Dataset Information

Distribution, diversity, evolution, and survival of Helitrons in the maize genome.

ABSTRACT: Homology and structure-based approaches were used to identify Helitrons in the genome of maize inbred B73. A total of 1,930 intact Helitrons from eight families (62 subfamilies) and >20,000 Helitron fragments were identified, accounting for approximately 2.2% of the B73 genome. Transposition of at least one of these families is ongoing, but the most prominent burst of amplification activity was approximately 250,000 years ago. Sixty percent of maize Helitrons were found to have captured fragments of nuclear genes ( approximately 840 different fragment acquisitions, with tens of thousands of predicted gene fragments inside Helitrons within the B73 assembly). Most acquired gene fragments are undergoing random drift, but 4% were calculated to be under purifying selection, whereas another 4% exhibit apparent adaptive selection, suggesting beneficial effects for the host or Helitron transposition/retention. Gene fragment capture is frequent in some Helitron subfamilies, with as many as 10 unlinked genes providing DNA inserts within a single element. Gene fragment acquisition appears to positively influence element survival and/or ability of the Helitron to acquire additional gene fragments. Helitrons with gene fragment captures in the antisense orientation have a lesser chance of survival. Helitron distribution in maize exhibits severe biases, including preferential accumulation in relatively gene-rich regions. Insertions, however, are not usually found inside genes. Rather, Helitrons preferentially insert near (but not into) other Helitrons. This biased accumulation is not caused by a preference for cis or nearby transposition, suggesting a specific association between Helitron integration functions and unknown chromatin characteristics that specifically mark Helitrons.

SUBMITTER: Yang L

PROVIDER: S-EPMC2785268 | biostudies-literature | 2009 Nov

REPOSITORIES: biostudies-literature

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Distribution, diversity, evolution, and survival of Helitrons in the maize genome.

Yang Lixing L Bennetzen Jeffrey L JL

Proceedings of the National Academy of Sciences of the United States of America 20091119 47

Homology and structure-based approaches were used to identify Helitrons in the genome of maize inbred B73. A total of 1,930 intact Helitrons from eight families (62 subfamilies) and >20,000 Helitron fragments were identified, accounting for approximately 2.2% of the B73 genome. Transposition of at least one of these families is ongoing, but the most prominent burst of amplification activity was approximately 250,000 years ago. Sixty percent of maize Helitrons were found to have captured fragment ...[more]

PMID: 19926865

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Project description:Recent comprehensive sequence analysis of the maize genome now permits detailed discovery and description of all transposable elements (TEs) in this complex nuclear environment. Reiteratively optimized structural and homology criteria were used in the computer-assisted search for retroelements, TEs that transpose by reverse transcription of an RNA intermediate, with the final results verified by manual inspection. Retroelements were found to occupy the majority (>75%) of the nuclear genome in maize inbred B73. Unprecedented genetic diversity was discovered in the long terminal repeat (LTR) retrotransposon class of retroelements, with >400 families (>350 newly discovered) contributing >31,000 intact elements. The two other classes of retroelements, SINEs (four families) and LINEs (at least 30 families), were observed to contribute 1,991 and approximately 35,000 copies, respectively, or a combined approximately 1% of the B73 nuclear genome. With regard to fully intact elements, median copy numbers for all retroelement families in maize was 2 because >250 LTR retrotransposon families contained only one or two intact members that could be detected in the B73 draft sequence. The majority, perhaps all, of the investigated retroelement families exhibited non-random dispersal across the maize genome, with LINEs, SINEs, and many low-copy-number LTR retrotransposons exhibiting a bias for accumulation in gene-rich regions. In contrast, most (but not all) medium- and high-copy-number LTR retrotransposons were found to preferentially accumulate in gene-poor regions like pericentromeric heterochromatin, while a few high-copy-number families exhibited the opposite bias. Regions of the genome with the highest LTR retrotransposon density contained the lowest LTR retrotransposon diversity. These results indicate that the maize genome provides a great number of different niches for the survival and procreation of a great variety of retroelements that have evolved to differentially occupy and exploit this genomic diversity.

Project description:BACKGROUND: As a newly identified category of DNA transposon, helitrons have been found in a large number of eukaryotes genomes. Helitrons have contributed significantly to the intra-specific genome diversity in maize. Although many characteristics of helitrons in the maize genome have been well documented, the sequence of an intact autonomous helitrons has not been identified in maize. In addition, the process of gene fragment capturing during the transposition of helitrons has not been characterized. RESULTS: The whole genome sequences of maize inbred line B73 were analyzed, 1,649 helitron-like transposons including 1,515 helAs and 134 helBs were identified. ZmhelA1, ZmhelB1 and ZmhelB2 all encode an open reading frame (ORF) with intact replication initiator (Rep) motif and a DNA helicase (Hel) domain, which are similar to previously reported autonomous helitrons in other organisms. The putative autonomous ZmhelB1 and ZmhelB2 contain an extra replication factor-a protein1 (RPA1) transposase (RPA-TPase) including three single strand DNA-binding domains (DBD)-A/-B/-C in the ORF. Over ninety percent of maize helitrons identified have captured gene fragments. HelAs and helBs carry 4,645 and 249 gene fragments, which yield 2,507 and 187 different genes respectively. Many helitrons contain mutilple terminal sequences, but only one 3'-terminal sequence had an intact "CTAG" motif. There were no significant differences in the 5'-termini sequence between the veritas terminal sequence and the pseudo sequence. Helitrons not only can capture fragments, but were also shown to lose internal sequences during the course of transposing. CONCLUSIONS: Three putative autonomous elements were identified, which encoded an intact Rep motif and a DNA helicase domain, suggesting that autonomous helitrons may exist in modern maize. The results indicate that gene fragments captured during the transposition of many helitrons happen in a stepwise way, with multiple gene fragments within one helitron resulting from several sequential transpositions. In addition, we have proposed a potential mechanism regarding how helitrons with multiple termini are generated.

Dataset Information

Distribution, diversity, evolution, and survival of Helitrons in the maize genome.

Publications

Distribution, diversity, evolution, and survival of Helitrons in the maize genome.

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