Generation of microsatellite repeat families by RTE retrotransposons in lepidopteran genomes

Abstract

Abstract Background Developing lepidopteran microsatellite DNA markers can be problematical, as markers often exhibit multiple banding patterns and high frequencies of non-amplifying "null" alleles. Previous studies identified sequences flanking simple sequence repeat (SSR) units that are shared among many lepidopteran species and can be grouped into microsatellite-associated DNA families. These families are thought to be associated with unequal crossing-over during DNA recombination or with transposable elements (TEs). Results We identified full-length lepidopteran non-LTR retrotransposable elements of the RTE clade in Heliconius melpomene and Bombyx mori. These retroelements possess a single open reading frame encoding the Exonuclease/Endonuclease/Phosphatase and the Reverse Transcriptase/nLTR domains, a 5' UTR (untranslated region), and an extremely short 3' UTR that regularly consists of SSR units. Phylogenetic analysis supported previous suggestions of horizontal transfer among unrelated groups of organisms, but the diversity of lepidopteran RTE elements appears due to ancient divergence of ancestral elements rather than introgression by horizontal transfer. Similarity searches of lepidopteran genomic sequences in GenBank identified partial RTE elements, usually consisting of the 3' terminal region, in 29 species. Furthermore, we identified the C-terminal end of the Reverse Transcriptase/nLTR domain and the associated 3' UTR in over 190 microsatellite markers from 22 lepidopteran species, accounting for 10% of the lepidopteran microsatellites in GenBank. Occasional retrotransposition of autonomous elements, frequent retrotransposition of 3' partial elements, and DNA replication slippage during retrotransposition offers a mechanistic explanation for the association of SSRs with RTE elements in lepidopteran genomes. Conclusions Non-LTR retrotransposable elements of the RTE clade therefore join a diverse group of TEs as progenitors of SSR units in various organisms. When microsatellites are isolated using standard SSR enrichment protocols and primers designed at complementary repeated regions, amplification from multiple genomic sites can cause scoring difficulties that compromise their utility as markers. Screening against RTE elements in the isolation procedure provides one strategy for minimizing this problem.