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DINE-1, the highest copy number repeats in Drosophila melanogaster are non-autonomous endonuclease-encoding rolling-circle transposable elements (Helentrons).

Thomas J, Vadnagara K, Pritham EJ - Mob DNA (2014)

Bottom Line: The Drosophila INterspersed Elements-1 (DINE-1/INE1) transposable elements (TEs) are the most abundant component of the Drosophila melanogaster genome and have been associated with functional gene duplications.DINE-1 TEs do not encode any proteins (non-autonomous) thus are moved by autonomous partners.The structural features of Helentrons are described, which resemble the organization of the non-autonomous partners, but differ significantly from canonical Helitrons.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Human Genetics, University of Utah, Salt Lake City, UT 84112, USA.

ABSTRACT

Background: The Drosophila INterspersed Elements-1 (DINE-1/INE1) transposable elements (TEs) are the most abundant component of the Drosophila melanogaster genome and have been associated with functional gene duplications. DINE-1 TEs do not encode any proteins (non-autonomous) thus are moved by autonomous partners. The identity of the autonomous partners has been a mystery. They have been allied to Helitrons (rolling-circle transposons), MITEs (DNA transposons), and non-LTR retrotransposons by different authors.

Results: We report multiple lines of bioinformatic evidence that illustrate the relationship of DINE-1 like TEs to endonuclease-encoding rolling-circle TEs (Helentrons). The structural features of Helentrons are described, which resemble the organization of the non-autonomous partners, but differ significantly from canonical Helitrons. In addition to the presence of an endonuclease domain fused to the Rep/Helicase protein, Helentrons have distinct structural features. Evidence is presented that illustrates that Helentrons are widely distributed in invertebrate, fish, and fungal genomes. We describe an intermediate family from the Phytophthora infestans genome that phylogenetically groups with Helentrons but that displays Helitron structure. In addition, evidence is presented that Helentrons can capture gene fragments in a pattern reminiscent of canonical Helitrons.

Conclusions: We illustrate the relationship of DINE-1 and related TE families to autonomous partners, the Helentrons. These findings will allow their proper classification and enable a more accurate understanding of the contribution of rolling-circle transposition to the birth of new genes, gene networks, and genome composition.

No MeSH data available.


Related in: MedlinePlus

The structural characteristics of Helentrons and their non-autonomous partners from other species. The open black box denotes the ORF encoding the Rep/Helicase protein (the lighter green is the Rep, the medium green is the helicase, and the endonuclease is the darker olive shade). The orange block denotes the ORF encoding the RPA protein. The histone gene and gene fragments are represented in pink. The green arrows represent the subterminal repeats (subTIRs). The red stem loop structure represents the 3' palindrome. The green sideways triangle in the 5' end represents the 3' side of the inverted repeat (IR) (the 5' side is nested inside the 5' subTIR). The red T represents the flanking host sequence. Black vertical and horizontal lines point to the pairwise sequence identities and length of alignment (excluding gaps) of the sequences compared. (A-D) The structures of select Helentrons (Helentron-Cq-32A.4 and Helentron-Cq-31A.1) and their non-autonomous partners (HINE-Cq-32A.1 and HINE-Cq-31A.1) from the Culex quinquefasciatus genome. (E, F) The structure of another Helentron family (Helentron-Da-40A.1) from D. ananassae and the non-autonomous partner (DINE-Da-40A.1) described in [7]. The putative Rep/Helicase/Endonuclease in this Helentron is in the opposite orientation relative to others. (G-J) The structure of a novel family of Helentron (Helentron-Da-41A.1, Helentron-Dw-41B.1) present in both Drosophila ananassae and D. willistoni genomes and the non-autonomous partners (HINE-Da-41A.1, HINE-Dw-41B.1).
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Figure 4: The structural characteristics of Helentrons and their non-autonomous partners from other species. The open black box denotes the ORF encoding the Rep/Helicase protein (the lighter green is the Rep, the medium green is the helicase, and the endonuclease is the darker olive shade). The orange block denotes the ORF encoding the RPA protein. The histone gene and gene fragments are represented in pink. The green arrows represent the subterminal repeats (subTIRs). The red stem loop structure represents the 3' palindrome. The green sideways triangle in the 5' end represents the 3' side of the inverted repeat (IR) (the 5' side is nested inside the 5' subTIR). The red T represents the flanking host sequence. Black vertical and horizontal lines point to the pairwise sequence identities and length of alignment (excluding gaps) of the sequences compared. (A-D) The structures of select Helentrons (Helentron-Cq-32A.4 and Helentron-Cq-31A.1) and their non-autonomous partners (HINE-Cq-32A.1 and HINE-Cq-31A.1) from the Culex quinquefasciatus genome. (E, F) The structure of another Helentron family (Helentron-Da-40A.1) from D. ananassae and the non-autonomous partner (DINE-Da-40A.1) described in [7]. The putative Rep/Helicase/Endonuclease in this Helentron is in the opposite orientation relative to others. (G-J) The structure of a novel family of Helentron (Helentron-Da-41A.1, Helentron-Dw-41B.1) present in both Drosophila ananassae and D. willistoni genomes and the non-autonomous partners (HINE-Da-41A.1, HINE-Dw-41B.1).

Mentions: To determine if related Helentrons were present in the organisms where DINE-1 like families had already been described or vice versa, full-length Helentrons and non-autonomous families were mined from representative species (see Methods). Two families of Helentron and their derived HINEs and a novel family of HINE (FigureĀ 4A-D, Additional file 7: Table S2, Additional file 8) were mined from the C. quinquefasciatus genome. The Culex Helentrons display similar structural characteristics as that of the mite including the palindromic subTIRs and the stem loop at the 3' end (Additional file 7: Table S2). The elements preferentially insert within the TT dinucleotide and have a string of Ts (2 to 5) on the boundaries (Additional file 2: Figure S1, Additional file 3: Figure S2). These Ts are part of the element but sometime vary in number between copies (Additional file 2: Figure S1, Additional file 3: Figure S2). The non-autonomous families share >95% sequence identity with the respective partner, Helentron. Some copies contain simple or tandem repeats that occupy approximately 50% of the total length of the element (HINE-Cq-32A.1 and HINE-Cq-31A.1).


DINE-1, the highest copy number repeats in Drosophila melanogaster are non-autonomous endonuclease-encoding rolling-circle transposable elements (Helentrons).

Thomas J, Vadnagara K, Pritham EJ - Mob DNA (2014)

The structural characteristics of Helentrons and their non-autonomous partners from other species. The open black box denotes the ORF encoding the Rep/Helicase protein (the lighter green is the Rep, the medium green is the helicase, and the endonuclease is the darker olive shade). The orange block denotes the ORF encoding the RPA protein. The histone gene and gene fragments are represented in pink. The green arrows represent the subterminal repeats (subTIRs). The red stem loop structure represents the 3' palindrome. The green sideways triangle in the 5' end represents the 3' side of the inverted repeat (IR) (the 5' side is nested inside the 5' subTIR). The red T represents the flanking host sequence. Black vertical and horizontal lines point to the pairwise sequence identities and length of alignment (excluding gaps) of the sequences compared. (A-D) The structures of select Helentrons (Helentron-Cq-32A.4 and Helentron-Cq-31A.1) and their non-autonomous partners (HINE-Cq-32A.1 and HINE-Cq-31A.1) from the Culex quinquefasciatus genome. (E, F) The structure of another Helentron family (Helentron-Da-40A.1) from D. ananassae and the non-autonomous partner (DINE-Da-40A.1) described in [7]. The putative Rep/Helicase/Endonuclease in this Helentron is in the opposite orientation relative to others. (G-J) The structure of a novel family of Helentron (Helentron-Da-41A.1, Helentron-Dw-41B.1) present in both Drosophila ananassae and D. willistoni genomes and the non-autonomous partners (HINE-Da-41A.1, HINE-Dw-41B.1).
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4067079&req=5

Figure 4: The structural characteristics of Helentrons and their non-autonomous partners from other species. The open black box denotes the ORF encoding the Rep/Helicase protein (the lighter green is the Rep, the medium green is the helicase, and the endonuclease is the darker olive shade). The orange block denotes the ORF encoding the RPA protein. The histone gene and gene fragments are represented in pink. The green arrows represent the subterminal repeats (subTIRs). The red stem loop structure represents the 3' palindrome. The green sideways triangle in the 5' end represents the 3' side of the inverted repeat (IR) (the 5' side is nested inside the 5' subTIR). The red T represents the flanking host sequence. Black vertical and horizontal lines point to the pairwise sequence identities and length of alignment (excluding gaps) of the sequences compared. (A-D) The structures of select Helentrons (Helentron-Cq-32A.4 and Helentron-Cq-31A.1) and their non-autonomous partners (HINE-Cq-32A.1 and HINE-Cq-31A.1) from the Culex quinquefasciatus genome. (E, F) The structure of another Helentron family (Helentron-Da-40A.1) from D. ananassae and the non-autonomous partner (DINE-Da-40A.1) described in [7]. The putative Rep/Helicase/Endonuclease in this Helentron is in the opposite orientation relative to others. (G-J) The structure of a novel family of Helentron (Helentron-Da-41A.1, Helentron-Dw-41B.1) present in both Drosophila ananassae and D. willistoni genomes and the non-autonomous partners (HINE-Da-41A.1, HINE-Dw-41B.1).
Mentions: To determine if related Helentrons were present in the organisms where DINE-1 like families had already been described or vice versa, full-length Helentrons and non-autonomous families were mined from representative species (see Methods). Two families of Helentron and their derived HINEs and a novel family of HINE (FigureĀ 4A-D, Additional file 7: Table S2, Additional file 8) were mined from the C. quinquefasciatus genome. The Culex Helentrons display similar structural characteristics as that of the mite including the palindromic subTIRs and the stem loop at the 3' end (Additional file 7: Table S2). The elements preferentially insert within the TT dinucleotide and have a string of Ts (2 to 5) on the boundaries (Additional file 2: Figure S1, Additional file 3: Figure S2). These Ts are part of the element but sometime vary in number between copies (Additional file 2: Figure S1, Additional file 3: Figure S2). The non-autonomous families share >95% sequence identity with the respective partner, Helentron. Some copies contain simple or tandem repeats that occupy approximately 50% of the total length of the element (HINE-Cq-32A.1 and HINE-Cq-31A.1).

Bottom Line: The Drosophila INterspersed Elements-1 (DINE-1/INE1) transposable elements (TEs) are the most abundant component of the Drosophila melanogaster genome and have been associated with functional gene duplications.DINE-1 TEs do not encode any proteins (non-autonomous) thus are moved by autonomous partners.The structural features of Helentrons are described, which resemble the organization of the non-autonomous partners, but differ significantly from canonical Helitrons.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Human Genetics, University of Utah, Salt Lake City, UT 84112, USA.

ABSTRACT

Background: The Drosophila INterspersed Elements-1 (DINE-1/INE1) transposable elements (TEs) are the most abundant component of the Drosophila melanogaster genome and have been associated with functional gene duplications. DINE-1 TEs do not encode any proteins (non-autonomous) thus are moved by autonomous partners. The identity of the autonomous partners has been a mystery. They have been allied to Helitrons (rolling-circle transposons), MITEs (DNA transposons), and non-LTR retrotransposons by different authors.

Results: We report multiple lines of bioinformatic evidence that illustrate the relationship of DINE-1 like TEs to endonuclease-encoding rolling-circle TEs (Helentrons). The structural features of Helentrons are described, which resemble the organization of the non-autonomous partners, but differ significantly from canonical Helitrons. In addition to the presence of an endonuclease domain fused to the Rep/Helicase protein, Helentrons have distinct structural features. Evidence is presented that illustrates that Helentrons are widely distributed in invertebrate, fish, and fungal genomes. We describe an intermediate family from the Phytophthora infestans genome that phylogenetically groups with Helentrons but that displays Helitron structure. In addition, evidence is presented that Helentrons can capture gene fragments in a pattern reminiscent of canonical Helitrons.

Conclusions: We illustrate the relationship of DINE-1 and related TE families to autonomous partners, the Helentrons. These findings will allow their proper classification and enable a more accurate understanding of the contribution of rolling-circle transposition to the birth of new genes, gene networks, and genome composition.

No MeSH data available.


Related in: MedlinePlus