Rolling-circle amplification of centromeric Helitrons in plant genomes

Wenwei Xiong, Hugo K. Dooner, Chunguang Du

Research output: Contribution to journalArticle

3 Citations (Scopus)

Abstract

The unusual eukaryotic Helitron transposons can readily capture host sequences and are, thus, evolutionarily important. They are presumed to amplify by rolling-circle replication (RCR) because some elements encode predicted proteins homologous to RCR prokaryotic transposases. In support of this replication mechanism, it was recently shown that transposition of a bat Helitron generates covalently closed circular intermediates. Another strong prediction is that RCR should generate tandem Helitron concatemers, yet almost all Helitrons identified to date occur as solo elements in the genome. To investigate alternative modes of Helitron organization in present-day genomes, we have applied the novel computational tool HelitronScanner to 27 plant genomes and have uncovered numerous tandem arrays of partially decayed, truncated Helitrons in all of them. Strikingly, most of these Helitron tandem arrays are interspersed with other repeats in centromeres. Many of these arrays have multiple Helitron 5′ ends, but a single 3′ end. The number of repeats in any one array can range from a handful to several hundreds. We propose here an RCR model that conforms to the present Helitron landscape of plant genomes. Our study provides strong evidence that plant Helitrons amplify by RCR and that the tandemly arrayed replication products accumulate mostly in centromeres.

Original languageEnglish
Pages (from-to)1038-1045
Number of pages8
JournalPlant Journal
Volume88
Issue number6
DOIs
StatePublished - 1 Dec 2016

Fingerprint

Plant Genome
Centromere
Genome
Transposases
genome
centromeres
transposition (genetics)
Proteins
ornamental plants
transposons
Chiroptera
prediction
proteins

Keywords

  • Arabidopsis thaliana
  • Helitron
  • Oryza sativa
  • Zea mays
  • centromere
  • rolling-circle replication (RCR)
  • tandem repeat
  • transposon

Cite this

Xiong, Wenwei ; Dooner, Hugo K. ; Du, Chunguang. / Rolling-circle amplification of centromeric Helitrons in plant genomes. In: Plant Journal. 2016 ; Vol. 88, No. 6. pp. 1038-1045.
@article{f68d492e3b9043559ec7014a3b94f08a,
title = "Rolling-circle amplification of centromeric Helitrons in plant genomes",
abstract = "The unusual eukaryotic Helitron transposons can readily capture host sequences and are, thus, evolutionarily important. They are presumed to amplify by rolling-circle replication (RCR) because some elements encode predicted proteins homologous to RCR prokaryotic transposases. In support of this replication mechanism, it was recently shown that transposition of a bat Helitron generates covalently closed circular intermediates. Another strong prediction is that RCR should generate tandem Helitron concatemers, yet almost all Helitrons identified to date occur as solo elements in the genome. To investigate alternative modes of Helitron organization in present-day genomes, we have applied the novel computational tool HelitronScanner to 27 plant genomes and have uncovered numerous tandem arrays of partially decayed, truncated Helitrons in all of them. Strikingly, most of these Helitron tandem arrays are interspersed with other repeats in centromeres. Many of these arrays have multiple Helitron 5′ ends, but a single 3′ end. The number of repeats in any one array can range from a handful to several hundreds. We propose here an RCR model that conforms to the present Helitron landscape of plant genomes. Our study provides strong evidence that plant Helitrons amplify by RCR and that the tandemly arrayed replication products accumulate mostly in centromeres.",
keywords = "Arabidopsis thaliana, Helitron, Oryza sativa, Zea mays, centromere, rolling-circle replication (RCR), tandem repeat, transposon",
author = "Wenwei Xiong and Dooner, {Hugo K.} and Chunguang Du",
year = "2016",
month = "12",
day = "1",
doi = "10.1111/tpj.13314",
language = "English",
volume = "88",
pages = "1038--1045",
journal = "Plant Journal",
issn = "0960-7412",
publisher = "Wiley-Blackwell Publishing Ltd",
number = "6",

}

Rolling-circle amplification of centromeric Helitrons in plant genomes. / Xiong, Wenwei; Dooner, Hugo K.; Du, Chunguang.

In: Plant Journal, Vol. 88, No. 6, 01.12.2016, p. 1038-1045.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Rolling-circle amplification of centromeric Helitrons in plant genomes

AU - Xiong, Wenwei

AU - Dooner, Hugo K.

AU - Du, Chunguang

PY - 2016/12/1

Y1 - 2016/12/1

N2 - The unusual eukaryotic Helitron transposons can readily capture host sequences and are, thus, evolutionarily important. They are presumed to amplify by rolling-circle replication (RCR) because some elements encode predicted proteins homologous to RCR prokaryotic transposases. In support of this replication mechanism, it was recently shown that transposition of a bat Helitron generates covalently closed circular intermediates. Another strong prediction is that RCR should generate tandem Helitron concatemers, yet almost all Helitrons identified to date occur as solo elements in the genome. To investigate alternative modes of Helitron organization in present-day genomes, we have applied the novel computational tool HelitronScanner to 27 plant genomes and have uncovered numerous tandem arrays of partially decayed, truncated Helitrons in all of them. Strikingly, most of these Helitron tandem arrays are interspersed with other repeats in centromeres. Many of these arrays have multiple Helitron 5′ ends, but a single 3′ end. The number of repeats in any one array can range from a handful to several hundreds. We propose here an RCR model that conforms to the present Helitron landscape of plant genomes. Our study provides strong evidence that plant Helitrons amplify by RCR and that the tandemly arrayed replication products accumulate mostly in centromeres.

AB - The unusual eukaryotic Helitron transposons can readily capture host sequences and are, thus, evolutionarily important. They are presumed to amplify by rolling-circle replication (RCR) because some elements encode predicted proteins homologous to RCR prokaryotic transposases. In support of this replication mechanism, it was recently shown that transposition of a bat Helitron generates covalently closed circular intermediates. Another strong prediction is that RCR should generate tandem Helitron concatemers, yet almost all Helitrons identified to date occur as solo elements in the genome. To investigate alternative modes of Helitron organization in present-day genomes, we have applied the novel computational tool HelitronScanner to 27 plant genomes and have uncovered numerous tandem arrays of partially decayed, truncated Helitrons in all of them. Strikingly, most of these Helitron tandem arrays are interspersed with other repeats in centromeres. Many of these arrays have multiple Helitron 5′ ends, but a single 3′ end. The number of repeats in any one array can range from a handful to several hundreds. We propose here an RCR model that conforms to the present Helitron landscape of plant genomes. Our study provides strong evidence that plant Helitrons amplify by RCR and that the tandemly arrayed replication products accumulate mostly in centromeres.

KW - Arabidopsis thaliana

KW - Helitron

KW - Oryza sativa

KW - Zea mays

KW - centromere

KW - rolling-circle replication (RCR)

KW - tandem repeat

KW - transposon

UR - http://www.scopus.com/inward/record.url?scp=85007416071&partnerID=8YFLogxK

U2 - 10.1111/tpj.13314

DO - 10.1111/tpj.13314

M3 - Article

C2 - 27553634

AN - SCOPUS:85007416071

VL - 88

SP - 1038

EP - 1045

JO - Plant Journal

JF - Plant Journal

SN - 0960-7412

IS - 6

ER -