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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

Pipeline for helitron identification in theP. ostreatusPC9 and PC15 genomes.
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Fig1: Pipeline for helitron identification in theP. ostreatusPC9 and PC15 genomes.

Mentions: We designed a pipeline for helitron identification in P. ostreatus (Figure 1) starting with a structure-based approach using HelSearch. This approach yielded 11 and 9 putative helitron families in the PC15 and PC9 genomes, respectively (Additional file 1: Table S1). Our subsequent homology-based approach uncovered another putative helitron family that could not be detected by the first method. After a manual curation of the alignments and the removal of false positives, we obtained two verified helitron families named HELPO1 and HELPO2. Both families contain most of the structural and enzymatic features described earlier in plant/animal helitrons such as AT insertion specificity, T[C/G]-5′ and CTRR-3′ ends (CTTG in the case of HELPO2), the presence of a subterminal palindromic hairpin, and a rolling-circle replication initiator as well as a helicase domain in a common ORF (Figure 2). Based on the similarity of the 5′ and 3′ boundaries (see Materials and Methods), helitrons of the HELPO1 family can be further classified into three subfamilies: HELPO1.1, HELPO1.2 and HELPO1.3, with elements ranging from 1.5 to 13.7 kb length (Figure 2.A). The similarity of their 5′ and 3′ helitron ends indicates that the HELPO1.2 and HELPO1.3 subfamilies are more closely related, while HELPO1.1 is more distant (data not shown). HELPO2 contained elements varying from 3.9 to 10 kb in length. Both the HELPO1 and HELPO2 families contain putative autonomous elements, however, the HELPO1 family is the only one carrying intact non-autonomous copies, all of them belonging to subfamily HELPO1.3 (Figure 2). The flanking regions of the helitron insertion sites (50 bp) are AT-rich. In fact, these regions show an AT content of 57%, while the helitrons’ AT content is similar to that of the whole genome (49%). The putative autonomous elements of the HELPO1 and HELPO2 families carry an ORF encoding a RepHel helicase of approximately 1400 aa. The protein contains three motifs defining the rep domain [3] as well as six conserved motifs present in members of the SF1 helicase superfamily described in other helitrons (Additional file 2: Figure S1) [13, 29] and necessary for replication and DNA unwinding. Using a maximum likelihood approach, we clustered the RepHel helicases into three groups (Additional file 2: Figure S1), where the HELPO1 and HELPO2 proteins were grouped separately. Interestingly, the third group lacks the rolling-circle replication initiator but ferries some of the helicase domains. Apparently, these helicases do not belong to a specific helitron family. It should be pointed out that putative HELPO1 and HELPO2 autonomous elements share about 60-70% similarity to Helitron 1_SLL_1p of Serpula lacrymans[30] and Helitron2_Ppa_1p of Physcomytrella[31], but only in the regions corresponding to the Helitron helicase-like domain (Pfam PF14214) and the PIF1-like helicase domain (Pfam PF05970).Figure 1


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)

Pipeline for helitron identification in theP. ostreatusPC9 and PC15 genomes.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig1: Pipeline for helitron identification in theP. ostreatusPC9 and PC15 genomes.
Mentions: We designed a pipeline for helitron identification in P. ostreatus (Figure 1) starting with a structure-based approach using HelSearch. This approach yielded 11 and 9 putative helitron families in the PC15 and PC9 genomes, respectively (Additional file 1: Table S1). Our subsequent homology-based approach uncovered another putative helitron family that could not be detected by the first method. After a manual curation of the alignments and the removal of false positives, we obtained two verified helitron families named HELPO1 and HELPO2. Both families contain most of the structural and enzymatic features described earlier in plant/animal helitrons such as AT insertion specificity, T[C/G]-5′ and CTRR-3′ ends (CTTG in the case of HELPO2), the presence of a subterminal palindromic hairpin, and a rolling-circle replication initiator as well as a helicase domain in a common ORF (Figure 2). Based on the similarity of the 5′ and 3′ boundaries (see Materials and Methods), helitrons of the HELPO1 family can be further classified into three subfamilies: HELPO1.1, HELPO1.2 and HELPO1.3, with elements ranging from 1.5 to 13.7 kb length (Figure 2.A). The similarity of their 5′ and 3′ helitron ends indicates that the HELPO1.2 and HELPO1.3 subfamilies are more closely related, while HELPO1.1 is more distant (data not shown). HELPO2 contained elements varying from 3.9 to 10 kb in length. Both the HELPO1 and HELPO2 families contain putative autonomous elements, however, the HELPO1 family is the only one carrying intact non-autonomous copies, all of them belonging to subfamily HELPO1.3 (Figure 2). The flanking regions of the helitron insertion sites (50 bp) are AT-rich. In fact, these regions show an AT content of 57%, while the helitrons’ AT content is similar to that of the whole genome (49%). The putative autonomous elements of the HELPO1 and HELPO2 families carry an ORF encoding a RepHel helicase of approximately 1400 aa. The protein contains three motifs defining the rep domain [3] as well as six conserved motifs present in members of the SF1 helicase superfamily described in other helitrons (Additional file 2: Figure S1) [13, 29] and necessary for replication and DNA unwinding. Using a maximum likelihood approach, we clustered the RepHel helicases into three groups (Additional file 2: Figure S1), where the HELPO1 and HELPO2 proteins were grouped separately. Interestingly, the third group lacks the rolling-circle replication initiator but ferries some of the helicase domains. Apparently, these helicases do not belong to a specific helitron family. It should be pointed out that putative HELPO1 and HELPO2 autonomous elements share about 60-70% similarity to Helitron 1_SLL_1p of Serpula lacrymans[30] and Helitron2_Ppa_1p of Physcomytrella[31], but only in the regions corresponding to the Helitron helicase-like domain (Pfam PF14214) and the PIF1-like helicase domain (Pfam PF05970).Figure 1

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