A family of DNA repeats in Aspergillus nidulans has assimilated degenerated retrotransposons

Abstract

In the course of a chromosomal walk towards the centromere of chromosome IV of Aspergillus nidulans, several cross-hybridizing genomic cosmid clones were isolated. Restriction mapping of two such clones revealed that their restriction patterns were similar in a region of at least 15 kb, indicating the presence of a large repeat. The nature of the repeat was further investigated by sequencing and Southern analysis. The study revealed a family of long dispersed repeats with a high degree of sequence similarity. The number and location of the repeats vary between wild isolates. Two copies of the repeat contained degenerated long-terminal-repeat (LTR) retrotransposons, which were named Dane1 and Dane2 (for Degenerated Aspergillus nidulans element). The pattern of degeneration suggested that a process similar to the repeat-induced point-mutation (RIP) phenomenon, first described in Neurospora crassa, may have operated in A. nidulans. The data indicate that this family of repeats has assimilated mobile elements that subsequently degenerated but then underwent further duplications as a part of the host repeats.

Patterns of Repeat-Induced Point Mutation in Transposable Elements of Basidiomycete Fungi

“…Experimental evidence has subsequently shown that RIP, as an active process, exists in many other ascomycetes, including Magnaporthe grisea (Nakayashiki et al 1999; Ikeda et al 2002), Podospora anserina (Graïa et al 2001), and Leptosphaeria maculans (Idnurm and Howlett 2003). Mutation patterns indicative of RIP, that is, elevated rates of transition mutations of cytosines in the context of particular surrounding nucleotides, have been observed in repetitive elements from Fusarium oxysporum (Hua-Van et al 1998), Penicillium chrysogenum (Braumann et al 2008), Nectria haematococca (Coleman et al 2009), Grossmannia clavigera (DiGuistini et al 2011), and several Neurospora (Kinsey et al 1994) and Aspergillus species (Neuveglise et al 1996; Nielsen et al 2001; Montiel et al 2006; Braumann et al 2008; Clutterbuck 2011). Though the RIP process causes C-to-T transitions in each of these species, there is substantial variation in the preferred adjacent nucleotide context for RIP mutations (reviewed in Galagan and Selker 2004; Clutterbuck 2011), which may be a consequence of coevolutionary dynamics between the RIP defense and the TEs.…”

Repeat‐induced point mutation (RIP) in Magnaporthe grisea: implications for its sexual cycle in the natural field context

“…So far, only the two fungal species, both of which are classified into the same order Sordariales, are clearly proven to have the RIP mechanism. RIP-like C:G to T:A transitions are, however, also reported in the sequence of transposable elements in several phylogenetically more distant filamentous fungi, including Aspergillus fumigatus (Neuveglise et al ., 1996), Aspergillus nidulans (Nielsen et al ., 2001), Fusarium oxysporum (Julien et al ., 1992;Hua-van et al ., 1998) and Magnaporthe grisea (Nakayashiki et al ., 1999a) . Interestingly, some of them have no known sexual stage (e.g.…”

“…For example, (A/Tp)Cp(A/T) in M. grisea (Nakayashiki et al ., 1999a), Cp(A/G) in F. oxysporum (Hua-van et al ., 1998) and CpG in A . fumigatus and A. nidulans (Neuveglise et al ., 1996;Nielsen et al ., 2001) . Therefore, it is not clear whether the RIP-like transitions found in those fungi were operated by processes equivalent to RIP or not.…”

In silico reversal of repeat-induced point mutation (RIP) identifies the origins of repeat families and uncovers obscured duplicated genes

“…First discovered in Neurospora crassa [1,2], RIP was later demonstrated in the Ascomycetes Magnaporthe oryzae [3,4], Podospora anserina [5], Leptosphaeria maculans [6] and Fusarium graminearum [7]. Putative RIP events have also been detected bioinformatically in Aspergillus fumigatus [8], Fusarium oxysporum [9-11], Aspergillus nidulans [12], Neurospora tetrasperma [13], Microbotryum violaceum [14], Aspergillus oryzae [15], Magnaporthe oryzae [16], Colletotrichum cereal [17], Aspergillus niger [18], Penicillium chysogenum [18] and most recently in Stagonospora nodorum [19,20]. Given this broad distribution, it is reasonable to assume that RIP is widespread across, but so far restricted to, filamentous ascomycota and basidiomycota.…”

“…RIP increases the frequency of particular di-nucleotides (TpA in most cases studied to date) in affected regions of DNA. Thus RIP can be identified by comparing ratios of di-nucleotide frequencies in pre-RIP to post-RIP sequences; these ratios are referred to as "RIP indices" [8,12,25,26]. However, in reality RIP depends upon the alignment of two similar regions of double-stranded DNA [23] and therefore it is more appropriate to use alignments of repeat families to identify and quantify RIP.…”