1887
No metrics data to plot.
The attempt to load metrics for this article has failed.
The attempt to plot a graph for these metrics has failed.

Tyrosine Recombinase Retrotransposons and Transposons

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.
  • PDF
    743.43 Kb
  • HTML
    159.20 Kb
  • XML
    123.24 Kb
  • Authors: Russell T. M. Poulter1, Margi I. Butler2
  • Editors: Alan Lambowitz3, Nancy Craig4
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    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, margi.butler@otago.ac.nz
image of Tyrosine Recombinase Retrotransposons and Transposons
    Preview this microbiology spectrum article:
    Zoom in
    Zoomout

    Tyrosine Recombinase Retrotransposons and Transposons, Page 1 of 2

    | /docserver/preview/fulltext/microbiolspec/3/2/MDNA3-0036-2014-1.gif /docserver/preview/fulltext/microbiolspec/3/2/MDNA3-0036-2014-2.gif
  • 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

1. Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P, Chalhoub B, Flavell A, Leroy P, Morgante M, Panaud O, Paux E, SanMiguel P, Schulman AH. 2007. A unified classification system for eukaryotic transposable elements. Nat Rev Genet 8(12):973–982. [PubMed][CrossRef]
2. Duncan L, Bouckaert K, Yeh F, Kirk DL. 2002. kangaroo a mobile element from Volvox carteri is a member of a newly recognized third class of retrotransposons. Genetics 162:1617–1630. [PubMed]
3. Goodwin TJ, Poulter RT. 2001. The DIRS1 group of retrotransposons. Mol Biol Evol 18:2067–2082. [PubMed][CrossRef]
4. Nunes-Düby SE, Kwon HJ, Tirumalai RS, Ellenberger T, Landy A. 1998. Similarities and differences among 105 members of the Int family of site-specific recombinases. Nucleic Acids Res 26:391–406. [PubMed][CrossRef]
5. Cappello J, Handelsman K, Lodish HF. 1985. Sequence of Dictyostelium DIRS-1: an apparent retrotransposon with inverted terminal repeats and an internal circle junction sequence. Cell 43:105–115. [PubMed][CrossRef]
6. de Chastonay Y, Felder H, Link C, Aeby P, Tobler H, Muller F. 1992. Unusual features of the retroid element PAT from the nematode Panagrellus redivivus. Nucleic Acids Res 20:1623–1628. [PubMed][CrossRef]
7. Ruiz-Perez VL, Murillo FJ, Torres-Martinez S. 1996. Prt1 an unusual retrotransposon-like sequence in the fungus Phycomyces blakesleeanus. Mol Gen Genet 253:324–333. [PubMed][CrossRef]
8. Goodwin TJ, Poulter RT. 2004. A new group of tyrosine recombinase-encoding retrotransposons. Mol Biol Evol 21:746–759. [PubMed][CrossRef]
9. Piednoël M, Gonçalves IR, Higuet D, Bonnivard E. 2011. Eukaryote DIRS1-like retrotransposons: an overview. BMC Genomics 12:621. [PubMed][CrossRef]
10. Goodwin TJD, Butler MI, Poulter RTM. 2003. Cryptons: a group of tyrosine recombinase-encoding DNA transposons from pathogenic fungi. Microbiology 149:3099–3109. [PubMed][CrossRef]
11. Poulter RT, Goodwin TJ. 2005. DIRS-1 and the other tyrosine recombinase retrotransposons. Cytogenet Genome Res 110:575–588. [PubMed][CrossRef]
12. Dugas JC, Ngai J. 2001. Analysis and characterization of an odorant receptor gene cluster in the zebrafish genome. Genomics 71:53–65. [PubMed][CrossRef]
13. Metcalfe CJ, Filée J, Germon I, Joss J, Casane D. 2012. Evolution of the Australian lungfish (Neoceratodus forsteri) genome: a major role for CR1 and L2 LINE elements. Mol Biol Evol 29:3529–3539. [PubMed][CrossRef]
14. Chalopin D, Fan S, Simakov O, Meyer A, Schartl M, Volff JN. 2013. Evolutionary active transposable elements in the genome of the coelacanth. J Exp Zool, Part B 322:322–333. doi:10.1002/jez.b.22521. [PubMed][CrossRef]
15. Detrich HW, Amemiya CT. 2010. Antarctic Notothenioid Fishes: Genomic Resources and Strategies for Analyzing an Adaptive Radiation. Integr Comp Biol 50:1009–1017. [PubMed][CrossRef]
16. Hellsten U, Harland RM, Gilchrist MJ, Hendrix D, Jurka J, Kapitonov V, Ovcharenko I, Putnam NH, Shu S, Taher L, Blitz IL, Blumberg B, Dichmann DS, Dubchak I, Amaya E, Detter JC, Fletcher R, Gerhard DS, Goodstein D, Graves T, Grigoriev IV, Grimwood J, Kawashima T, Lindquist E, Lucas SM, Mead PE, Mitros T, Ogino H, Ohta Y, Poliakov AV, Pollet N, Robert J, Salamov A, Sater AK, Schmutz J, Terry A, Vize PD, Warren WC, Wells D, Wills A, Wilson RK, Zimmerman LB, Zorn AM, Grainger R, Grammer T, Khokha MK, Richardson PM, Rokhsar DS. 2010. The genome of the Western clawed frog Xenopus tropicalis. Science 328(5978):633–636. [PubMed][CrossRef]
17. Sun C, Shepard DB, Chong RA, López Arriaza J, Hall K, Castoe TA, Feschotte C, Pollock DD, Mueller RL. 2012. LTR retrotransposons contribute to genomic gigantism in plethodontid salamanders. Genome Biol Evol 4(2):168–183. [PubMed][CrossRef]
18. Castoe TA, Hall KT, Guibotsy Mboulas ML, Gu W, de Koning AP, Fox SE, Poole AW, Vemulapalli V, Daza JM, Mockler T, Smith EN, Feschotte C, Pollock DD. 2011. Discovery of highly divergent repeat landscapes in snake genomes using high-throughput sequencing. Genome Biol Evol 3:641–653. [PubMed][CrossRef]
19. Shedlock AM. Phylogenomic investigation of CR1 LINE diversity in reptiles. 2006. Syst Biol 55(6):902–911. [PubMed][CrossRef]
20. Goodwin TJ, Poulter RT, Lorenzen MD, Beeman RW. 2004. DIRS retroelements in arthropods: identification of the recently active TcDirs1 element in the red flour beetle Tribolium castaneum. Mol Genet Genomics 272:47–56. [PubMed][CrossRef]
21. Piednoël M, Bonnivard E. 2009. DIRS1-like retrotransposons are widely distributed among Decapoda and are particularly present in hydrothermal vent organisms. BMC Evol Biol 9:86. [PubMed][CrossRef]
22. Rho M, Schaack S, Gao X, Kim S, Lynch M, Tang H. 2010. LTR retroelements in the genome of Daphnia pulex. BMC Genomics 11:425. [PubMed][CrossRef]
23. Zhang G, Fang X, Guo X, Li L, Luo R, Xu F, Yang P, Zhang L, Wang X, Qi H, Xiong Z, Que H, Xie Y, Holland PW, Paps J, Zhu Y, Wu F, Chen Y, Wang J, Peng C, Meng J, Yang L, Liu J, Wen B, Zhang N, Huang Z, Zhu Q, Feng Y, Mount A, Hedgecock D, Xu Z, Liu Y, Domazet-Lošo T, Du Y, Sun X, Zhang S, Liu B, Cheng P, Jiang X, Li J, Fan D, Wang W, Fu W, Wang T, Wang B, Zhang J, Peng Z, Li Y, Li N, Wang J, Chen M, He Y, Tan F, Song X, Zheng Q, Huang R, Yang H, Du X, Chen L, Yang M, Gaffney PM, Wang S, Luo L, She Z, Ming Y, Huang W, Zhang S, Huang B, Zhang Y, Qu T, Ni P, Miao G, Wang J, Wang Q, Steinberg CE, Wang H, Li N, Qian L, Zhang G, Li Y, Yang H, Liu X, Wang J, Yin Y, Wang J. 2012. The oyster genome reveals stress adaptation and complexity of shell formation. Nature 490(7418):49–54. [PubMed][CrossRef]
24. Takeuchi T, Kawashima T, Koyanagi R, Gyoja F, Tanaka M, Ikuta T, Shoguchi E, Fujiwara M, Shinzato C, Hisata K, Fujie M, Usami T, Nagai K, Maeyama K, Okamoto K, Aoki H, Ishikawa T, Masaoka T, Fujiwara A, Endo K, Endo H, Nagasawa H, Kinoshita S, Asakawa S, Watabe S, Satoh N. 2013. Draft genome of the pearl oyster Pinctada fucata: a platform for understanding bivalve biology. DNA Res 19(2):117–130. [PubMed][CrossRef]
25. Muszewska A, Steczkiewicz K, Ginalski K. 2013. DIRS and Ngaro Retrotransposons in Fungi. PLoS One 8(9):e76319. [PubMed][CrossRef]
26. Day A, Rochaix JD. 1991. A transposon with an unusual LTR arrangement from Chlamydomonas reinhardtii contains an internal tandem array of 76 bp repeats. Nucleic Acids Res 19:1259–1266. [PubMed][CrossRef]
27. Dishaw LJ, Mueller MG, Gwatney N, Cannon JP, Haire RN, Litman RT, Amemiya CT, Ota T, Rowen L, Glusman G, Litman GW. 2008. Genomic complexity of the variable region containing chitin-binding proteins in amphioxus. BMC Genet 9:78. [PubMed][CrossRef]
28. Manfrin C, Tom M, De Moro G, Gerdol M, Guarnaccia C, Mosco A, Pallavicini A, Giulianini PG. 2013. Application of D-Crustacean Hyperglycemic Hormone Induces Peptidases Transcription and Suppresses Glycolysis-Related Transcripts in the Hepatopancreas of the Crayfish Pontastacus leptodactylus - Results of a Transcriptomic Study. PLoS One 8(6):e65176. [PubMed][CrossRef]
29. Lenz PH, Roncalli V, Hassett RP, Wu LS, Cieslak M C, Hartline DK, Christie AE. 2014. De Novo Assembly of a Transcriptome for Calanus finmarchicus (Crustacea, Copepoda), The Dominant Zooplankter of the North Atlantic Ocean. PLoS One 9(2):e88589. [PubMed][CrossRef]
30. Arkhipova IR, Pyatkov KI, Meselson M, Evgen'ev MB. 2003. Retroelements containing introns in diverse invertebrate taxa. Nat Genet 33:123–124. [PubMed][CrossRef]
31. Curcio MJ, Derbyshire KM. 2003. The outs and ins of transposition: from Mu to kangaroo. Nat Rev Mol Cell Biol 4:865–877. [PubMed][CrossRef]
32. Doak TG, Witherspoon DJ, Jahn CL, Herrick G. 2003. Selection on the genes of Euplotes crassus Tec1 and Tec2 transposons: evolutionary appearance of a programmed frameshift in a Tec2 gene encoding a tyrosine family site-specific recombinase. Eukaryotic Cell 2:95–102. [PubMed][CrossRef]
33. Kossykh VG, Schlagman SL, Hattman S. 1993. Conserved sequence motif DPPY in region IV of the phage T4 DAM DNA-[N6-adenine]-methyltransferase is important for S-adenosyl-L-methionine binding. Nucleic Acids Res 21:4659–4662. [PubMed][CrossRef]
34. Haas NB, Grabowski JM, Sivitz AB, Burch JBE. 1997. Chicken repeat 1 (CR1) elements which define an ancient family of vertebrate non-LTR retrotransposons. Microbiol Rev 21:157–178.
35. Poulter R, Butler M, Ormandy J. 1999. A LINE element from the pufferfish (fugu) Fugu rubripes that shows similarity to the CR1 family of non-LTR retrotransposons. Gene 227:169–179. [PubMed][CrossRef]
36. Kapitonov VV, Jurka J. 2003. The esterase and PHD domains in CR1-like non-LTR retrotransposons. Mol Biol Evol 20:38–46. [PubMed][CrossRef]
37. Huang Y-T, Liaw Y-C, Gorbatyuk VY, Huang TH. 2001. Backbone dynamics of Escherichia coli Thioesterase/ Protease I: evidence of a flexible active-site environment for a serine protease. J Mol Biol 307:1075–1090. [PubMed][CrossRef]
38. Ho YS, Swenson L, Derewenda L, Serre L, Wei Y, Dauter Z, Hattori M, Adachi T, Aoki J, Arai H, Inoue K, Derewenda ZS. 1997. Brain acetylhydrolase that inactivates platelet-activating factor is a G-protein-like trimer. Nature 385:89–93. [PubMed][CrossRef]
39. Fukuda K, Kiyokawa Y, Yanagiuchi T, Wakai Y, Kitamoto K, Inoue Y, Kimura A. 2000. Purification and characterization of isoamyl acetate-hydrolyzing esterase encoded by the IAH1 gene of Saccharomyces cerevisiae from a recombinant Escherichia coli. Appl Microbiol Biotechnol 53:596–600. [PubMed][CrossRef]
40. Bon E, Casaregola S, Blandin G, Llorente B, Neuvéglise C, Munsterkotter M, Guldener U, Mewes HW, Van Helden J, Dujon B, Gaillardin C. 2003. Molecular evolution of eukaryotic genomes: hemiascomycetous yeast spliceosomal introns. Nucleic Acids Res 31(4):1121–1135. [PubMed][CrossRef]
41. Huie MA, Baker HV. 1996. DNA-binding properties of the yeast transcriptional activator, Gcr1p. Yeast 12:307–317. [PubMed][CrossRef]
42. Huie MA, Scott EW, Drazinic CM, Lopez MC, Hornstra IK, Yang TP, Baker HV. 1992. Characterization of the DNA-binding activity of GCR1: in vivo evidence for two GCR1- binding sites in the upstream activating sequence of TP1 of Saccharomyces cerevisiae. Mol Cell Biol 12:2690–2700. [PubMed]
43. D'Souza CA, Kronstad JW, Taylor G, Warren R, Yuen M, Hu G, Jung WH, Sham A, Kidd SE, Tangen K, Lee N, Zeilmaker T, Sawkins J, McVicker G, Shah S, Gnerre S, Griggs A, Zeng Q, Bartlett K, Li W, Wang X, Heitman J, Stajich JE, Fraser JA, Meyer W, Carter D, Schein J, Krzywinski M, Kwon-Chung KJ, Varma A, Wang J, Brunham R, Fyfe M, Ouellette BF, Siddiqui A, Marra M, Jones S, Holt R, Birren BW, Galagan JE, Cuomo CA. 2011. Genome variation in Cryptococcus gattii, an emerging pathogen of immunocompetent hosts. mBio 2(1):e00342-10. [PubMed]
44. Kojima KK, Jurka J. 2011. Crypton transposons: identification of new diverse families and ancient domestication events. Mobile DNA 2(1):12. [PubMed][CrossRef]
45. Goodwin TJD, Ormandy JE, Poulter RT. 2001. L1-like non-LTR retrotransposons in the yeast Candida albicans. Curr Genet 39(2):83–91. [PubMed][CrossRef]
46. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. (2011) MEGA5: Molecular Evolutionary Genetics Analysis using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Mol Biol Evol 28:2731–2739. [PubMed][CrossRef]
microbiolspec.MDNA3-0036-2014.citations
cm/3/2
content/journal/microbiolspec/10.1128/microbiolspec.MDNA3-0036-2014
Loading

Citations loading...

Loading

Article metrics loading...

/content/journal/microbiolspec/10.1128/microbiolspec.MDNA3-0036-2014
2015-03-05
2017-06-25

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.

Highlighted Text: Show | Hide
Loading full text...

Full text loading...

/deliver/fulltext/microbiolspec/3/2/MDNA3-0036-2014.html?itemId=/content/journal/microbiolspec/10.1128/microbiolspec.MDNA3-0036-2014&mimeType=html&fmt=ahah

Figures

Image of FIGURE 1

Click to view

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. doi:10.1128/microbiolspec.MDNA3-0036-2014.f1

Source: microbiolspec March 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0036-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 2

Click to view

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. doi:10.1128/microbiolspec.MDNA3-0036-2014.f2

Source: microbiolspec March 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0036-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 3

Click to view

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 . doi:10.1128/microbiolspec.MDNA3-0036-2014.f3

Source: microbiolspec March 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0036-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 4

Click to view

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 . doi:10.1128/microbiolspec.MDNA3-0036-2014.f4

Source: microbiolspec March 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0036-2014
Permissions and Reprints Request Permissions
Download as Powerpoint

Tables

Generic image for table

Click to view

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
Generic image for table

Click to view

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

Supplemental Material

No supplementary material available for this content.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error