5-26 · Cited by 30
Self-citationWatkins, R. F., & Gray, M. W. (2006) · Journal of Molecular Evolution · doi:10.1007/s00239-006-0031-0 · Cited by 29
Genomics and Evolution of Microbial Eukaryotes
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Metadata
- Authors
- Keeling, P. J., & Palmer, J. D.
- Affiliations
- University of British Columbia (CA)
- Indiana University Bloomington (US)
- Corresponding author
- Keeling, Patrick J.
- Venue
- Nature Reviews Genetics
- Published
- 2008-08
- Volume
- 9
- Issue
- 8
- Pages
- 605-618
- ISSN
- 1471-0056 (ISSN-L)
- 1471-0064
- OpenAlex
- W2055758623
- Cited by
- 1,355
- References
- 159
- Citations by year
- 2026: 54 · 2025: 53 · 2024: 63 · 2023: 91 · 2022: 81 · 2021: 76 · 2020: 76 · 2019: 85 · 2018: 65 · 2017: 70 · 2016: 90 · 2015: 86 · 2014: 82 · 2013: 100 · 2012: 81
- FWCI
- 5.66
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Reviews Genetics (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Lilly Endowment
- Canadian Institute for Advanced Research
- Tula Foundation
- National Institutes of Health
- Natural Sciences and Engineering Research Council of Canada
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Chromosomal and Genetic Variations
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Protist diversity and phylogeny
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Keywords
- horizontal gene transfer, eukaryotic evolution, genome evolution, endosymbiosis, eukaryotic lineages
- MeSH terms
- Adaptation, Biological, Animals, DNA Transposable Elements, Eukaryotic Cells, Biological Evolution, Humans, Models, Biological, Phylogeny, Plants, Prokaryotic Cells, Symbiosis, Genome, Protein Transport, Gene Transfer, Horizontal
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