Review
Promiscuous DNA: horizontal transfer of transposable elements and why it matters for eukaryotic evolution

https://doi.org/10.1016/j.tree.2010.06.001Get rights and content

Horizontal transfer is the passage of genetic material between genomes by means other than parent-to-offspring inheritance. Although the transfer of genes is thought to be crucial in prokaryotic evolution, few instances of horizontal gene transfer have been reported in multicellular eukaryotes; instead, most cases involve transposable elements. With over 200 cases now documented, it is possible to assess the importance of horizontal transfer for the evolution of transposable elements and their host genomes. We review criteria for detecting horizontal transfers and examine recent examples of the phenomenon, shedding light on its mechanistic underpinnings, including the role of host–parasite interactions. We argue that the introduction of transposable elements by horizontal transfer in eukaryotic genomes has been a major force propelling genomic variation and biological innovation.

Section snippets

The importance of horizontal transfer of DNA in genome evolution

Horizontal transfer has long been recognized as a crucial mechanism driving bacterial evolution [1]. In contrast, the evolutionary significance of horizontal transfer between the nuclear genomes of multicellular eukaryotes has remained more obscure [2]. We believe this gap in perceived importance is attributable to the disproportionate attention given to the transfer of genes as opposed to non-genic DNA. A fundamental difference in the genomic composition of multicellular eukaryotes compared to

The role of horizontal transfer in the persistence of transposable elements

The question of how TEs and other forms of ‘selfish DNA’ [9] persist in genomes while having no direct selective benefit to the host has long intrigued evolutionary biologists (e.g. 10, 11). Several models have been developed to assess the relative effects of transposition and excision rates, negative selection, and population genetic parameters (such as effective population size) on the long-term survival of TEs in the population (e.g. 12, 13). Most of these models aimed to identify conditions

Detecting HTT in the genomic era

Traditionally, three criteria have been used to infer HTT: (i) patchy distribution of the TE within a group of taxa, (ii) high sequence similarity of the TE from different host species which exceeds levels that would be expected given the divergence time of the hosts, and (iii) incongruence of TE and host phylogeny (reviewed by Refs 19, 20). It is, however, important to keep in mind that each of these patterns may also result from other evolutionary processes, such as stochastic loss and/or

Known cases of HTT: the tip of the iceberg?

Data accumulated over the last two decades have shown that both RNA- and DNA-mediated elements have crossed species boundaries on many occasions (Table 1; see also Supplemental Table 1 and references therein). Our survey of the literature reveals 218 convincing cases of HTT; with 103, 97, and 14 cases affecting DNA transposons, LTR retrotransposons, and non-LTR retrotransposons, respectively (Table 1). The apparent difference in the success rate of HTT among TE types may stem from differences

In search of the smoking gun: mechanisms underlying HTT

While the inherent mobility and replication abilities of TEs undoubtedly facilitate excision and integration, the precise mechanisms by which TEs can be transported between organisms, including potential vectors, remain largely mysterious. Successful transfer requires delivery of DNA from donor to host cell (and to the germline for multicellular organisms), followed by integration into the recipient host genome. It has long been established that ‘naked’ DNA and RNA can circulate in animal

Consequences of HTT for eukaryotic evolution

Regardless of the precise mechanism(s) underlying HTT, the accumulation of cases in the literature clearly points to a recurrent phenomenon that may be viewed as an integral facet of the lifecycle of TEs. But does it matter for eukaryotic evolution? It has been argued that biological innovation in multicellular organisms is largely driven by changes in copy number or function of pre-existing genetic material, rather than by the sudden appearance of genes and pathways de novo [66]. Because TEs

Conclusions and Future Directions

Recognizing the prevalence of HTT and its importance for the long-term persistence of many TEs is a major step towards understanding the impact of this phenomenon on the evolution of eukaryotic genomes. Further progress will necessitate systematic, genome-wide scans to identify broad and unbiased patterns of HTT across different types of TEs and taxonomic groups. This effort should lead to a better understanding of the genetic, physiological and ecological factors influencing HTT. In addition,

Acknowledgments

We would like to acknowledge the research conducted on this topic by many colleagues that could not be cited or discussed due to space constraints. We also wish to thank the following for helpful discussions and comments: E.J. Pritham, J. Meik, B. Koskella, and three anonymous reviewers. This work was supported by NSF award 0805546 to SS and NIH grant R01GM77582 to CF.

Glossary

Autonomous elements
Transposable elements that encode the proteins necessary to perform a complete transposition reaction on their own, i.e. to move from one genomic locus to another.
DNA transposons (Class 2)
Transposable elements that transpose via a DNA intermediate, also often referred to as ‘cut-and-paste’ elements because they excise and integrate elsewhere, unlike retroelements which do not excise.
LTR elements
one of two major subclasses of retroelements comprised of several superfamilies

References (100)

  • J.E. Galagan et al.

    RIP: the evolutionary cost of genome defense

    Trends Genet.

    (2004)
  • F.D. Bushman

    Targeting survival: integration site selection by retroviruses and LTR-retrotransposons

    Cell

    (2003)
  • A.V. Furano

    L1 (LINE-1) retrotransposon diversity differs dramatically between mammals and fish

    Trends Genet.

    (2004)
  • T.H. Eickbush et al.

    The diversity of retrotransposons and the properties of their reverse transcriptases

    Virus Res.

    (2008)
  • J. Gonzalez et al.

    The adaptive role of transposable elements in the Drosophila genome

    Gene

    (2009)
  • T. Marques-Bonet

    The origins and impact of primate segmental duplications

    Trends Genet.

    (2009)
  • L.S. Frost

    Mobile genetic elements: the agents of open source evolution

    Nat. Rev. Microbiol.

    (2005)
  • P.J. Keeling et al.

    Horizontal gene transfer in eukaryotic evolution

    Nat. Rev. Genet.

    (2008)
  • E.S. Lander

    Initial sequencing and analysis of the human genome

    Nature

    (2001)
  • P.S. Schnable

    The B73 maize genome: complexity, diversity, and dynamics

    Science

    (2009)
  • C. Feschotte et al.

    DNA transposons and the evolution of eukaryotic genomes

    Annu. Rev. Genet.

    (2007)
  • K.R. Oliver et al.

    Transposable elements: powerful facilitators of evolution

    Bioessays

    (2009)
  • D.W. Zeh

    Transposable elements and an epigenetic basis for punctuated equilibria

    Bioessays

    (2009)
  • R. Cordaux et al.

    The impact of retrotransposons on human genome evolution

    Nat. Rev. Genet.

    (2009)
  • L.E. Orgel et al.

    Selfish DNA- the ultimate parasite

    Nature

    (1980)
  • D.A. Hickey

    Selfish DNA: a sexually-transmitted nuclear parasite

    Genetics

    (1982)
  • E.J. Pritham

    Transposable elements and factors influencing their success in eukaryotes

    J. Hered.

    (2009)
  • J.F.Y. Brookfield et al.

    Population genetics models of transposable elements

    Genetica

    (1997)
  • A. Le Rouzic

    Long-term evolution of transposable elements

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

    (2007)
  • B. Charlesworth

    The evolutionary dynamics of repetitive DNA in eukaryotes

    Nature

    (1994)
  • S.B. Daniels

    Evidence for the horizontal transmission of the P transposable element between Drosophila species

    Genetics

    (1990)
  • D.L. Hartl

    Modern thoughts on an ancyent marinere: function, evolution, regulation

    Annu. Rev. Genet.

    (1997)
  • H.M. Roberston

    Evolution of DNA transposons in eukaryotes

  • M.G. Kidwell

    Horizontal transfer of P-elements and other short inverted repeat transposons

    Genetica

    (1992)
  • J.C. Silva

    Factors that affect the horizontal transfer of transposable elements

    Curr. Issues Mol. Biol.

    (2004)
  • E.L.S. Loreto

    Revisiting horizontal transfer of transposable elements in Drosophila

    Heredity

    (2008)
  • J.N. Volff

    Turning junk into gold: domestication of transposable elements and the creation of new genes in eukaryotes

    Bioessays

    (2006)
  • J.K. Pace

    Repeated horizontal transfer of a DNA transposon in mammals and other tetrapods

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

    (2008)
  • D. Kordis et al.

    Unusual horizontal transfer of a long interspersed nuclear element between distant vertebrate classes

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

    (1998)
  • H.S. Malik

    The age and evolution of non-LTR retrotransposable elements

    Mol. Biol. Evol.

    (1999)
  • V. Zupunski

    Evolutionary dynamics and evolutionary history in the RTE clade of non-LTR retrotransposons

    Mol. Biol. Evol.

    (2001)
  • O. Piskurek et al.

    Poxviruses as possible vectors for horizontal transfer of retroposons from reptiles to mammals

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

    (2007)
  • C. Bartolome

    Widespread evidence for horizontal transfer of transposable elements across Drosophila genomes

    Genome Biol.

    (2009)
  • A. Roulin

    Evidence of multiple horizontal transfers of the long terminal repeat retrotransposon RIRE1 within the genus Oryza

    Plant J.

    (2008)
  • A. Roulin

    Whole genome surveys of rice, maize and sorghum reveal multiple horizontal transfers of the LTR-retrotransposon Route66 in Poaceae

    BMC Evol. Biol.

    (2009)
  • D. Anxolabehere

    Molecular characteristics of diverse populations are consistent with the hypothesis of a recent invasion of Drosophila melanogaster by mobile P elements

    Mol. Biol. Evol.

    (1988)
  • A. Le Rouzic et al.

    The first steps of transposable elements invasion: Parasitic strategy vs. genetic drift

    Genetics

    (2005)
  • H. Khan

    Molecular evolution and tempo of amplification of human LINE-1 retrotransposons since the origin of primates

    Genome Res.

    (2006)
  • J.K. Pace et al.

    The evolutionary history of human DNA transposons: Evidence for intense activity in the primate lineage

    Genome Res.

    (2007)
  • K. Kodama

    The Tol1 element of the medaka fish, a member of the hAT transposable element family, jumps in Caenorhabditis elegans

    Heredity

    (2008)
  • Cited by (0)

    *

    These authors contributed equally to this review.

    View full text