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Tyrosine Recombinase Retrotransposons and Transposons

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  • Authors: Russell T. M. Poulter1, Margi I. Butler2
  • Editors: Alan Lambowitz3, Nancy Craig4
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    Affiliations: 1: Department of Biochemistry, University of Otago, Dunedin 9054, New Zealand; 2: Department of Biochemistry, University of Otago, Dunedin 9054, New Zealand; 3: University of Texas, Austin, TX; 4: Johns Hopkins University, Baltimore, MD
    • Source: microbiolspec March 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0036-2014
  • Received 12 June 2014 Accepted 04 August 2014 Published 05 March 2015
  • Margi Butler, [email protected]
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  • Abstract:

    Retrotransposons carrying tyrosine recombinases (YR) are widespread in eukaryotes. The first described tyrosine recombinase mobile element, DIRS1, is a retroelement from the slime mold . The YR elements are bordered by terminal repeats related to their replication via free circular dsDNA intermediates. Site-specific recombination is believed to integrate the circle without creating duplications of the target sites. Recently a large number of YR retrotransposons have been described, including elements from fungi (mucorales and basidiomycetes), plants (green algae) and a wide range of animals including nematodes, insects, sea urchins, fish, amphibia and reptiles. YR retrotransposons can be divided into three major groups: the DIRS elements, PAT-like and the Ngaro elements. The three groups form distinct clades on phylogenetic trees based on alignments of reverse transcriptase/ribonuclease H (RT/RH) and YR sequences, and also having some structural distinctions. A group of eukaryote DNA transposons, cryptons, also carry tyrosine recombinases. These DNA transposons do not encode a reverse transcriptase. They have been detected in several pathogenic fungi and oomycetes. Sequence comparisons suggest that the crypton YRs are related to those of the YR retrotransposons. We suggest that the YR retrotransposons arose from the combination of a crypton-like YR DNA transposon and the RT/RH encoding sequence of a retrotransposon. This acquisition must have occurred at a very early point in the evolution of eukaryotes.

  • Citation: Poulter R, Butler M. 2015. Tyrosine Recombinase Retrotransposons and Transposons. Microbiol Spectrum 3(2):MDNA3-0036-2014. doi:10.1128/microbiolspec.MDNA3-0036-2014.

References

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2015-03-05
2021-04-18

Abstract:

Retrotransposons carrying tyrosine recombinases (YR) are widespread in eukaryotes. The first described tyrosine recombinase mobile element, DIRS1, is a retroelement from the slime mold . The YR elements are bordered by terminal repeats related to their replication via free circular dsDNA intermediates. Site-specific recombination is believed to integrate the circle without creating duplications of the target sites. Recently a large number of YR retrotransposons have been described, including elements from fungi (mucorales and basidiomycetes), plants (green algae) and a wide range of animals including nematodes, insects, sea urchins, fish, amphibia and reptiles. YR retrotransposons can be divided into three major groups: the DIRS elements, PAT-like and the Ngaro elements. The three groups form distinct clades on phylogenetic trees based on alignments of reverse transcriptase/ribonuclease H (RT/RH) and YR sequences, and also having some structural distinctions. A group of eukaryote DNA transposons, cryptons, also carry tyrosine recombinases. These DNA transposons do not encode a reverse transcriptase. They have been detected in several pathogenic fungi and oomycetes. Sequence comparisons suggest that the crypton YRs are related to those of the YR retrotransposons. We suggest that the YR retrotransposons arose from the combination of a crypton-like YR DNA transposon and the RT/RH encoding sequence of a retrotransposon. This acquisition must have occurred at a very early point in the evolution of eukaryotes.

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Tyrosine Recombinase Retrotransposons and Transposons
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Citation: Poulter R, Butler M. 2015. Tyrosine recombinase retrotransposons and transposons. microbiolspec 3(2): doi:10.1128/microbiolspec.MDNA3-0036-2014
/content/microbiolspec/10.1128/microbiolspec.MDNA3-0036-2014.fig1
FIGURE 1
Structures of YR-encoding elements discussed in this chapter. These include: members of the DIRS-like group with ITRs and an ICR, a PAT-like element with ‘split’ direct repeats (SpPat1); Ngaro elements with ‘split’ direct repeats; a YR-encoding DNA transposon from (Crypton_Cn1). Repeat sequences are represented by boxed triangles. Shaded boxes represent ORFs. V-shaped lines represent introns. In the crypton, the stippled box represents the YR-encoding region, while the hatched box represents a putative DNA-binding domain.
microbiolspec/3/2/MDNA3-0036-2014-fig1_thmb.gif
microbiolspec/3/2/MDNA3-0036-2014-fig1.gif
Image of FIGURE 1

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FIGURE 1

Structures of YR-encoding elements discussed in this chapter. These include: members of the DIRS-like group with ITRs and an ICR, a PAT-like element with ‘split’ direct repeats (SpPat1); Ngaro elements with ‘split’ direct repeats; a YR-encoding DNA transposon from (Crypton_Cn1). Repeat sequences are represented by boxed triangles. Shaded boxes represent ORFs. V-shaped lines represent introns. In the crypton, the stippled box represents the YR-encoding region, while the hatched box represents a putative DNA-binding domain.

Source: microbiolspec March 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0036-2014
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/content/microbiolspec/10.1128/microbiolspec.MDNA3-0036-2014.fig2
FIGURE 2
Alignment of tyrosine recombinase conserved domains. A comparison of aligned tyrosine recombinase sequences from retrotransposons and DNA transposons with those from prokaryotes. Four regions of the recombinases are illustrated; the dashed lines common to all elements represent intervening regions of variable length. The conserved RHRY tetrad is denoted by *; the conserved CPV motif is overlined.
microbiolspec/3/2/MDNA3-0036-2014-fig2_thmb.gif
microbiolspec/3/2/MDNA3-0036-2014-fig2.gif
Image of FIGURE 2

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FIGURE 2

Alignment of tyrosine recombinase conserved domains. A comparison of aligned tyrosine recombinase sequences from retrotransposons and DNA transposons with those from prokaryotes. Four regions of the recombinases are illustrated; the dashed lines common to all elements represent intervening regions of variable length. The conserved RHRY tetrad is denoted by *; the conserved CPV motif is overlined.

Source: microbiolspec March 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0036-2014
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FIGURE 3
Relationships among YR-encoding retroelements. This phylogenetic tree is based on an alignment of the conserved RT and RH protein sequences. Sequences from three LTR retrotransposons have been used as an outgroup: sushi (AF030881), Ty3 (M23367) and gypsy (AF033821). The tree was constructed by the Neighbour-joining method using MEGA5 ( 46 ). Bootstrap support from 1050 replicates is indicated for branches with >50% support. Element descriptions can be found in Table 2 .
microbiolspec/3/2/MDNA3-0036-2014-fig3_thmb.gif
microbiolspec/3/2/MDNA3-0036-2014-fig3.gif
Image of FIGURE 3

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FIGURE 3

Relationships among YR-encoding retroelements. This phylogenetic tree is based on an alignment of the conserved RT and RH protein sequences. Sequences from three LTR retrotransposons have been used as an outgroup: sushi (AF030881), Ty3 (M23367) and gypsy (AF033821). The tree was constructed by the Neighbour-joining method using MEGA5 ( 46 ). Bootstrap support from 1050 replicates is indicated for branches with >50% support. Element descriptions can be found in Table 2 .

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FIGURE 4
Relationships among YR-encoding retrotransposons and DNA transposons. This phylogenetic tree is based on an alignment of the YR protein sequences. Sequences from prokaryote tyrosine recombinases have been used as an outgroup: Lambda recombinase (KDT52537), Tn916 from (U09422) and two tyrosine recombinases (XerC, CDL28161; XerD, CDL49882 ). The tree was constructed by the Neighbour-joining method using MEGA5 ( 46 ). Bootstrap support from 1050 replicates is indicated for branches with >50% support. Element descriptions can be found in Table 2 .
microbiolspec/3/2/MDNA3-0036-2014-fig4_thmb.gif
microbiolspec/3/2/MDNA3-0036-2014-fig4.gif
Image of FIGURE 4

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FIGURE 4

Relationships among YR-encoding retrotransposons and DNA transposons. This phylogenetic tree is based on an alignment of the YR protein sequences. Sequences from prokaryote tyrosine recombinases have been used as an outgroup: Lambda recombinase (KDT52537), Tn916 from (U09422) and two tyrosine recombinases (XerC, CDL28161; XerD, CDL49882 ). The tree was constructed by the Neighbour-joining method using MEGA5 ( 46 ). Bootstrap support from 1050 replicates is indicated for branches with >50% support. Element descriptions can be found in Table 2 .

Source: microbiolspec March 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0036-2014
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Tables

Tyrosine Recombinase Retrotransposons and Transposons
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Citation: Poulter R, Butler M. 2015. Tyrosine recombinase retrotransposons and transposons. microbiolspec 3(2): doi:10.1128/microbiolspec.MDNA3-0036-2014
/content/microbiolspec/10.1128/microbiolspec.MDNA3-0036-2014.T1
TABLE 1
DIRS-like elements in fish. All those in this table are from the Actinopterygii except (Sarcopterygii) and the little skate, (Chondrichthyes)
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TABLE 1

DIRS-like elements in fish. All those in this table are from the Actinopterygii except (Sarcopterygii) and the little skate, (Chondrichthyes)

Source: microbiolspec March 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0036-2014
/content/microbiolspec/10.1128/microbiolspec.MDNA3-0036-2014.T2
TABLE 2
Tyrosine recombinase-encoding (YR) elements used for phylogenetic analyses in this study. The sources of the sequence data are held in the Genbank accessions, references or database sources shown. Element names are generated from the initial of the genus and either 2 or 3 initial letters from the species name of the organism in which the element is found
Generic image for table

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TABLE 2

Tyrosine recombinase-encoding (YR) elements used for phylogenetic analyses in this study. The sources of the sequence data are held in the Genbank accessions, references or database sources shown. Element names are generated from the initial of the genus and either 2 or 3 initial letters from the species name of the organism in which the element is found

Source: microbiolspec March 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0036-2014

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