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HelitronScanner uncovers a large overlooked cache of Helitron transposons in many plant genomes

Identifieur interne : 000D39 ( Pmc/Curation ); précédent : 000D38; suivant : 000D40

HelitronScanner uncovers a large overlooked cache of Helitron transposons in many plant genomes

Auteurs : Wenwei Xiong ; Limei He ; Jinsheng Lai [République populaire de Chine] ; Hugo K. Dooner ; Chunguang Du

Source :

RBID : PMC:4104883

Abstract

Significance

Helitrons are unusual rolling-circle eukaryotic transposons with a remarkable ability to capture gene sequences, which makes them of considerable evolutionary importance. Because Helitrons lack typical transposon features, they are challenging to identify and are estimated to comprise at most 2% of sequenced genomes. Here, we describe HelitronScanner, a generalized tool for their identification based on a motif-extracting algorithm proposed initially in a study of natural languages. HelitronScanner overcomes the divergence of Helitron termini among species by using conserved nucleotides at potentially variable locations. Many new Helitrons were identified in all organisms examined, resulting in a major reassessment of their abundance in eukaryotic genomes. In maize, they make up >6% of the genome and are the most abundant DNA transposons identified.


Url:
DOI: 10.1073/pnas.1410068111
PubMed: 24982153
PubMed Central: 4104883

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PMC:4104883

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08854;</nlm:aff>
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08801</nlm:aff>
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<title>Significance</title>
<p>
<italic>Helitrons</italic>
are unusual rolling-circle eukaryotic transposons with a remarkable ability to capture gene sequences, which makes them of considerable evolutionary importance. Because
<italic>Helitrons</italic>
lack typical transposon features, they are challenging to identify and are estimated to comprise at most 2% of sequenced genomes. Here, we describe HelitronScanner, a generalized tool for their identification based on a motif-extracting algorithm proposed initially in a study of natural languages. HelitronScanner overcomes the divergence of
<italic>Helitron</italic>
termini among species by using conserved nucleotides at potentially variable locations. Many new
<italic>Helitrons</italic>
were identified in all organisms examined, resulting in a major reassessment of their abundance in eukaryotic genomes. In maize, they make up >6% of the genome and are the most abundant DNA transposons identified.</p>
</div>
</front>
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<journal-id journal-id-type="iso-abbrev">Proc. Natl. Acad. Sci. U.S.A</journal-id>
<journal-id journal-id-type="hwp">pnas</journal-id>
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transposons in many plant genomes</article-title>
<alt-title alt-title-type="short">Helitron identification by local sequence patterns</alt-title>
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<given-names>Wenwei</given-names>
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<sup>b</sup>
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<surname>Lai</surname>
<given-names>Jinsheng</given-names>
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<sup>c</sup>
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<sup>b</sup>
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<sup>d</sup>
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<sup>1</sup>
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<sup>a</sup>
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<sup>a</sup>
Department of Biology and Molecular Biology,
<institution>Montclair State University</institution>
, Montclair,
<addr-line>NJ</addr-line>
07043;</aff>
<aff id="aff2">
<sup>b</sup>
Waksman Institute,
<institution>Rutgers, the State University of New Jersey</institution>
, Piscataway,
<addr-line>NJ</addr-line>
08854;</aff>
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<sup>c</sup>
National Maize Improvement Center,
<institution>China Agricultural University</institution>
, Beijing 100083,
<country>China</country>
; and</aff>
<aff id="aff4">
<sup>d</sup>
Department of Plant Biology,
<institution>Rutgers, the State University of New Jersey</institution>
, New Brunswick,
<addr-line>NJ</addr-line>
08801</aff>
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<author-notes>
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<sup>1</sup>
To whom correspondence may be addressed. E-mail:
<email>dooner@waksman.rutgers.edu</email>
or
<email>duc@mail.montclair.edu</email>
.</corresp>
<fn fn-type="edited-by">
<p>Contributed by Hugo K. Dooner, June 6, 2014 (sent for review January 28, 2014)</p>
</fn>
<fn fn-type="con">
<p>Author contributions: W.X. and C.D. designed research; W.X., L.H., and C.D. performed research; J.L. contributed new reagents/analytic tools; W.X., L.H., H.K.D., and C.D. analyzed data; and W.X., H.K.D., and C.D. wrote the paper.</p>
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<abstract abstract-type="executive-summary">
<title>Significance</title>
<p>
<italic>Helitrons</italic>
are unusual rolling-circle eukaryotic transposons with a remarkable ability to capture gene sequences, which makes them of considerable evolutionary importance. Because
<italic>Helitrons</italic>
lack typical transposon features, they are challenging to identify and are estimated to comprise at most 2% of sequenced genomes. Here, we describe HelitronScanner, a generalized tool for their identification based on a motif-extracting algorithm proposed initially in a study of natural languages. HelitronScanner overcomes the divergence of
<italic>Helitron</italic>
termini among species by using conserved nucleotides at potentially variable locations. Many new
<italic>Helitrons</italic>
were identified in all organisms examined, resulting in a major reassessment of their abundance in eukaryotic genomes. In maize, they make up >6% of the genome and are the most abundant DNA transposons identified.</p>
</abstract>
<abstract>
<p>Transposons make up the bulk of eukaryotic genomes, but are difficult to annotate because they evolve rapidly. Most of the unannotated portion of sequenced genomes is probably made up of various divergent transposons that have yet to be categorized.
<italic>Helitrons</italic>
are unusual rolling circle eukaryotic transposons that often capture gene sequences, making them of considerable evolutionary importance. Unlike other DNA transposons,
<italic>Helitrons</italic>
do not end in inverted repeats or create target site duplications, so they are particularly challenging to identify. Here we present HelitronScanner, a two-layered local combinational variable (LCV) tool for generalized
<italic>Helitron</italic>
identification that represents a major improvement over previous identification programs based on DNA sequence or structure. HelitronScanner identified 64,654
<italic>Helitrons</italic>
from a wide range of plant genomes in a highly automated way. We tested HelitronScanner’s predictive ability in maize, a species with highly heterogeneous
<italic>Helitron</italic>
elements. LCV scores for the 5′ and 3′ termini of the predicted
<italic>Helitrons</italic>
provide a primary confidence level and element copy number provides a secondary one. Newly identified
<italic>Helitrons</italic>
were validated by PCR assays or by in silico comparative analysis of insertion site polymorphism among multiple accessions. Many new
<italic>Helitrons</italic>
were identified in model species, such as maize, rice, and
<italic>Arabidopsis</italic>
, and in a variety of organisms where
<italic>Helitrons</italic>
had not been reported previously to our knowledge, leading to a major upward reassessment of their abundance in plant genomes. HelitronScanner promises to be a valuable tool in future comparative and evolutionary studies of this major transposon superfamily.</p>
</abstract>
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