Highly expressed captured genes and cross-kingdom domains present in Helitrons create novel diversity in Pleurotus ostreatus and other fungi

Abstract

BackgroundHelitrons are class-II eukaryotic transposons that transpose via a rolling circle mechanism. Due to their ability to capture and mobilize gene fragments, they play an important role in the evolution of their host genomes. We have used a bioinformatics approach for the identification of helitrons in two Pleurotus ostreatus genomes using de novo detection and homology-based searching. We have analyzed the presence of helitron-captured genes as well as the expansion of helitron-specific helicases in fungi and performed a phylogenetic analysis of their conserved domains with other representative eukaryotic species.ResultsOur results show the presence of two helitron families in P. ostreatus that disrupt gene colinearity and cause a lack of synteny between their genomes. Both putative autonomous and non-autonomous helitrons were transcriptionally active, and some of them carried highly expressed captured genes of unknown origin and function. In addition, both families contained eukaryotic, bacterial and viral domains within the helitron’s boundaries. A phylogenetic reconstruction of RepHel helicases using the Helitron-like and PIF1-like helicase conserved domains revealed a polyphyletic origin for eukaryotic helitrons.ConclusionP. ostreatus helitrons display features similar to other eukaryotic helitrons and do not tend to capture host genes or gene fragments. The occurrence of genes probably captured from other hosts inside the helitrons boundaries pose the hypothesis that an ancient horizontal transfer mechanism could have taken place. The viral domains found in some of these genes and the polyphyletic origin of RepHel helicases in the eukaryotic kingdom suggests that virus could have played a role in a putative lateral transfer of helitrons within the eukaryotic kingdom. The high similarity of some helitrons, along with the transcriptional activity of its RepHel helicases indicates that these elements are still active in the genome of P. ostreatus.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-1071) contains supplementary material, which is available to authorized users.

Genomic and phylogenetic evidence of VIPER retrotransposon domestication in trypanosomatids

“…L. pyrrhocoris , L. braziliensis, L. panamensis , and C. fasciculata proteins also presented matches with PHA03247, although below the threshold, indicating very low conservation in this domain. The presence of the PHA03247 domain is interesting since viral domains, including the domain under discussion, were found to be part of a special type of TEs, the helitrons (Castañera et al 2014). However, PHA03247 is the second most frequently found domain in L. amazonensis (126 copies) in a less stringent search (Tschoeke et al 2014).…”

Non-canonical Helitrons in Fusarium oxysporum

“…Helitrons are well-known for their ability to capture (parts of) genes [4, 6, 7, 14–22]. To determine the extent of gene capture in FOSC Helitrons, we search NCBIs non-redundant nucleotide database (nr/nt) using 48 full-length FOSC Helitrons.…”

“…They were first characterized in an in silico analysis of the genomes of A. thaliana , O. sativa and C. elegans [1], where they were found to have a 5’-TC and 3’-CTRR (where R stands for A or G) motif and a short hairpin at 10–12 nucleotides distance from the 3’ terminus. Recent reports indicate that Helitrons can be divided into two groups: Helitron1 and Helitron2 [2–4]. The motifs that were found upon first discovery of Helitrons are specific to the Helitron1.…”

“…Recent biochemical studies show that they transpose via copy-paste rather than cut-and-paste, which explains their high copy number [14]. Helitrons can capture (parts of) genes and thus contribute to the emergence of new genes through combining of different coding and non-coding sequence that have been sequentially captured [4, 6, 7, 14–22]. Grabundzija and others confirmed the ‘end-bypass’ model of gene capture in Helitrons, in which the transposase skips the 3’ terminus and thus includes 3’ flanking DNA sequence in the excised Helitron.…”

“…Helitrons are found in a wide range of eukaryotes, including plants, animals, fungi and oomycetes, but have predominantly been described in plants and animals [1, 4–6, 15, 18, 21, 25–37]. We ask whether FOSC Helitrons are relatively unique or whether they represent a larger and relatively unknown reservoir of Pezizomycotina Helitrons.…”