|Lecturer at Paris-Sud University
Associate Professor at Paris-Sud University
Team Leader “Invasive Genes and Genetic Interactions in Populations“
Phone +33 1 69 82 37 24
Biodiversity, Evolution and Population genetics (for non-biologist Master 1 students)
Animal and plant life cycle (L1)
Genetics and molecular biology in Drosophila (L2)
The origin of life (Chemistry-Biology courses L1)
Transposable elements diversity and evolution
Transposable elements evolutionary dynamics
Transposable elements regulation (The mariner element in Drosophila)
Eukaryotic Transposable Elements : Diversity, Structure and Classification
Transposable elements are typically divided into two main Classes. Class I corresponds to TEs that use an RNA intermediate for copy-and-paste transposition, whereas Class II transpose directly by excision and reinsertion (cut-and-paste mechanisms). Several subclasses and sub-families are then distinguished, according to their structural characteristics (presence of LTR, genes order…) and phylogenetic relationships (protein motifs)
The discovery of new atypic families of transposable elements has made necessary an update of the classification system. The classification proposed in 2007 by Wicker and coworkers is based on the classical one. A new criterion is used: the number of strand cut at the donor site during transposition defines two subclasses among the Class II. An intermediate hierarchical level is proposed : the Order, that relies on structural characteristics of elements
Autonomous transposable elements encode one or several proteins that are required for transposition, for exemple an integrase, for Class I elements or a transposase for Class II elements. Both are involved in the reinsertion process and have endonucleases and strand transfer activities. In most families, those proteins belong to the Ribonuclease H-like large protein superfamily and are characterized by a catalytic motif DDE.
Mutator is a superfamily, comprising bacterial and eukaryotic elements. Bacterial Mutator families (IS256-like) contain a DDE atalytic domain, that differ for the classic DDE present in retroelement integrases. Notably, the two last residue are separated by more than 100 AA. In eukaryotic Mutator this motif is less conserved, and barely detectable. The comparison of the primary sequence of a large number of transposase, combined with secondary and tertiary structures analysis have allowed characterizing this catalytic motif. This illustrates the fact that for highly divergent protein, multi- level analyses are necessary .
Autonomous elements versus non-autonomous ones
The MITEs (Miniature Inverted-repeat Transposable Elements), and other non-autonomous elements, parasite the autonomous copies.
MITEs are non autonomous elements that uses the transposases encoded by related autonomous copies for multiply. This parasitic strategy is succesful and often lead to highly repeated MITE families. However newly formed MITEs that are not yet amplified are difficult to detect, because of their small size and the absence of coding regions. De novo detection of MITE in genomes relies mainly on their structural characteristic, i.e, the presence of terminal inverted repeats (TIRs) and the fact that they can transpose (at least two independent copies). Detection tools can only be efficient if they contain some methods to filter out the numerous false positive candidates.
Dynamics and evolution of transposable elements
Transposable elements usually amplify in genomes and populations from one initial copy. Within the genome, a family is then monophyletic, and relationships between copies can be described by a phylogenetic analysis. if we suppose that copies accumulate mutations with time. Then the topology of the trees, and more particularly the deepness of the nodes can be used to estimate the past transposition rate, and its variation across time. The resulting graphs easily illustrate the evolutionary dynamic of a transposon family (Le Rouzic et al. 2013)
The mariner transposable element
The Class II mariner family comprises numerous elements found in metazoa. All share a very homogeneous structure: About 1.3 kb long, they are characterized by two TIRs (Terminal Inverted Repeats) and one intronless ORF. Like all elements from the Tc1-mariner superfamily, they insert specifically into TA dinucleotide, and the transposase has a typical DDE catalytic motif (rve type).
mariner elements populate numerous metazoa genomes, and in particular Drosophila. The first mariner element was discovered in 1986 in Drosophila mauritiana, a sister species of Drosophila melanogaster.
mariner in Drosophila genomes
The availability of 20 sequenced Drosophila genome offers the opportunity for deep comparative analysis.
The phenotypic excision assay
Somatic excision of mariner (type Mos1) can be visualised in Drosophila (D. melanogaster, D. mauritiana et D. simulans) using a phenotypic excision assay of the peach copy. This mariner copy is inserted in 5′ of the white gene, conferring flies a peach-colored-eyed phenotype [peach]. peach excision in eye cells restore white activity, leading to red spots or dots on a peach background. Such flies are said “mosaic”. This assay allows evaluating the influence various environmental or genomic factors on the transposition level.
Photo: Fly with mosaic eyes, resulting from the excision of mariner from the white gene
This assay also offers a simple phenotypic way for following genome and population invasion by mariner. We follow experimental populations in which one mos1-carrying fly is introduced as a migrant, among 99 flies that only contain the inactive copy. At each generation, the extent of invasion can be followed by counting the proportion of mosaic flies. The copy number amplification is monitored by qPCR.
Saint-Leandre, B., I. Clavereau, A. Hua-Van & P. Capy (2017) Transcriptional polymorphism of piRNA regulatory genes underlies the mariner activity in Drosophila simulans testes. Molecular Ecology, 26, 3715-3731. 10.1111/mec.14145.
BOUALLEGUE M, ROUAULT JD, HUA-VAN A, MAKNI M and CAPY P (2017) Molecular evolution of piggyBac superfamily: from selfishness to domestication. Genome Biol Evol.
ROBILLARD E, LE ROUZIC A, ZHANG Z, CAPY P and HUA-VAN A (2016) Experimental evolution reveals hyperparasitic interactions among transposable elements. PNAS. doi/10.1073/pnas.1524143113
WALLAU G.L., CAPY P., LORETO E., LE ROUZIC A., HUA-VAN A (2016) VHICA, a new method to discriminate between vertical and horizontal transposon transfer: application to the mariner family within Drosophila. Molecular Biology and Evolution 33(4) 1094-1109.
FILEE J, ROUAULT JD, HARRY M and HUA-VAN A (2015) Mariner transposons are sailing in the genome of the blood-sucking bug Rhodnius prolixius.BMC Genomics 16:1061.DOI 10.1186/s12864-015-2060-9
GASMI L, BOULAIN H, GAUTHIER J, HUA-VAN A, MUSSET K, JAKUBOWSKA AK, AURY JM, VOLKOFF AN, HUGUET E, HERRERO S and DREZEN JM. 2015. Recurrent Domestication by Lepidoptera of Genes from Their Parasites Mediated by Bracoviruses. PLoS Genet 11:e1005470.
HOEN DR, HICKEY G, BOURQUE G, CASACUBERTA J, CORDAUX R, FESCHOTTE C, FISTON-LAVIER AS, HUA-VAN A, HUBLEY R, KAPUSTA A, et al. 2015. A call for benchmarking transposable element annotation methods. Mob DNA 6:13.
WALLAU, GL, CAPY, P, LORETO, E, HUA-VAN, A. 2014. Genomic landscape and evolutionary dynamics of mariner transposable elements within the Drosophila genus. BMC Genomics 15:727.
DA LAGE J.-L., BINDER M., HUA VAN A., JANECEK S., CASANE D. (2013)Gene make-up: rapid and massive intron gains after horizontal transfer of a bacterial alpha-amylase gene to Basidiomycetes. BMC Evol. Biol. 13: 40
KAMOUN C, PAYEN T., HUA-VAN A., FILEE J. 2013 Improving prokaryotic transposable elements identification using a combination of de novo and profile HMM methods. BMC Genomics 11;14:700
LE ROUZIC A., PAYEN T. , HUA-VAN A. 2013 Reconstructing the evolutionary history of transposable elements Genome, Biology and Evolution 5(1): 77-86
FORT P., ALBERTINI A., HUA-VAN A., BERTHOMIEU A., ROCHE S., DELSUC F., PASTEUR N., CAPY P., GAUDIN Y., WEILL M. 2012 Fossil thabdoviral sequences integrated into arthropod genomes: ontogeny, evolution, and potential functionality Molecular Biology and Evolution 29(1): 381-390
DUFRESNE M., LESPINET O., DABOUSSI M.J., HUA-VAN A. 2011 Genome-Wide Comparative Analysis of pogo-Like Transposable Elements in Different Fusarium Species. J Mol Evol 73(3): 230-243 url
WALLAU G.L. , HUA-VAN A. , CAPY P., LORETO E.L. 2011 The evolutionary history of mariner-like elements in Neotropical drosophilids Genetica 139(3): 327
MA L.J., VAN DER DOES H.C., BORKOVITCH K.A., COLEMAN J.J. and DABOUSSI M.-J., ET AL. 2010 Comparative genomic reveals mobile pathogenicity chromosomes in Fusarium Nature 464(7287): 367
HUA-VAN A. and CAPY P. 2008 Analysis of the DDE motif in the Mutator superfamily J Mol Evol 67(6): 670
PICOT S., WALLAU GL., LORETO ELS., HEREDIA FO., HUA-VAN A. and CAPY P. 2008 The mariner transposable element in natural populations of Drosophila simulans. Heredity 101: 53
MAISONHAUTE C., HUA-VAN A., OGEREAU D and CAPY P. 2007 Amplification of the 1731 LTR retrotransposon in Drosophila melanogaster cells : origin of neocopies and impact on the genome. Gene 393: 116
DUFRESNE M., HUA-VAN A., ABD EL WAHAB H., M’BAREK S.B., VASNIER C., TEYSSET L., KEMA G.H. and DABOUSSI M.J. 2007 Transposition of a fungal miniature inverted-repeat transposable element through the action of a Tc1-like transposase Genetics 175: 441
WICKER T., SABOT F., HUA-VAN A., BENNETZEN J.L., CAPY P., CHALHOUB B., FLAVELL A., LEROY P., MORGANTE M., PANAUD O., PAUX E., SANMIGUEL P. and SCHULMAN A.H. 2007 A unified classification system for eukaryotic transposable elements. Nat Rev Genet 8: 973
HUA-VAN A., LE ROUZIC A., MAISONHAUTE C. and CAPY P. 2005 Abundance, distribution and dynamics of retrotransposable elements and transposons: similarities and differences. Cytogenetics and Genome Research 110: 426 pdf url