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A Novel Class of Miniature Inverted Repeat Transposable Elements (Mites) That Contain Hitchhiking (GTCY)N Microsatellites

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A Novel Class of Miniature Inverted Repeat Transposable Elements (Mites) That Contain Hitchhiking (GTCY)N Microsatellites Insect Molecular Biology Insect Molecular Biology (2011) 20(1), 15–27 doi: 10.1111/j.1365-2583.2010.01046.x A novel class of miniature inverted repeat transposable elements (MITEs) that contain hitchhiking (GTCY)n microsatellites B. S. Coates*, J. A. Kroemer*, D. V. Sumerford*† and Gutman, 1987). PCR-based molecular genetic markers R. L. Hellmich*† are often designed to assay for fragment-size variation *USDA-ARS, Corn Insects & Crop Genetics Research amongst alleles at microsatellite loci, and rely on unique Unit, Genetics Laboratory; and †Department of DNA sequence flanking independent tandem repeats to Entomology, Iowa State University, Ames, IA, USA attain locus specificity (Tautz, 1989; Weber & May, 1989). In contrast, instances occur when PCR amplification prod- ucts are weak or contain unintended background frag- Abstractimb_1046 15..27 ments derived from >1 locus (Economou et al., 1990). The movement of miniature inverted repeat transpos- Genotypes are difficult to determine correctly from these able elements (MITEs) modifies genome structure and problematic loci, and analysis of data often result in devia- function. We describe the microsatellite-associated tions from Hardy–Weinberg equilibrium within natural interspersed nuclear element 2 (MINE-2), that inte- populations and Mendelian expectations within pedigrees grates at consensus WTTTT target sites, creates (Terro et al., 2006). Analogous difficulties are often dinucleotide TT target site duplications (TSDs), and encountered when microsatellite markers are developed forms predicted MITE-like secondary structures; a 5Ј for species of Lepidoptera (Anthony et al., 2001; Meglécz subterminal inverted repeat (SIR; AGGGTTCCGTAG) et al., 2004), and may in part be affected by the movement that is partially complementary to a 5Ј inverted repeat of transposable elements (TEs; Coates et al., 2009, (IR; ACGAAGCCCT) and 3Ј-SIRs (TTACGGAACCCT). 2010). A (GTCY)n microsatellite is hitchhiking downstream of Transposable elements are portions of genome DNA conserved 5Ј MINE-2 secondary structures, causing capable of ‘jumping’ amongst loci, and can affect microsat- flanking sequence similarity amongst mobile micro- ellites by inserting in proximity or by carrying hitchhiking satellite loci. Transfection of insect cell lines indicates microsatellites within the TE itself (Chen & Li, 2007; Yang & that MITE-like secondary structures are sufficient to Barbash, 2008; Coates et al., 2009, 2010). Miniature mediate genome integration, and provides insight into inverted-repeat TEs (MITEs) are class II TEs that use a the transposition mechanism used by MINE-2s. ‘cut-and-paste’ mechanism to move a DNA segment amongst loci, and are nonreplicative as a result of the Keywords: transposons, repetitive element, PCR excision of the entire MITE and subsequent reinsertion at competition. different genome locations (Craig, 1995). MITEs have characteristic hairpin-like secondary structures that include Introduction terminal inverted repeats (TIRs; Wessler et al., 1995) or Microsatellites are composed of short nucleotide units subterminal inverted repeats (SIRs) that may be required repeated in tandem, and can show allelic size variation for recognition by enzymes that facilitate their mobility (Tu because of the addition or deletion of repeat units by slip & Orphanidis, 2001). As a result of a lack of protein coding strand mispairing during DNA replication (Levinson & sequence, MITEs are small in size (100 to 600 bp) and are referred to as non-autonomous TEs because movement depends upon the function of enzymes encoded within First published online 24 October 2010. ancestral autonomous TEs (MacRae & Clegg, 1992). Thus, Correspondence: Brad S. Coates, USDA-ARS, Corn Insects & Crop MITEs are hypothesized to result from deletions within Genetics Research, 113 Genetics Lab, Iowa State University, Ames, IA 50010, USA. Tel.: + 1 515 294 0668; fax: + 1 515 294 2265; e-mail: ancestral autonomous TEs or fortuitous proximity of juxta- [email protected] posed TIRs within the genome (Tsubota & Huong, 1991; © 2010 The Authors Insect Molecular Biology © 2010 The Royal Entomological Society 15 16 B. S. Coates et al. MacRae & Clegg, 1992). These autonomous TE-encoded integration of MINE-2 elements into insect cell lines, which enzymes are dual-function, and act as both an endonu- suggests that sequence within these regions is conserved clease and integrase during excision (‘cut’) and integration as a result of the requirement for active transposition. (‘paste’), respectively. The integrase functions in site- specific recognition ofa4to5bpgenome sequence that is Results and discussion followed by endonuclease-mediated cleavage that leaves a pair of nucleotide overhangs at the site of integration, and Annotation of MITE-like sequence and secondary is analogous to type II restriction enzymes commonly used structural features in molecular biology applications (Roberts, 2005). Follow- Although gene coding regions are important for cellular ing insertion of the MITE into the cut site, the nucleotide functions, the movement of TEs within a genome is known overhangs are filled in by DNA polymerase, which results in to cause chromosomal changes and alterations in gene sequence duplication flanking the TE, and are referred to expression (Kidwell & Lisch, 2001; Eichler & Sankoff, as the target site duplications (TSDs). Excision is essen- 2003; Kazazian, 2004; Feschotte & Pritham, 2007; tially integration in reverse, and results in the ‘cutting’ of the Feschotte, 2008). Knowledge of the type and number of MITE from a genome location for eventual reinsertion into TEs in a genome is fundamental to the study of changes another genome location. As movement is nonreplicative in genome structure, function and adaptation, and is a the entire MITE ‘jumps’ from an existing integration posi- critical initial step in order to define future comparative tion, but indications of past TE inserts remain because of studies. A 555 bp sequence was previously described retention of the TSD (Dawid & Rebbert, 1981). within an exon of the Helicoverpa zea cyp321A2 gene Nonreplicative ‘cut-and-paste’ movement may pose a (GenBank accession no. DQ788841 in Fig. 1) and was quandary as to how MITEs increase copy number within a annotated as a retroelement-like short interspersed genome. This propagation is shown to occur indirectly nuclear element (SINE; Chen & Li, 2007). This annotation through DNA gap repair and DNA replication events. In the was based upon the observation of AAAAA sequences 5′ first instance, MITE excision from one homologous chro- and 3′ of the integrated TE, which were assumed to rep- mosome pair in a diploid organism can invoke the DNA resent target site duplications (TSDs) similar to those gap repair mechanism, causing restoration of the MITE generated by Bos taurus (Szemraj et al., 1995) and Gallus when present upon the homologous chromosome. Simi- gallus retroelements (Salva & Birch, 1989). This TE was larly, DNA gap repair acts upon a sister chromatid when subsequently referred to as HzSINE1 (Chen & Li, 2007). MITE integration occurs at a novel genome haplotype SINEs are class I non-long terminal repeat (non-LTR) TEs location, where the newly integrated TE is used as tem- that propagate or make copies of themselves by a repli- plate for repair (Engels et al., 1990). A second method cative mechanism that uses an RNA intermediate tran- takes place during DNA replication, when a MITE excises scribed from the SINE itself (Weiner, 2002). The 5′ regions from the newly replicated strand with subsequent of SINEs retain homology to tRNA, 5S rRNA or 7SL RNA- re-integration at novel positions within the parental strand like genes from which they were derived (Okada, 1991; leading to a net MITE copy number gain (Ros & Kunze, 2001). These methods of MITE propagation have contrib- uted to the proliferation of hitchhiking microsatellites within genomes of the insect species Ostrinia nubilalis (Coates et al., 2009), and Drosophila sp. (Locke et al., 1999; Vivas et al., 1999; Miller et al., 2000; Wilder & Hollocher, 2001; Yang et al., 2006; Yang & Barbash, 2008). Despite initial descriptions, the extent to which propagation of MITE-like elements have contributed to the proliferation of microsat- ellite loci within the genomes of Lepidoptera remain largely unknown. To partially address this question, we herein describe a novel group of MITEs called the microsatellite-associated interspersed nuclear element family 2 (MINE-2), that contain an internal hitchhiking Figure 1. Amplification and expression of Helicoverpa zea short (GTCY)n microsatellite. Evidence suggests that MINE-2 interspersed nuclear element 1 [HzSINE1; H. zea microsatellite- elements are conserved within the genomes of Lepi- associated interspersed nuclear element 2 (HzMINE-2)] from (A) doptera, and sequence immediately flanking the (GTCY)n genomic DNA (gDNA) for the 555 bp HzSINE1 (HzMINE-2) and microsatellite is highly conserved as a result of involve- ~1250 bp ribosomal protein small subunit 13 (rpS13) gene products. (B) mRNA-enriched and mRNA subtracted pools from larvae under ment in the formation of TIR and IR structures. These normal growth conditions (n; 27 °C) and heat shock conditions secondary structures are shown to facilitate the stable (h; 48 °C for 30 min). © 2010 The Authors Insect Molecular Biology © 2010 The Royal Entomological Society, 20, 15–27 Lepidopteran mobile microsatellites 17 Frenkel et al., 2003), and the region includes an RNA Lack of an RNA pol III promoter.
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