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

Castanera R, Pérez G, López L, Sancho R, Santoyo F, Alfaro M, Gabaldón T, Pisabarro AG, Oguiza JA, Ramírez L - BMC Genomics (2014)

Bottom Line: Our results show the presence of two helitron families in P. ostreatus that disrupt gene colinearity and cause a lack of synteny between their genomes.P. ostreatus helitrons display features similar to other eukaryotic helitrons and do not tend to capture host genes or gene fragments.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Agrarian Production, Genetics and Microbiology Research Group, Public University of Navarre, 31006 Pamplona, Navarre, Spain. lramirez@unavarra.es.

ABSTRACT

Background: Helitrons 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.

Results: Our 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.

Conclusion: P. 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.

No MeSH data available.


Related in: MedlinePlus

Helitron length polymorphisms in allelic copies of the HELPO1.3 subfamily. Regions in red are highly conserved. Blue triangles represent inverted repeats, and the black square represents a satellite sequence (the number of repeats is shown in parentheses). Empty arrows represent predicted ORFs.
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Fig4: Helitron length polymorphisms in allelic copies of the HELPO1.3 subfamily. Regions in red are highly conserved. Blue triangles represent inverted repeats, and the black square represents a satellite sequence (the number of repeats is shown in parentheses). Empty arrows represent predicted ORFs.

Mentions: An analysis of the conserved domains showed significant hits (CDD, cutoff E-value <0.01) in a HELPO1.2 copy harboring LTR/Gypsy and in a helpo1.3 copy, both present on chromosome 1 (Figure 2B, Table 1). The HELPO1.2 copy on chromosome I carried viral and retrotransposon domains in addition to helitron motifs (Figure 2, Additional file 5: Dataset S1). BLASTN searches performed on PC15 filtered model genes using intact helitrons as queries showed that this HELPO1.2 was the only helitron harboring plant and animal re-arranged retroviral genes shuttled by a retroelement. The largest helpo1.3 copy on chromosome I was 10.7 kb longer than the mean of the lengths of the other helpo1.3 copies in the P. ostreatus genome (12.2 kb vs. 1.5 kb, Figure 2B and Figure 4), and it bore a small EST without a predicted gene model (the capC gene) as well as three predicted genes (capD, capE and capF). The capD gene contains a domain present in the large tegument protein UL36 of the herpes virus (PHA03247), capE carries a Caulimovirus viroplasmin (pfam01693), and capF carries a predicted nuclease (RNAse H L fold, COG4328). All of the cap genes described above are exclusively captured by helitrons and do not have additional copies outside helitron boundaries.Figure 4


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

Castanera R, Pérez G, López L, Sancho R, Santoyo F, Alfaro M, Gabaldón T, Pisabarro AG, Oguiza JA, Ramírez L - BMC Genomics (2014)

Helitron length polymorphisms in allelic copies of the HELPO1.3 subfamily. Regions in red are highly conserved. Blue triangles represent inverted repeats, and the black square represents a satellite sequence (the number of repeats is shown in parentheses). Empty arrows represent predicted ORFs.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4289320&req=5

Fig4: Helitron length polymorphisms in allelic copies of the HELPO1.3 subfamily. Regions in red are highly conserved. Blue triangles represent inverted repeats, and the black square represents a satellite sequence (the number of repeats is shown in parentheses). Empty arrows represent predicted ORFs.
Mentions: An analysis of the conserved domains showed significant hits (CDD, cutoff E-value <0.01) in a HELPO1.2 copy harboring LTR/Gypsy and in a helpo1.3 copy, both present on chromosome 1 (Figure 2B, Table 1). The HELPO1.2 copy on chromosome I carried viral and retrotransposon domains in addition to helitron motifs (Figure 2, Additional file 5: Dataset S1). BLASTN searches performed on PC15 filtered model genes using intact helitrons as queries showed that this HELPO1.2 was the only helitron harboring plant and animal re-arranged retroviral genes shuttled by a retroelement. The largest helpo1.3 copy on chromosome I was 10.7 kb longer than the mean of the lengths of the other helpo1.3 copies in the P. ostreatus genome (12.2 kb vs. 1.5 kb, Figure 2B and Figure 4), and it bore a small EST without a predicted gene model (the capC gene) as well as three predicted genes (capD, capE and capF). The capD gene contains a domain present in the large tegument protein UL36 of the herpes virus (PHA03247), capE carries a Caulimovirus viroplasmin (pfam01693), and capF carries a predicted nuclease (RNAse H L fold, COG4328). All of the cap genes described above are exclusively captured by helitrons and do not have additional copies outside helitron boundaries.Figure 4

Bottom Line: Our results show the presence of two helitron families in P. ostreatus that disrupt gene colinearity and cause a lack of synteny between their genomes.P. ostreatus helitrons display features similar to other eukaryotic helitrons and do not tend to capture host genes or gene fragments.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Agrarian Production, Genetics and Microbiology Research Group, Public University of Navarre, 31006 Pamplona, Navarre, Spain. lramirez@unavarra.es.

ABSTRACT

Background: Helitrons 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.

Results: Our 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.

Conclusion: P. 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.

No MeSH data available.


Related in: MedlinePlus