Telomeric retrotransposons show propensity to form G-quadruplexes in various eukaryotic species

Abstract Background Canonical telomeres (telomerase-synthetised) are readily forming G-quadruplexes (G4) on the G-rich strand. However, there are examples of non-canonical telomeres among eukaryotes where telomeric tandem repeats are invaded by specific retrotransposons. Drosophila melanogaster repr...

Full description

Bibliographic Details
Main Authors: Pavel Jedlička, Viktor Tokan, Iva Kejnovská, Roman Hobza, Eduard Kejnovský
Format: Article
Language:English
Published: BMC 2023-04-01
Series:Mobile DNA
Subjects:
Online Access:https://doi.org/10.1186/s13100-023-00291-9
_version_ 1797845886129143808
author Pavel Jedlička
Viktor Tokan
Iva Kejnovská
Roman Hobza
Eduard Kejnovský
author_facet Pavel Jedlička
Viktor Tokan
Iva Kejnovská
Roman Hobza
Eduard Kejnovský
author_sort Pavel Jedlička
collection DOAJ
description Abstract Background Canonical telomeres (telomerase-synthetised) are readily forming G-quadruplexes (G4) on the G-rich strand. However, there are examples of non-canonical telomeres among eukaryotes where telomeric tandem repeats are invaded by specific retrotransposons. Drosophila melanogaster represents an extreme example with telomeres composed solely by three retrotransposons—Het-A, TAHRE and TART (HTT). Even though non-canonical telomeres often show strand biased G-distribution, the evidence for the G4-forming potential is limited. Results Using circular dichroism spectroscopy and UV absorption melting assay we have verified in vitro G4-formation in the HTT elements of D. melanogaster. Namely 3 in Het-A, 8 in TART and 2 in TAHRE. All the G4s are asymmetrically distributed as in canonical telomeres. Bioinformatic analysis showed that asymmetric distribution of potential quadruplex sequences (PQS) is common in telomeric retrotransposons in other Drosophila species. Most of the PQS are located in the gag gene where PQS density correlates with higher DNA sequence conservation and codon selection favoring G4-forming potential. The importance of G4s in non-canonical telomeres is further supported by analysis of telomere-associated retrotransposons from various eukaryotic species including green algae, Diplomonadida, fungi, insects and vertebrates. Virtually all analyzed telomere-associated retrotransposons contained PQS, frequently with asymmetric strand distribution. Comparison with non-telomeric elements showed independent selection of PQS-rich elements from four distinct LINE clades. Conclusion Our findings of strand-biased G4-forming motifs in telomere-associated retrotransposons from various eukaryotic species support the G4-formation as one of the prerequisites for the recruitment of specific retrotransposons to chromosome ends and call for further experimental studies.
first_indexed 2024-04-09T17:47:17Z
format Article
id doaj.art-8b86b1add91b4f9f86f01b1b38bbe7e7
institution Directory Open Access Journal
issn 1759-8753
language English
last_indexed 2024-04-09T17:47:17Z
publishDate 2023-04-01
publisher BMC
record_format Article
series Mobile DNA
spelling doaj.art-8b86b1add91b4f9f86f01b1b38bbe7e72023-04-16T11:16:41ZengBMCMobile DNA1759-87532023-04-0114111510.1186/s13100-023-00291-9Telomeric retrotransposons show propensity to form G-quadruplexes in various eukaryotic speciesPavel Jedlička0Viktor Tokan1Iva Kejnovská2Roman Hobza3Eduard Kejnovský4Department of Plant Developmental Genetics, Institute of Biophysics of the Czech Academy of SciencesDepartment of Plant Developmental Genetics, Institute of Biophysics of the Czech Academy of SciencesDepartment of Biophysics of Nucleic Acids, Institute of Biophysics of the Czech Academy of SciencesDepartment of Plant Developmental Genetics, Institute of Biophysics of the Czech Academy of SciencesDepartment of Plant Developmental Genetics, Institute of Biophysics of the Czech Academy of SciencesAbstract Background Canonical telomeres (telomerase-synthetised) are readily forming G-quadruplexes (G4) on the G-rich strand. However, there are examples of non-canonical telomeres among eukaryotes where telomeric tandem repeats are invaded by specific retrotransposons. Drosophila melanogaster represents an extreme example with telomeres composed solely by three retrotransposons—Het-A, TAHRE and TART (HTT). Even though non-canonical telomeres often show strand biased G-distribution, the evidence for the G4-forming potential is limited. Results Using circular dichroism spectroscopy and UV absorption melting assay we have verified in vitro G4-formation in the HTT elements of D. melanogaster. Namely 3 in Het-A, 8 in TART and 2 in TAHRE. All the G4s are asymmetrically distributed as in canonical telomeres. Bioinformatic analysis showed that asymmetric distribution of potential quadruplex sequences (PQS) is common in telomeric retrotransposons in other Drosophila species. Most of the PQS are located in the gag gene where PQS density correlates with higher DNA sequence conservation and codon selection favoring G4-forming potential. The importance of G4s in non-canonical telomeres is further supported by analysis of telomere-associated retrotransposons from various eukaryotic species including green algae, Diplomonadida, fungi, insects and vertebrates. Virtually all analyzed telomere-associated retrotransposons contained PQS, frequently with asymmetric strand distribution. Comparison with non-telomeric elements showed independent selection of PQS-rich elements from four distinct LINE clades. Conclusion Our findings of strand-biased G4-forming motifs in telomere-associated retrotransposons from various eukaryotic species support the G4-formation as one of the prerequisites for the recruitment of specific retrotransposons to chromosome ends and call for further experimental studies.https://doi.org/10.1186/s13100-023-00291-9TelomereG-quadruplexRetrotransposonDrosophilaHet-ATART
spellingShingle Pavel Jedlička
Viktor Tokan
Iva Kejnovská
Roman Hobza
Eduard Kejnovský
Telomeric retrotransposons show propensity to form G-quadruplexes in various eukaryotic species
Mobile DNA
Telomere
G-quadruplex
Retrotransposon
Drosophila
Het-A
TART
title Telomeric retrotransposons show propensity to form G-quadruplexes in various eukaryotic species
title_full Telomeric retrotransposons show propensity to form G-quadruplexes in various eukaryotic species
title_fullStr Telomeric retrotransposons show propensity to form G-quadruplexes in various eukaryotic species
title_full_unstemmed Telomeric retrotransposons show propensity to form G-quadruplexes in various eukaryotic species
title_short Telomeric retrotransposons show propensity to form G-quadruplexes in various eukaryotic species
title_sort telomeric retrotransposons show propensity to form g quadruplexes in various eukaryotic species
topic Telomere
G-quadruplex
Retrotransposon
Drosophila
Het-A
TART
url https://doi.org/10.1186/s13100-023-00291-9
work_keys_str_mv AT paveljedlicka telomericretrotransposonsshowpropensitytoformgquadruplexesinvariouseukaryoticspecies
AT viktortokan telomericretrotransposonsshowpropensitytoformgquadruplexesinvariouseukaryoticspecies
AT ivakejnovska telomericretrotransposonsshowpropensitytoformgquadruplexesinvariouseukaryoticspecies
AT romanhobza telomericretrotransposonsshowpropensitytoformgquadruplexesinvariouseukaryoticspecies
AT eduardkejnovsky telomericretrotransposonsshowpropensitytoformgquadruplexesinvariouseukaryoticspecies