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Next-generation sequencing reveals recent horizontal transfer of a DNA transposon between divergent mosquitoes.

Diao Y, Qi Y, Ma Y, Xia A, Sharakhov I, Chen X, Biedler J, Ling E, Tu ZJ - PLoS ONE (2011)

Bottom Line: Among 24 mosquito species surveyed, MJ1 is only found in Ae. aegypti and the hyrcanus group of anopheline mosquitoes to which An. sinensis belongs.Therefore we have shown that it is feasible to use low coverage sequencing to systematically uncover horizontal transfer events.Expanding such efforts across a wide range of species will generate novel insights into the relative frequency of horizontal transfer of different TEs and provide the evolutionary context of these lateral transfer events.

View Article: PubMed Central - PubMed

Affiliation: Institute of Plant Physiology and Ecology, Shanghai Institute for Biological Sciences, Chinese Academy of Sciences, Shanghai, China.

ABSTRACT
Horizontal transfer of genetic material between complex organisms often involves transposable elements (TEs). For example, a DNA transposon mariner has been shown to undergo horizontal transfer between different orders of insects and between different phyla of animals. Here we report the discovery and characterization of an ITmD37D transposon, MJ1, in Anopheles sinensis. We show that some MJ1 elements in Aedes aegypti and An. sinensis contain intact open reading frames and share nearly 99% nucleotide identity over the entire transposon, which is unexpectedly high given that these two genera had diverged 145-200 million years ago. Chromosomal hybridization and TE-display showed that MJ1 copy number is low in An. sinensis. Among 24 mosquito species surveyed, MJ1 is only found in Ae. aegypti and the hyrcanus group of anopheline mosquitoes to which An. sinensis belongs. Phylogenetic analysis is consistent with horizontal transfer and provides the basis for inference of its timing and direction. Although report of horizontal transfer of DNA transposons between higher eukaryotes is accumulating, our analysis is one of a small number of cases in which horizontal transfer of nearly identical TEs among highly divergent species has been thoroughly investigated and strongly supported. Horizontal transfer involving mosquitoes is of particular interest because there are ongoing investigations of the possibility of spreading pathogen-resistant genes into mosquito populations to control malaria and other infectious diseases. The initial indication of horizontal transfer of MJ1 came from comparisons between a 0.4x coverage An. sinensis 454 sequence database and available TEs in mosquito genomes. Therefore we have shown that it is feasible to use low coverage sequencing to systematically uncover horizontal transfer events. Expanding such efforts across a wide range of species will generate novel insights into the relative frequency of horizontal transfer of different TEs and provide the evolutionary context of these lateral transfer events.

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Fluorescence in situ hybridization confirmed the presence of MJ1 in An. sinensis.Arrows point to signals on An. sinensis polytene chromosomes, resulting from hybridization with an Asi_MJ1 probe.
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pone-0016743-g003: Fluorescence in situ hybridization confirmed the presence of MJ1 in An. sinensis.Arrows point to signals on An. sinensis polytene chromosomes, resulting from hybridization with an Asi_MJ1 probe.

Mentions: We performed TE-display [19] to compare and isolate MJ1 insertion sites in individual Ae. aegypti and An. sinensis mosquitoes. There were no shared bands (or shared insertion sites) between Ae. aegypti and An. sinensis while there were multiple shared bands among individuals within each species (Figure 2). We cloned and sequenced a few of these bands recovered from TE-display gels, which further confirmed the presence of MJ1 in both species. More importantly, the recovered insertion site sequences were specific to each species (Figure 2). In other words, sequence flanking the MJ1 insertion site that was recovered from Ae. aegypti matched Ae. aegypti genomic sequence alone. Sequence flanking the MJ1 insertion recovered from An. sinensis matched An. sinensis genomic sequence alone. Using Asi_MJ1 as a probe, we performed in situ hybridization on the polytene chromosomes of An. sinensis. A representative image is shown in Figure 3 and five distinct bands are apparent. These results further confirmed the presence of Asi_MJ1 in An. sinensis. Although it is difficult to determine the exact copy number of MJ1 on the basis of in situ and TE-display results, both experiments suggest that the copy number of MJ1 in An. sinensis is low, most likely less than 10 copies per genome.


Next-generation sequencing reveals recent horizontal transfer of a DNA transposon between divergent mosquitoes.

Diao Y, Qi Y, Ma Y, Xia A, Sharakhov I, Chen X, Biedler J, Ling E, Tu ZJ - PLoS ONE (2011)

Fluorescence in situ hybridization confirmed the presence of MJ1 in An. sinensis.Arrows point to signals on An. sinensis polytene chromosomes, resulting from hybridization with an Asi_MJ1 probe.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3037385&req=5

pone-0016743-g003: Fluorescence in situ hybridization confirmed the presence of MJ1 in An. sinensis.Arrows point to signals on An. sinensis polytene chromosomes, resulting from hybridization with an Asi_MJ1 probe.
Mentions: We performed TE-display [19] to compare and isolate MJ1 insertion sites in individual Ae. aegypti and An. sinensis mosquitoes. There were no shared bands (or shared insertion sites) between Ae. aegypti and An. sinensis while there were multiple shared bands among individuals within each species (Figure 2). We cloned and sequenced a few of these bands recovered from TE-display gels, which further confirmed the presence of MJ1 in both species. More importantly, the recovered insertion site sequences were specific to each species (Figure 2). In other words, sequence flanking the MJ1 insertion site that was recovered from Ae. aegypti matched Ae. aegypti genomic sequence alone. Sequence flanking the MJ1 insertion recovered from An. sinensis matched An. sinensis genomic sequence alone. Using Asi_MJ1 as a probe, we performed in situ hybridization on the polytene chromosomes of An. sinensis. A representative image is shown in Figure 3 and five distinct bands are apparent. These results further confirmed the presence of Asi_MJ1 in An. sinensis. Although it is difficult to determine the exact copy number of MJ1 on the basis of in situ and TE-display results, both experiments suggest that the copy number of MJ1 in An. sinensis is low, most likely less than 10 copies per genome.

Bottom Line: Among 24 mosquito species surveyed, MJ1 is only found in Ae. aegypti and the hyrcanus group of anopheline mosquitoes to which An. sinensis belongs.Therefore we have shown that it is feasible to use low coverage sequencing to systematically uncover horizontal transfer events.Expanding such efforts across a wide range of species will generate novel insights into the relative frequency of horizontal transfer of different TEs and provide the evolutionary context of these lateral transfer events.

View Article: PubMed Central - PubMed

Affiliation: Institute of Plant Physiology and Ecology, Shanghai Institute for Biological Sciences, Chinese Academy of Sciences, Shanghai, China.

ABSTRACT
Horizontal transfer of genetic material between complex organisms often involves transposable elements (TEs). For example, a DNA transposon mariner has been shown to undergo horizontal transfer between different orders of insects and between different phyla of animals. Here we report the discovery and characterization of an ITmD37D transposon, MJ1, in Anopheles sinensis. We show that some MJ1 elements in Aedes aegypti and An. sinensis contain intact open reading frames and share nearly 99% nucleotide identity over the entire transposon, which is unexpectedly high given that these two genera had diverged 145-200 million years ago. Chromosomal hybridization and TE-display showed that MJ1 copy number is low in An. sinensis. Among 24 mosquito species surveyed, MJ1 is only found in Ae. aegypti and the hyrcanus group of anopheline mosquitoes to which An. sinensis belongs. Phylogenetic analysis is consistent with horizontal transfer and provides the basis for inference of its timing and direction. Although report of horizontal transfer of DNA transposons between higher eukaryotes is accumulating, our analysis is one of a small number of cases in which horizontal transfer of nearly identical TEs among highly divergent species has been thoroughly investigated and strongly supported. Horizontal transfer involving mosquitoes is of particular interest because there are ongoing investigations of the possibility of spreading pathogen-resistant genes into mosquito populations to control malaria and other infectious diseases. The initial indication of horizontal transfer of MJ1 came from comparisons between a 0.4x coverage An. sinensis 454 sequence database and available TEs in mosquito genomes. Therefore we have shown that it is feasible to use low coverage sequencing to systematically uncover horizontal transfer events. Expanding such efforts across a wide range of species will generate novel insights into the relative frequency of horizontal transfer of different TEs and provide the evolutionary context of these lateral transfer events.

Show MeSH
Related in: MedlinePlus