Did DNA replication evolve twice independently?
Open accessAbstract
DNA replication is central to all extant cellular organisms. There are substantial functional similarities between the bacterial and the archaeal/eukaryotic replication machineries, including but not limited to defined origins, replication bidirectionality, RNA primers and leading and lagging strand synthesis. However, several core components of the bacterial replication machinery are unrelated or only distantly related to the functionally equivalent components of the archaeal/eukaryotic replication apparatus. This is in sharp contrast to the principal proteins involved in transcription and translation, which are highly conserved in all divisions of life. We performed detailed sequence comparisons of the proteins that fulfill indispensable functions in DNA replication and classified them into four main categories with respect to the conservation in bacteria and archaea/eukaryotes: (i) non-homologous, such as replicative polymerases and primases; (ii) containing homologous domains but apparently non-orthologous and conceivably independently recruited to function in replication, such as the principal replicative helicases or proofreading exonucleases; (iii) apparently orthologous but poorly conserved, such as the sliding clamp proteins or DNA ligases; (iv) orthologous and highly conserved, such as clamp-loader ATPases or 5'-->3' exonucleases (FLAP nucleases). The universal conservation of some components of the DNA replication machinery and enzymes for DNA precursor biosynthesis but not the principal DNA polymerases suggests that the last common ancestor (LCA) of all modern cellular life forms possessed DNA but did not replicate it the way extant cells do. We propose that the LCA had a genetic system that contained both RNA and DNA, with the latter being produced by reverse transcription. Consequently, the modern-type system for double-stranded DNA replication likely evolved independently in the bacterial and archaeal/eukaryotic lineages.
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The last common ancestor may not have used a strictly DNA genome.
“Specifically, the last common ancestor may have had a cell membrane (Jékely 2006;Koga 2011;Lombard et al. 2012;Sojo et al. 2014;Coleman et al. 2019), RNA and phosphodiester-based energy coupling (e.g.Werner and Grohmann 2011), as well as thioester-based intermediary metabolism (Goldford et al. 2017;Weiss et al. 2018), but may not have used a strictly DNA genome (Mushegian and Koonin 1996;Leipe et”
From The Emergence of Life (2019) · cites this paper as Leipe et al. 1999
DNA as the primary information storage molecule evolved independently in bacteria and archaea.
“The fact that the mechanisms of DNA replication in bacteria and archaea are different [133] suggests the possibility that DNA, as the primary information storage molecule, evolved independently in each of these lineages [133,134,135].”
From Opinion: The Key Steps in the Origin of Life to the Formation of the Eukaryotic Cell (2024) · cites this paper as [134]
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Bleichert, F., Botchan, M. R., & Berger, J. M. (2017) · Science · doi:10.1126/science.aah6317 · Cited by 220 · see citing works
“Despite the clear functional conservation of core replisomal activities, the helicases and primase/polymerases used for replicating DNA have evolved twice independently, with bacteria using one class of enzymes and archaea/eukaryotes using another (2).”
BackgroundFilée, J., Forterre, P., Sen-Lin, T., & Laurent, J. (2002) · Journal of Molecular Evolution · doi:10.1007/s00239-001-0078-x · Cited by 247 · see citing works
Wolf, Y. I., & Koonin, E. V. (2007) · Biology Direct · doi:10.1186/1745-6150-2-14 · Cited by 235 · see citing works
“Thus, plausible, even if conflicting, accounts of the emergence of these systems have been derived from comparative-genomic data and evolutionary reasoning [70,140-144].”
BackgroundSelf-citationEukaryotic DNA replication control: Lock and load, then fire
Remus, D., & Diffley, J. F. X. (2009) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2009.08.002 · Cited by 245 · see citing works
“Distinct helicase mechanisms may require distinct helicase loading mechanisms in bacteria and eukaryotes Surprisingly, whilst DnaA and ORC (subunits 1–5) belong to the same clade of AAA+ ATPases [8], the respective replicative helicases DnaB and Mcm2-7 are not orthologous [9].”
BackgroundVirus World as an Evolutionary Network of Viruses and Capsidless Selfish Elements
Koonin, E. V., & Dolja, V. V. (2014) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00049-13 · Cited by 242 · see citing works
“Most likely, retroelements have been an integral part of biological systems since the stage of the primordial replicators, when they actually gave rise to the first DNA genomes (125).”
BackgroundSelf-citationBacterial Mode of Replication with Eukaryotic-Like Machinery in a Hyperthermophilic Archaeon
Myllykallio, H., Lopez, P., López‐García, P., Heilig, R., Saurin, W., Zivanovic, Y., Philippe, H., & Forterre, P. (2000) · Science · doi:10.1126/science.288.5474.2212 · Cited by 244 · see citing works
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From volcanic origins of chemoautotrophic life to Bacteria, Archaea and Eukarya
Wächtershäuser, G. (2006) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2006.1904 · Cited by 275 · see citing works
“In both the Bacteria and Archaea, non-homologous enzyme complexes for DNA replication (Leippe et al. 1999) with coordinated leading strand and lagging strand synthesis departed from the much simpler system of rolling circle replication of the pre-cells, perhaps under the directing influence of the two different kinds…”
BackgroundThree monophyletic superfamilies account for the majority of the known glycosyltransferases
Liu, J., & Mushegian, A. R. (2003) · Protein Science · doi:10.1110/ps.0302103 · Cited by 235 · see citing works
“…a nucleotidyltransferase involved in copying its genomic nucleic acid; it has been proposed that such copying proceeded via an RNA intermediate (Leipe et al. 1999), and that said nucleotidyltransferase more than likely was of the palm-domain ferredoxin-like fold, consisting of four- or…”
BackgroundStructure and Function of Cdc6/Cdc18
Liu, J., Smith, C. L., DeRyckere, D., et al. (2000) · Molecular Cell · doi:10.1016/s1097-2765(00)00062-9 · Cited by 227 · see citing works
Evolutionary genomics of archaeal viruses: Unique viral genomes in the third domain of life
Prangishvili, D. A., Garrett, R. A., & Koonin, E. V. (2006) · Virus Research · doi:10.1016/j.virusres.2006.01.007 · Cited by 218 · see citing works
Self-citationInventing the dynamo machine: the evolution of the F-type and V-type ATPases
Mulkidjanian, A. Y., Makarova, K. S., Galperin, M. Y., & Koonin, E. V. (2007) · Nature Reviews Microbiology · doi:10.1038/nrmicro1767 · Cited by 210 · see citing works
Self-citationBacteriophage replication modules
Weigel, C., & Seitz, H. (2006) · FEMS Microbiology Reviews · doi:10.1111/j.1574-6976.2006.00015.x · Cited by 196 · see citing works
“…when compared with archaea and eukarya, in marked contrast to the considerable orthology found for proteins of the other two major information processing systems – translation and transcription – in all three domains (Edgell & Doolittle, 1997; Leipe et al., 1999; Tye, 2000; Woese, 2000, 2002).”
BackgroundAn origin-of-life reactor to simulate alkaline hydrothermal vents
Herschy, B., Whicher, A., Camprubi, E., Watson, C., Dartnell, L., Ward, J., Evans, J. R. G., & Lane, N. (2014) · Journal of Molecular Evolution · doi:10.1007/s00239-014-9658-4 · Cited by 194 · see citing works
“For example, most enzymes involved in DNA replication are not homologous in bacteria and archaea (Edgell and Doolittle 1997; Leipe et al. 1999).”
BackgroundBiophysical characterization of DNA binding from single molecule force measurements
Chaurasiya, K. R., Paramanathan, T., McCauley, M. J., et al. (2010) · Physics of Life Reviews · doi:10.1016/j.plrev.2010.06.001 · Cited by 192 · see citing works
“Although a crystal structure of residues 1–197 demonstrates that α subunit folds into the right-hand shape characteristic of DNA polymerases [282], the absence of significant sequence similarities between Pol III α and well-known DNA polymerases leaves DNA binding domains unclear [283].”
The origin of DNA genomes and DNA replication proteins
Forterre, P. (2002) · Current Opinion in Microbiology · doi:10.1016/s1369-5274(02)00360-0 · Cited by 190 · see citing works
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The replication clamp-loading machine at work in the three domains of life
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“Archaea contain a PCNA clamp and an RFC clamp loader that function with B-family DNA polymerase”
The bacterial replicative helicase DnaB evolved from a RecA duplication.
Leipe, D. D., Aravind, L., Grishin, N. V., & Koonin, E. V. (2000) · PubMed · Cited by 184 · see citing works
Self-citationMechanisms and regulation of DNA replication initiation in eukaryotes
Parker, M. W., Botchan, M. R., & Berger, J. M. (2017) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.1080/10409238.2016.1274717 · Cited by 186 · see citing works
“…eukaryotic kingdoms, there has been significant evolutionary diversification of the molecules that complete each task, to the point where it is now clear that aspects of the replicative machinery emerged twice, independently, during cellular evolution (Edgell & Doolittle, 1997; Leipe et al., 1999).”
BackgroundThe universal tree of life: an update
Forterre, P. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.00717 · Cited by 186 · see citing works
“Martin and colleagues recently reported a lack of correspondence between individual protein trees and the concatenation tree in several datasets of archaeal and bacterial proteins (Thiergart et al., 2014).”
BackgroundThe Deep Archaeal Roots of Eukaryotes
Yutin, N., Makarova, K. S., Mekhedov, S., Wolf, Y. I., & Koonin, E. V. (2008) · Molecular Biology and Evolution · doi:10.1093/molbev/msn108 · Cited by 181 · see citing works
“…in the form of homologous inserts in conserved proteins, indicate that, for the majority of these genes, the preferred tree topology is one with the eukaryotic branch placed outside the extant diversity of archaea although small subsets of genes show crenarchaeal and euryarchaeal affinities.”
BackgroundSelf-citationMechanisms for Initiating Cellular DNA Replication
Costa, A., Hood, I. V., & Berger, J. M. (2013) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-052610-094414 · Cited by 182 · see citing works
From pre‐cells to Eukarya – a tale of two lipids
Wächtershäuser, G. (2003) · Molecular Microbiology · doi:10.1046/j.1365-2958.2003.03267.x · Cited by 176 · see citing works
“Within the unitary populations of the Bacteria and Archaea enzyme complexes for modern DNA replication ( Leippe et al ., 1999 ) with co-ordinated leading strand and lagging strand synthesis departed independently from the much simpler system of rolling circle replication of the pre-cells.”
BackgroundEvolution of prokaryotic gene order: genome rearrangements in closely related species
Suyama, M., & Bork, P. (2001) · Trends in Genetics · doi:10.1016/s0168-9525(00)02159-4 · Cited by 169 · see citing works
Co-evolution of primordial membranes and membrane proteins
Mulkidjanian, A. Y., Galperin, M. Y., & Koonin, E. V. (2009) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2009.01.005 · Cited by 169 · see citing works
Self-citationCrystal Structure of the Catalytic α Subunit of E. coli Replicative DNA Polymerase III
Lamers, M. H., Georgescu, R. E., Lee, S.-G., O’Donnell, M. E., & Kuriyan, J. (2006) · Cell · doi:10.1016/j.cell.2006.07.028 · Cited by 167 · see citing works
Aravind, L., Anantharaman, V., & Koonin, E. V. (2002) · Proteins: Structure, Function, and Bioinformatics · doi:10.1002/prot.10064 · Cited by 153 · see citing works
“some of their central components probably evolving independently in the two principal lines of descent.(9)”
BackgroundSelf-citationThe origin of eukaryotes and their relationship with the Archaea: are we at a phylogenomic impasse?
Gribaldo, S., Poole, A. M., Daubin, V., Forterre, P., & Brochier‐Armanet, C. (2010) · Nature Reviews Microbiology · doi:10.1038/nrmicro2426 · Cited by 159 · see citing works
A Bioenergetic Basis for Membrane Divergence in Archaea and Bacteria
Sojo, V., Pomiankowski, A., & Lane, N. (2014) · PLoS Biology · doi:10.1371/journal.pbio.1001926 · Cited by 154 · see citing works
“ion pumping [13], and even DNA replication [14].”
BackgroundInfluentialInsertion Sequence Diversity in Archaea
Filée, J., Siguier, P., & Chandler, M. (2007) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00031-06 · Cited by 147 · see citing works
“This is perhaps surprising in view of the fact that Archaea have important similarities to Eukarya, notably enzymes involved in DNA replication (47).”
BackgroundBailey, S., Wing, R. A., & Steitz, T. (2006) · Cell · doi:10.1016/j.cell.2006.07.027 · Cited by 145 · see citing works
The NYN Domains: Novel Predicted RNAses with a PIN Domain-Like Fold
Anantharaman, V., & Aravind, L. (2006) · RNA Biology · doi:10.4161/rna.3.1.2548 · Cited by 143 · see citing works
Self-citationA planarian nidovirus expands the limits of RNA genome size
Saberi, A., Gulyaeva, A. A., Brubacher, J. L., Newmark, P. A., & Gorbalenya, A. E. (2018) · PLoS Pathogens · doi:10.1371/journal.ppat.1007314 · Cited by 138 · see citing works
“It is especially unclear whether RNA entities ever evolved genomes close to the 100–300 kilobase (kb) range [2, 3] of the “minimal” reconstructed cellular DNA genome [4].”
A cytoprotective perspective on longevity regulation
Shore, D. E., & Ruvkun, G. (2013) · Trends in Cell Biology · doi:10.1016/j.tcb.2013.04.007 · Cited by 137 · see citing works
Matsunaga, F., Forterre, P., Ishino, Y., & Myllykallio, H. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.191387498 · Cited by 135 · see citing works
The nature of the universal ancestor and the evolution of the proteome
Doolittle, W. F. (2000) · Current Opinion in Structural Biology · doi:10.1016/s0959-440x(00)00096-8 · Cited by 134 · see citing works
Comparative mechanistic studies of de novo RNA synthesis by flavivirus RNA-dependent RNA polymerases
Selisko, B., Dutartre, H., Guillemot, J., et al. (2006) · Virology · doi:10.1016/j.virol.2006.03.026 · Cited by 131 · see citing works
“They are essential to viral replication and present a unique evolutionary fate of being the only replicative RdRps preserved from the RNA world (Leipe et al., 1999).”
BackgroundOpen Questions on the Origin of Eukaryotes
López-García, P., & Moreira, D. (2015) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2015.09.005 · Cited by 135 · see citing works
Protein Superfamily Evolution and the Last Universal Common Ancestor (LUCA)
Ranea, J. A. G., Sillero, A., Thornton, J. M., & Orengo, C. A. (2006) · Journal of Molecular Evolution · doi:10.1007/s00239-005-0289-7 · Cited by 122 · see citing works
Phylogenomics of type II DNA topoisomerases
Gadelle, D., Filée, J., Buhler, C., & Forterre, P. (2003) · BioEssays · doi:10.1002/bies.10245 · Cited by 126 · see citing works
“This scenario is in agreement with the idea of a LUCA with an RNA genome((50))”
On the Origin of Cells and Viruses
Koonin, E. V. (2009) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.04992.x · Cited by 122 · see citing works
“(i) did not have a typical, large DNA genome, 22, 44 and/or (ii) was not a typical membrane-bounded cell (Fig.”
BackgroundSelf-citationMushegian, A. R. (1999) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(99)00023-4 · Cited by 120 · see citing works
The replication machinery of LUCA: common origin of DNA replication and transcription
Koonin, E. V., Krupovìč, M., Ishino, S., & Ishino, Y. (2020) · BMC Biology · doi:10.1186/s12915-020-00800-9 · Cited by 110 · see citing works
Self-citationThe Dispersed Archaeal Eukaryome and the Complex Archaeal Ancestor of EukaryotesPreprint
Koonin, E. V., & Yutin, N. (2014) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a016188 · Cited by 116 · see citing works
“…thus, the key proteins involved in DNA replication in Archaea and eukaryotes are not homologous to the functionally analogous proteins of Bacteria (Leipe et al. 1999), and conversely, some of the principal enzymes of membrane biogenesis are homologous in eukaryotes and Bacteria but not in…”
BackgroundSelf-citationBecerra, A., Delaye, L., Islas, S., & Lazcano, A. (2007) · Annual Review of Ecology, Evolution, and Systematics · doi:10.1146/annurev.ecolsys.38.091206.095825 · Cited by 115 · see citing works
The Biological Big Bang model for the major transitions in evolution
Koonin, E. V. (2007) · Biology Direct · doi:10.1186/1745-6150-2-21 · Cited by 115 · see citing works
“Subsequently, the notion of a "communal ancestor" has been developed into a specific scenario [16,19] that derived from the comparative-genomic indications that the enzymes of membrane biogenesis and the core DNA replication machineries in archaea and bacteria were nonhomologous [18,42].”
BackgroundSelf-citationATPase switches controlling DNA replication initiation
Lee, D. G., & Bell, S. P. (2000) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(00)00089-2 · Cited by 114 · see citing works
The LUCA and its complex virome
Krupovìč, M., Dolja, V. V., & Koonin, E. V. (2020) · Nature Reviews Microbiology · doi:10.1038/s41579-020-0408-x · Cited by 110 · see citing works
“The fact that the replicative DNA polymerases (DNAPs) of bacteria, archaea and eukaryotes are not homologous has prompted ideas of an RNA-based LUCA 31,34,35 .”
Self-citationForterre, P., Brochier‐Armanet, C., & Philippe, H. (2002) · Theoretical Population Biology · doi:10.1006/tpbi.2002.1592 · Cited by 112 · see citing works
“This is especially striking in the case of DNA replication, since archaeal genomes encode homologues of nearly all eukaryal DNA replication proteins but only one homologue of a bacterial DNA replication protein (Edgell and Doolittle, 1997; Forterre, 1999; Leipe et al., 1999).”
BackgroundTahirov, T. H., Makarova, K. S., Rogozin, I. B., Pavlov, Y. I., & Koonin, E. V. (2009) · Biology Direct · doi:10.1186/1745-6150-4-11 · Cited by 110 · see citing works
“The replicative polymerases are sharply divided between the bacterial and archaealeukaryotic types that appear not to be homologous [7,8].”
Self-citationThe ring-shaped hexameric helicases that function at DNA replication forks
O’Donnell, M. E., & Li, H. (2018) · Nature Structural & Molecular Biology · doi:10.1038/s41594-018-0024-x · Cited by 109 · see citing works
Matsunaga, F., Norais, C. A., Forterre, P., & Myllykallio, H. (2003) · EMBO Reports · doi:10.1038/sj.embor.embor732 · Cited by 109 · see citing works
“Together these observations have suggested that molecular processes for DNA replication in Bacteria and Eukarya might have independent origins (Leipe et al., 1999; Forterre, 1999).”
BackgroundCrystal structure of a DNA-dependent RNA polymerase (DNA primase).
Augustin, M. A., Huber, R., & Kaiser, J. T. (2001) · Nature Structural Biology · doi:10.1038/83060 · Cited by 104 · see citing works
Kazlauskas, D., Krupovìč, M., & Venclovas, Č. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw322 · Cited by 103 · see citing works
“One of the outstanding questions in Biology is the origin of the two evolutionarily distinct DNA replication systems in bacteria and archaea/eukaryotes, respectively (4,68).”
BackgroundA novel type of replicative enzyme harbouring ATPase, primase and DNA polymerase activity
Lipps, G., Röther, S., Hart, C., & Krauss, G. (2003) · The EMBO Journal · doi:10.1093/emboj/cdg246 · Cited by 102 · see citing works
Primase-polymerases are a functionally diverse superfamily of replication and repair enzymes
Guilliam, T. A., Keen, B. A., Brissett, N. C., & Doherty, A. J. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv625 · Cited by 99 · see citing works
“This observation led to a hypothesis that the two replicative systems evolved twice independently from a common ancestor which utilized reverse transcription to replicate an RNA/DNA genome (27) (Figure 3A).”
BackgroundResultPodobnik, M., McInerney, P., O’Donnell, M. E., et al. (2000) · Journal of Molecular Biology · doi:10.1006/jmbi.2000.3844 · Cited by 99 · see citing works
“Bacterial and bacteriophage primases of the DnaG family have no apparent relationship to eukaryotic and archaebacterial primases, or to any other RNA or DNA polymerases (Aravind et al., 1998; Leipe et al., 1999).”
BackgroundNovel endonuclease in Archaea cleaving DNA with various branched structure.
Komori, K., Fujikane, R., Shinagawa, H., & Ishino, Y. (2002) · Genes & Genetic Systems · doi:10.1266/ggs.77.227 · Cited by 96 · see citing works
“However, many genes encoding proteins sharing sequence similarities with eukaryotic DNA replication proteins are present in all archaeal genomes (Olsen and Woese, 1997; Edgell and Doolittle, 1997; Ishino and Cann, 1998; Cann and Ishino, 1999, Leipe et al., 1999).”
BackgroundComparative genomics of Archaea: how much have we learned in six years, and what's next?
Makarova, K. S., & Koonin, E. V. (2003) · Genome biology · doi:10.1186/gb-2003-4-8-115 · Cited by 94 · see citing works
“This observation led to the hypothesis that replication of doublestranded DNA as the principal form of replication of the genetic material was ‘invented’ twice, independently: once in bacteria and once in the ancestor of archaea and eukaryotes [22,23].”
BackgroundSelf-citationDiversity and evolution of B-family DNA polymerases
Kazlauskas, D., Krupovìč, M., Guglielmini, J., Forterre, P., & Venclovas, Č. (2020) · Nucleic Acids Research · doi:10.1093/nar/gkaa760 · Cited by 85 · see citing works
“taken from the literature (7,69) or are named after the secondary structure elements of PolDelta (Supplementary Figure S1).”
BackgroundGiraldo, R. (2003) · FEMS Microbiology Reviews · doi:10.1111/j.1574-6976.2003.tb00629.x · Cited by 88 · see citing works
“In particular, the presence of common structural domains in this kind of OBPs, beyond their marginal sequence similarities, leaves the way open to discuss their possible phylogenetic relationships [8,9].”
BackgroundRNA damage in biological conflicts and the diversity of responding RNA repair systems
Burroughs, A. M., & Aravind, L. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw722 · Cited by 87 · see citing works
“Both sequence and structural evidence favors the deepest split among nucleic acid ligases as being between the ATPdependent and NAD-dependent DNA ligases (Figure 6D), which act as the primary DNA ligase respectively in the archaeo-eukaryotic and bacterial clades (292).”
BackgroundSelf-citationHistone deacetylases in fungi: novel members, new facts
Trojer, P. (2003) · Nucleic Acids Research · doi:10.1093/nar/gkg473 · Cited by 86 · see citing works
The Last Common Ancestor: What's in a name?
Delaye, L., Becerra, A., & Lazcano, A. (2005) · Origins of Life and Evolution of Biospheres · doi:10.1007/s11084-005-5760-3 · Cited by 83 · see citing works
“…and his collaborators analyzed a large set of primases, replicative polymerases, and other proteins involved in DNA replication, and suggested an alternative scheme with a hybrid RNA/DNA cenancestral genetic system whose complex replication cycle involved reverse transcription (Leipe et al., 1999).”
BackgroundInfluentialCamprubí, E., de Leeuw, J. W., House, C. H., Raulin, F., Russell, M. J., Spang, A., Tirumalai, M. R., & Westall, F. (2019) · Space Science Reviews · doi:10.1007/s11214-019-0624-8 · Cited by 84 · see citing works
RNA topoisomerase is prevalent in all domains of life and associates with polyribosomes in animals
Ahmad, M., Xue, Y., Lee, S. K., Martindale, J. L., Shen, W., Li, W., Zou, S., Ciaramella, M., Debat, H., Nadal, M., et al. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw508 · Cited by 85 · see citing works
“It has also been hypothesized that LU-CAs may have an RNA genome, or an RNA / DNA hybrid genome, or a DNA genome with an RNA replication intermediate (53,56,57) (Figure 7B).”
Archaeology of Eukaryotic DNA Replication
Makarova, K. S., & Koonin, E. V. (2013) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a012963 · Cited by 87 · see citing works
“Generally, the archaeal replication protein core appears to be the same as the eukaryotic core, but eukaryotes typically possess multiple paralogous subunits within complexes that are homomeric in archaea, many additional components interacting with the core ones and more complex regulation (Leipe et al. 1999; Bell an…”
BackgroundSelf-citationCrystal Structure of the Human Primase
Baranovskiy, A. G., Zhang, Y., Suwa, Y., et al. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.624742 · Cited by 83 · see citing works
“Most structural elements contributing to NTP and DNA binding by the large subunit are located in the C-terminal half of the protein (p58C in human primase) (11, 17–20).”
BackgroundResultInfluentialPoole, A. M., & Logan, D. T. (2005) · Molecular Biology and Evolution · doi:10.1093/molbev/msi132 · Cited by 82 · see citing works
Comprehensive analysis of DNA polymerase III α subunits and their homologs in bacterial genomes
Timinskas, K., Balvociute, M., Timinskas, A., & Venclovas, Č. (2013) · Nucleic Acids Research · doi:10.1093/nar/gkt900 · Cited by 82 · see citing works
Liu, L., Komori, K., Ishino, S., Bocquier, A. A., Cann, I., Kohda, D., & Ishino, Y. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m106391200 · Cited by 81 · see citing works
- Authors
- Leipe, D. D., Aravind, L., & Koonin, E. V.
- Affiliations
- National Institutes of Health (US)
- Texas A&M University (US)
- Corresponding author
- Koonin, E. V.
- Venue
- Nucleic Acids Research
- Publisher
- Oxford University Press (OUP)
- Published
- 1999-09-01
- Volume
- 27
- Issue
- 17
- Pages
- 3389-3401
- ISSN
- 0305-1048 (ISSN-L)
- 1362-4962
- PMC
- PMC148579
- OpenAlex
- W2018024025
- Semantic Scholar
- 9f9be31d2a06621cfbcaa7642db469b8cea929dc
- Cited by
- 351
- References
- 66
- Citations by year
- 2026: 6 · 2025: 5 · 2024: 16 · 2023: 5 · 2022: 5 · 2021: 11 · 2020: 10 · 2019: 6 · 2018: 12 · 2017: 13 · 2016: 15 · 2015: 13 · 2014: 18 · 2013: 12 · 2012: 5
- FWCI
- 13.34
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Nucleic Acids Research (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Physical Sciences › Physics and Astronomy › Astronomy and Astrophysics › Origins and Evolution of Life
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Keywords
- DNA replication, origin of replication, convergent evolution, last common ancestor, primase, replicative helicase, proofreading exonuclease, DNA ligase, RNA-DNA hybrids, reverse transcription, sequence conservation
- MeSH terms
- Animals, Bacterial Proteins, Cytoplasm, DNA Replication, Drosophila, Fungal Proteins, Models, Genetic, Sequence Homology, Nucleic Acid, Databases, Factual, Sequence Analysis, DNA, Evolution, Molecular, Archaeal Proteins
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