Telomere-Targeted Retrotransposons in the Rice Blast Fungus Magnaporthe oryzae: Agents of Telomere Instability

Abstract

The fungus Magnaporthe oryzae is a serious pathogen of rice and other grasses. Telomeric restriction fragments in Magnaporthe isolates that infect perennial ryegrass (prg) are hotspots for genomic rearrangement and undergo frequent, spontaneous alterations during fungal culture. The telomeres of rice-infecting isolates are very stable by comparison. Sequencing of chromosome ends from a number of prg-infecting isolates revealed two related non-LTR retrotransposons (M. oryzae Telomeric Retrotransposons or MoTeRs) inserted in the telomere repeats. This contrasts with rice pathogen telomeres that are uninterrupted by other sequences. Genetic evidence indicates that the MoTeR elements are responsible for the observed instability. MoTeRs represent a new family of telomere-targeted transposons whose members are found exclusively in fungi.T ELOMERES are the sequences that form the ends of linear chromosomes and are essential for maintaining the integrity of terminal DNA. In most organisms, the telomeres are composed of tandem arrays of short sequence motifs that are added on to the 39 ends of chromosomes by telomerase-a specialized reverse transcriptase (Greider and Blackburn 1989;Yu et al. 1990). This prevents the loss of DNA that would normally occur as a result of conservative DNA replication. The telomeres are bound by numerous proteins that shelter the terminal sequences from degradation (Garvik et al. 1995;Vodenicharov and Wellinger 2006) and illegitimate recombination (Dubois et al. 2002). Certain Diptera lack telomerase and, instead, their chromosome termini are maintained by different types of repeats (Saiga and Edstrom 1985;Biessmann et al. 1998;. The most striking example is in Drosophila whose telomeres are composed of arrays of non-LTR retrotransposons George et al. 2006), which are capable of transposing to free DNA ends (Traverse and Pardue 1988;Biessmann et al. 1990). The extension of chromosome ends through the addition of transposon sequences not only solves the end-replication problem but also serves to establish a nucleoprotein complex that is essential for protecting the chromosome ends and maintaining telomere homoeostasis (Fanti et al. 1998;Perrini et al. 2004).In many organisms, the telomeres are attached to a specific sequence that is duplicated (although often not perfectly) at many, and sometimes all, chromosome ends. Such sequences, which usually are TG-rich and often contain short tandem repeats, define a distinct distal subtelomere domain (Pryde et al. 1997). In addition to possessing distally located subtelomere domains, several organisms have proximal domains that contain genes and gene families that are also variously dispersed among different chromosome ends (Pryde et al. 1997). High levels of subtelomere polymorphism are found in many organisms, including vertebrates (Wilkie et al. 1991;Bassham et al. 1998;Baird et al. 2000;Mefford et al. 2001), insects (Biessmann et al. 1998Anderson et al. 2008;Kern and Begun 2008), plants (Yang et al. 2005), and fungi (Naumov et al. 1995Na...

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