Phylogenomics of type II DNA topoisomerases

Gadelle, Danièle; Filée, Jonathan; Buhler, Cyril; Forterre, Patrick

doi:10.1002/bies.10245

Cited by 111 publications

(100 citation statements)

References 61 publications

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“…These proteins have retained the typical signature of their original domain within the new setting, explaining why HGT can be detected via phylogenetic analyses. For instance, archaeal aminoacyl tRNA synthetases present in Bacteria, or bacterial DNA gyrase present in Archaea, cannot be distinguished from their homologues in their respective domain of origin (5,18).…”

Section: Why Does Canonical Pattern Exist?mentioning

confidence: 99%

“…Indeed, the overall picture becomes more complex when proteins involved in DNA replication, recombination, or repair (DNA informational proteins) are taken into account. The reason is that many DNA informational proteins do not display the classical pattern, i.e., three homologous versions (one for each domain) (18)(19)(20)(21)(22). In particular, the major proteins involved in bacterial DNA replication (DNA polymerase, primase, and helicase) are not homologous to their archaeal͞eukaryal counterparts (i.e., there is only one version of the DnaG primase, the bacterial one, and two versions of the archaeal͞eukaryal primase).…”

Section: The Multiple Versions and Erratic Distribution Of Dna Informmentioning

confidence: 99%

“…Generally speaking, cellular DNA informational proteins are often found in only one or two versions, instead of three. For instance, there are only two versions of cellular type II DNA topoisomerases of the A family, one in Bacteria and Archaea and another in Eukarya (18). Furthermore, many DNA informational proteins exist in different nonhomologous families (usually with several versions for one family).…”

Section: The Multiple Versions and Erratic Distribution Of Dna Informmentioning

confidence: 99%

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Three RNA cells for ribosomal lineages and three DNA viruses to replicate their genomes: A hypothesis for the origin of cellular domain

Forterre

2006

Proc. Natl. Acad. Sci. U.S.A.

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214

175

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The division of the living world into three cellular domains, Archaea, Bacteria, and Eukarya, is now generally accepted. However, there is no consensus about the evolutionary relationships among these domains, because all of the proposed models have a number of more or less severe pitfalls. Another drawback of current models for the universal tree of life is the exclusion of viruses, otherwise a major component of the biosphere. Recently, it was suggested that the transition from RNA to DNA genomes occurred in the viral world, and that cellular DNA and its replication machineries originated via transfers from DNA viruses to RNA cells. Here, I explore the possibility that three such independent transfers were at the origin of Archaea, Bacteria, and Eukarya, respectively. The reduction of evolutionary rates following the transition from RNA to DNA genomes would have stabilized the three canonical versions of proteins involved in translation, whereas the existence of three different founder DNA viruses explains why each domain has its specific DNA replication apparatus. In that model, plasmids can be viewed as transitional forms between DNA viruses and cellular chromosomes, and the formation of different levels of cellular organization (prokaryote or eukaryote) could be traced back to the nature of the founder DNA viruses and RNA cells.

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Section: Why Does Canonical Pattern Exist?mentioning

confidence: 99%

Section: The Multiple Versions and Erratic Distribution Of Dna Informmentioning

confidence: 99%

Section: The Multiple Versions and Erratic Distribution Of Dna Informmentioning

confidence: 99%

See 1 more Smart Citation

Three RNA cells for ribosomal lineages and three DNA viruses to replicate their genomes: A hypothesis for the origin of cellular domain

Forterre

2006

Proc. Natl. Acad. Sci. U.S.A.

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214

175

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“…The function of topo II's C-terminal region is not well understood, except that it is implicated in the regulation of topo II (25). Recent studies on two other closely related type IIA topos, DNA gyrase and topo IV, suggest that their C-terminal domains bind and bend DNA to correctly position substrate DNA for the enzymatic reaction (26,27).…”

Section: Hyp7 Is Essential For Successive Endocycles Beyond 8cmentioning

confidence: 99%

RHL1 is an essential component of the plant DNA topoisomerase VI complex and is required for ploidy-dependent cell growth

Sugimoto‐Shirasu

Roberts

Stacey

et al. 2005

Proc. Natl. Acad. Sci. U.S.A.

106

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How cells achieve their final sizes is a pervasive biological question. One strategy to increase cell size is for the cell to amplify its chromosomal DNA content through endoreduplication cycles. Although endoreduplication is widespread in eukaryotes, we know very little about its molecular mechanisms. Successful progression of the endoreduplication cycle in Arabidopsis requires a plant homologue of archaeal DNA topoisomerase (topo) VI. To further understand how DNA is endoreduplicated and how this process is regulated, we isolated a dwarf Arabidopsis mutant, hyp7 (hypocotyl 7), in which various large cell types that in the wild type normally endoreduplicate multiple times complete only the first two rounds of endoreduplication and stall at 8C. HYP7 encodes the RHL1 (ROOT HAIRLESS 1) protein, and sequence analysis reveals that RHL1 has similarity to the C-terminal domain of mammalian DNA topo II␣, another type II topo that shares little sequence homology with topo VI. RHL1 shows DNA binding activity in vitro, and we present both genetic and in vivo evidence that RHL1 forms a multiprotein complex with plant topo VI. We propose that RHL1 plays an essential role in the topo VI complex to modulate its function and that the two distantly related topos, topo II and topo VI, have evolved a common domain that extends their function. Our data suggest that plant topo II and topo VI play distinct but overlapping roles during the mitotic cell cycle and endoreduplication cycle.endoreduplication ͉ hypocotyl ͉ root hairless T he control of cell size is a highly regulated process with inputs from genetic, hormonal, and environmental cues. Yeast and mammalian cells usually only double their size during their development; therefore, a key question in their size control is how proliferating cells coordinate cell growth and cell division to maintain size homeostasis. Yeast and many mammalian cells have a cell size checkpoint mechanism in which cells divide only when they reach a critical size (1), whereas some mammalian cells may control their size through extracellular signals (2). Although plant cells also double their cell size during proliferation, they commonly undergo an additional, massive (sometimes Ͼ1,000-fold), postmitotic cell enlargement. Such a large increase in volume is driven by a combination of production of new cytoplasmic mass and cell expansion (driven by water uptake and vacuolar growth), but little is known about the underlying mechanisms involved. Recent genetic evidence strongly supports the classical ''karyoplasmic ratio'' theory that one mechanism to increase cell size is by increasing the ploidy level within a cell, for example through endoreduplication, defined as the amplification of chromosomal DNA without corresponding cell division (3). Several mutants and transgenic plants that have aberrant levels of endoreduplication have been isolated and have led to the identification of key regulators of the endoreduplication cycle or endocycle (3-7). How these regulators control downstream events, however, rem...

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“…Multiple sequence alignment revealed that, although most functional domains are conserved in all type IIA enzymes, the highly charged C-terminal domain (CTD) of the eukaryotic Topo has no detectable sequence similarity with the corresponding regions in either DNA gyrase or Topo IV (20). Instead of involving catalysis, various studies have suggested that the intracellular localization of eukaryotic Topo IIA is regulated by its CTD (21)(22)(23)(24).…”

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confidence: 99%

Structure of the Topoisomerase IV C-terminal Domain

Hsieh

Farh

Huang

et al. 2004

Journal of Biological Chemistry

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Bacteria possess two closely related yet functionally distinct essential type IIA topoisomerases (Topos). DNA gyrase supports replication and transcription with its unique supercoiling activity, whereas Topo IV preferentially relaxes (؉) supercoils and is a decatenating enzyme required for chromosome segregation. Here we report the crystal structure of the C-terminal domain of Topo IV ParC subunit (ParC-CTD) from Bacillus stearothermophilus and provide a structure-based explanation for how Topo IV and DNA gyrase execute distinct activities. Although the topological connectivity of ParC-CTD is similar to the recently determined CTD structure of DNA gyrase GyrA subunit (GyrA-CTD), ParC-CTD surprisingly folds as a previously unseen broken form of a six-bladed ␤-propeller. Propeller breakage is due to the absence of a DNA gyrase-specific GyrA box motif, resulting in the reduction of curvature of the proposed DNA binding region, which explains why ParC-CTD is less efficient than GyrA-CTD in mediating DNA bending, a difference that leads to divergent activities of the two homologous enzymes. Moreover, we found that the topology of the propeller blades observed in ParC-CTD and GyrA-CTD can be achieved from a concerted ␤-hairpin invasion-induced fold change event of a canonical six-bladed ␤-propeller; hence, we proposed to name this new fold as "hairpininvaded ␤-propeller" to highlight the high degree of similarity and a potential evolutionary linkage between them. The possible role of ParC-CTD as a geometry facilitator during various catalytic events and the evolutionary relationships between prokaryotic type IIA Topos have also been discussed according to these new structural insights.

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Phylogenomics of type II DNA topoisomerases

Cited by 111 publications

References 61 publications

Three RNA cells for ribosomal lineages and three DNA viruses to replicate their genomes: A hypothesis for the origin of cellular domain

Three RNA cells for ribosomal lineages and three DNA viruses to replicate their genomes: A hypothesis for the origin of cellular domain

RHL1 is an essential component of the plant DNA topoisomerase VI complex and is required for ploidy-dependent cell growth

Structure of the Topoisomerase IV C-terminal Domain

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