Horizontal Transfer of a Non-autonomous Helitron Among Insect and Viral Genomes

Overview

Journal BMC Genomics

Publisher Biomed Central

Specialty Genetics

Date 2015 Mar 14

PMID 25766741

Citations 15

Authors

Brad S Coates

Affiliations

Soon will be listed here.

Abstract

Background: The movement of mobile elements among species by horizontal transposon transfer (HTT) influences the evolution of genomes through the modification of structure and function. Helitrons are a relatively new lineage of DNA-based (class II) transposable elements (TEs) that propagate by rolling-circle replication, and are capable of acquiring host DNA. The rapid spread of Helitrons among animal lineages by HTT is facilitated by shuttling in viral particles or by unknown mechanisms mediated by close organism associations (e.g. between hosts and parasites).

Results: A non-autonomous Helitron independently annotated as BmHel-2 from Bombyx mori and the MITE01 element from Ostrinia nubilalis was predicted in the genomes of 24 species in the insect Order Lepidoptera. Integrated Helitrons retained ≥ 65% sequence identity over a 250 bp consensus, and were predicted to retain secondary structures inclusive of a 3'-hairpin and a 5'-subterminal inverted repeat. Highly similar Hel-2 copies were predicted in the genomes of insects and associated viruses, which along with a previous documented case of real-time virus-insect cell line transposition suggests that this Helitron has likely propagated by HTT.

Conclusions: These findings provide evidence that insect virus may mediate the HTT of Helitron-like TEs. This movement may facilitate the shuttling of DNA elements among insect genomes. Further sampling is required to determine the putative role of HTT in insect genome evolution.

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References

Vavre F, Fleury F, Lepetit D, Fouillet P, Bouletreau M . Phylogenetic evidence for horizontal transmission of Wolbachia in host-parasitoid associations. Mol Biol Evol. 1999; 16(12):1711-23. DOI: 10.1093/oxfordjournals.molbev.a026084. View

Silva J, Kidwell M . Horizontal transfer and selection in the evolution of P elements. Mol Biol Evol. 2000; 17(10):1542-57. DOI: 10.1093/oxfordjournals.molbev.a026253. View

Kapitonov V, Jurka J . Rolling-circle transposons in eukaryotes. Proc Natl Acad Sci U S A. 2001; 98(15):8714-9. PMC: 37501. DOI: 10.1073/pnas.151269298. View

Yoshiyama M, Tu Z, Kainoh Y, Honda H, Shono T, Kimura K . Possible horizontal transfer of a transposable element from host to parasitoid. Mol Biol Evol. 2001; 18(10):1952-8. DOI: 10.1093/oxfordjournals.molbev.a003735. View

McLachlin J, Escobar J, Harrelson J, Clem R, Miller L . Deletions in the Ac-iap1 gene of the baculovirus AcMNPV occur spontaneously during serial passage and confer a cell line-specific replication advantage. Virus Res. 2001; 81(1-2):77-91. DOI: 10.1016/s0168-1702(01)00362-8. View

Coates B, Hellmich R, Lewis L . Nuclear small subunit rRNA group I intron variation among Beauveria spp provide tools for strain identification and evidence of horizontal transfer. Curr Genet. 2002; 41(6):414-24. DOI: 10.1007/s00294-002-0317-8. View

Lal S, Giroux M, Brendel V, Vallejos C, Hannah L . The maize genome contains a helitron insertion. Plant Cell. 2003; 15(2):381-91. PMC: 141208. DOI: 10.1105/tpc.008375. View

Zuker M . Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 2003; 31(13):3406-15. PMC: 169194. DOI: 10.1093/nar/gkg595. View

Charlesworth B, Lapid A, Canada D . The distribution of transposable elements within and between chromosomes in a population of Drosophila melanogaster. II. Inferences on the nature of selection against elements. Genet Res. 1992; 60(2):115-30. DOI: 10.1017/s0016672300030809. View

10.

Espagne E, Dupuy C, Huguet E, Cattolico L, Provost B, Martins N . Genome sequence of a polydnavirus: insights into symbiotic virus evolution. Science. 2004; 306(5694):286-9. DOI: 10.1126/science.1103066. View

11.

Gallavotti A, Zhao Q, Kyozuka J, Meeley R, Ritter M, Doebley J . The role of barren stalk1 in the architecture of maize. Nature. 2004; 432(7017):630-5. DOI: 10.1038/nature03148. View

12.

Lai J, Li Y, Messing J, Dooner H . Gene movement by Helitron transposons contributes to the haplotype variability of maize. Proc Natl Acad Sci U S A. 2005; 102(25):9068-73. PMC: 1157042. DOI: 10.1073/pnas.0502923102. View

13.

Morgante M, Brunner S, Pea G, Fengler K, Zuccolo A, Rafalski A . Gene duplication and exon shuffling by helitron-like transposons generate intraspecies diversity in maize. Nat Genet. 2005; 37(9):997-1002. DOI: 10.1038/ng1615. View

14.

Diao X, Freeling M, Lisch D . Horizontal transfer of a plant transposon. PLoS Biol. 2005; 4(1):e5. PMC: 1310652. DOI: 10.1371/journal.pbio.0040005. View

15.

Galagan J, Calvo S, Cuomo C, Ma L, Wortman J, Batzoglou S . Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature. 2005; 438(7071):1105-15. DOI: 10.1038/nature04341. View

16.

Yang H, Hung T, You T, Yang T . Genomewide comparative analysis of the highly abundant transposable element DINE-1 suggests a recent transpositional burst in Drosophila yakuba. Genetics. 2006; 173(1):189-96. PMC: 1461449. DOI: 10.1534/genetics.105.051714. View

17.

Brookfield J . Models of repression of transposition in P-M hybrid dysgenesis by P cytotype and by zygotically encoded repressor proteins. Genetics. 1991; 128(2):471-86. PMC: 1204483. DOI: 10.1093/genetics/128.2.471. View

18.

Maddison W, Lacey Knowles L . Inferring phylogeny despite incomplete lineage sorting. Syst Biol. 2006; 55(1):21-30. DOI: 10.1080/10635150500354928. View

19.

Houck M, Clark J, Peterson K, Kidwell M . Possible horizontal transfer of Drosophila genes by the mite Proctolaelaps regalis. Science. 1991; 253(5024):1125-8. DOI: 10.1126/science.1653453. View

20.

Friesen P, Nissen M . Gene organization and transcription of TED, a lepidopteran retrotransposon integrated within the baculovirus genome. Mol Cell Biol. 1990; 10(6):3067-77. PMC: 360671. DOI: 10.1128/mcb.10.6.3067-3077.1990. View