Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2019 Sep 1;11(9):2505-2516.
doi: 10.1093/gbe/evz174.

Successful Invasions of Short Internally Deleted Elements (SIDEs) and Its Partner CR1 in Lepidoptera Insects

Ping-Lan Wang  1 , Andrea Luchetti  2 , Angelo Alberto Ruggieri  2 , Xiao-Min Xiong  3 , Min-Rui-Xuan Xu  1 , Xiao-Gu Zhang  1 , Hua-Hao Zhang  1
Affiliations

Successful Invasions of Short Internally Deleted Elements (SIDEs) and Its Partner CR1 in Lepidoptera Insects

Ping-Lan Wang et al. Genome Biol Evol. .

Abstract

Although DNA transposons often generated internal deleted derivatives such as miniature inverted-repeat transposable elements, short internally deleted elements (SIDEs) derived from nonlong terminal-repeat retrotransposons are rare. Here, we found a novel SIDE, named Persaeus, that originated from the chicken repeat 1 (CR1) retrotransposon Zenon and it has been found widespread in Lepidoptera insects. Our findings suggested that Persaeus and the partner Zenon have experienced a transposition burst in their host genomes and the copy number of Persaeus and Zenon in assayed genomes are significantly correlated. Accordingly, the activity though age analysis indicated that the replication wave of Persaeus coincided with that of Zenon. Phylogenetic analyses suggested that Persaeus may have evolved at least four times independently, and that it has been vertically transferred into its host genomes. Together, our results provide new insights into the evolution dynamics of SIDEs and its partner non-LTRs.

Keywords: Lepidoptera; chicken repeat 1 (CR1); long interspersed element (LINE); short internally deleted element (SIDE); transposable elements evolutionary dynamics; vertical inheritance.

PubMed Disclaimer

Figures

<sc>Fig.</sc> 1.
Fig. 1.
—Schematic view of Persaeus sequences (five copies per species) with indication of Zenon homologous regions. Approximate length of homologous regions is also reported (* H. doris and L. sinapis homologous 5′ end is ∼250 bp).
<sc>Fig</sc>. 2.
Fig. 2.
—Phylogenetic analysis Persaeus elements (five copies per species). Symbols at nodes represent maximum likelihood bootstrap/Bayesian posterior probability node support, as reported in the upper left legend. Branch color codes are indicative of the lepidopteran superfamily, as follow: Orange, Papilionoidea; blue, Bombycoidea; cyan, Noctuoidea; green, Pyraloidea; magenta, Tortricoidea. Each element has been labelled by a suffix indicating the pertaining species: Aya, Antheraea yamamai; Ape, A. pernyi; Aas, A. assama; Cca, Cadra cautella; Cce, Calycopis cecrops; Cfu, Choristoneura fumiferana; Dpl, D. plexippus; Hdo, H. doris; Lsi, Leptidea sinapis; Pda, Papilio dardanus; Pgl, P. glaucus; Pma, P. machaon; Pme, P. memnon; Ppo, P. polytes; Pxu, P. xuthus; Pze, P. zelicaon; Sex, Spodoptera exigua; Sfr, S. frugiperda; Slt, S. littoralis; Sli, S. litura; Vta, Vanessa tameamea.
<sc>Fig</sc>. 3.
Fig. 3.
—Sequence logo of Zenon region surrounding the break point where internal deletions occur (dashed, vertical lines). (A) The region upstream the break point. (B) The region downstream the break point. Black arrows in (A) and in (B) indicate direct repeats (microhomologies).
<sc>Fig</sc>. 4.
Fig. 4.
—Phylogenetic analyses of Persaeus and Zenon elements. Symbols at nodes represent support based on maximum likelihood bootstrap/Bayesian posterior probability, as reported on the upper left legend. Each element has been labelled by a suffix indicating the pertaining species: Aya, Antheraea yamamai; Ape, A. pernyi; Aas, A. assama; Bma, Bombyx mandarina; Cca, Cadra cautella; Cce, Calycopis cecrops; Cne, Calephelis nemesis; Cfu, Choristoneura fumiferana; Dcr, Danaus chrysippus; Dpl, D. plexippus; Hnu, Heliconius numata; Hdo, H. doris; Lsi, Leptidea sinapis; Hka, Hyposmocoma kahamanoa; Mur, Megathymus ursus; Pda, Papilio dardanus; Pgl, P. glaucus; Pma, P. machaon; Pme, P. memnon; Ppo, P. polytes; Pxu, P. xuthus; Pze, P. zelicaon; Sex, Spodoptera exigua; Sfr, S. frugiperda; Slt, S. littoralis; Sli, S. litura; Vta, Vanessa tameamea. Branch color codes as in figure 2.
<sc>Fig</sc>. 5.
Fig. 5.
—Persaeus and Zenon activity through age analysis. Where necessary, data were magnified (as indicated in graph insets) in order to improve the readability.
<sc>Fig</sc>. 6.
Fig. 6.
—Summary of Persaeus and Zenon distribution across the hosts phylogeny. Question marks indicate species where genome sequence was not available and, therefore, the absence of Zenon maybe to the limited data set available (GenBank database EST, TSA, or nt; table 1).
See this image and copyright information in PMC

Similar articles

See all similar articles

Cited by

References

    1. Bailly-Bechet M, Haudry A, Lerat E.. 2014. One code to find them all: a Perl tool to conveniently parse RepeatMasker output files. Mob DNA 5(1):13.
    1. Baker AJ, Haddrath O, McPherson JD, Cloutier A.. 2014. Genomic support for a moa-tinamou clade and adaptive morphological convergence in flightless ratites. Mol Biol Evol. 31(7):1686–1696. - PubMed
    1. Bibillo A, Eickbush T.. 2004. End-to-end template jumping by the reverse transcriptase encoded by the R2 retrotransposon. J Biol Chem. 279(15):14945–14953. - PubMed
    1. Biedler J, Tu Z.. 2003. Non-LTR retrotransposons in the African malaria mosquito, Anopheles gambiae: unprecedented diversity and evidence of recent activity. Mol Biol Evol. 20(11):1811–1825. - PubMed
    1. Burch JBE, Davis DL, Haas NB.. 1993. Chicken repeat 1 elements contain a pol-like open reading frame and belong to the non-long terminal repeat class of retrotransposons. Proc Natl Acad Sci U S A. 90(17):8199–8203. - PMC - PubMed

Publication types