A Novel Hybrid Open Reading Frame Formed by Multiple Cellular Gene Transductions by a Plant Long Terminal Repeat Retroelement

Elrouby, Nabil; Bureau, Thomas E.

doi:10.1074/jbc.m105850200

Cited by 32 publications

(38 citation statements)

References 56 publications

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“…This sequence could have been acquired by the element via capture of a cellular gene, as was reported for retroviruses (Telesnitsky and Goff et al, 1997) and also for the maize retrotransposon Bs1 (Elrouby and Bureau, 2001). However, the copy numbers of the ORF1 sequences in the pea genome are close to those of other parts of the Ogre elements, suggesting that they are present in most or all element copies.…”

Section: Discussionmentioning

confidence: 98%

Highly abundant pea LTR retrotransposon Ogre is constitutively transcribed and partially spliced

2003

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We have isolated and characterized a novel giant retroelement, named Ogre, which is over 22 kb long and makes up at least 5% of the pea (Pisum sativum L.) genome. This element can be classified as a Ty3/gypsy-like LTR retrotransposon based on the presence of long terminal repeats (LTRs) and the order of the domains coding for typical retrotransposon proteins. In addition to its extreme length, it has several features which make it unique among the retroelements described so far: (1) the sequences coding for gag and prot proteins are separated from the rt/rh-int domains by several stop codons; (2) the region containing these stop codons is removed from the element transcripts by splicing which results in reconstitution of the complete gag-pol coding sequence; (3) only a part of the transcripts is spliced which probably determines the ratio of translated proteins; (4) the element contains an extra ORF located upstream the gag-pol coding sequences, potentially coding for a protein of 546-562 amino acids with unknown function. The transcriptional activity of the Ogre elements has been detected in all organs tested (leaves, roots, flowers) as well as in wounded leaves and protoplasts. Considering this retroelement's constitutive expression and observed high mutual similarity of the element genomic sequences, it is possible to speculate about its recent amplification in the genomes of pea and other legume plants.

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Section: Discussionmentioning

confidence: 98%

Highly abundant pea LTR retrotransposon Ogre is constitutively transcribed and partially spliced

2003

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“…If, as suggested for helicase and RPA (12), these genes are being recruited from the host, the requirements for gene capture by nonautonomous maize Helitrons do not appear to be very stringent. The capture of genes or gene fragments from the host by transposable elements has been documented in several plants (28)(29)(30)(31)(32). The maize Helitrons share several features with the Pack-MULEs (mutator-like elements) recently described in rice (33): Most of the sequences captured are gene fragments, not complete genes; a single element can contain fragments from multiple genes; sequence acquisition is at the DNA level, as indicated by the conservation of introns; and transcripts can initiate within the element (e.g., hypro2) or outside of the element, producing chimeric transcripts (13,16).…”

Section: Discussionmentioning

confidence: 99%

Gene movement by Helitron transposons contributes to the haplotype variability of maize

Lai

Li²,

Messing³

et al. 2005

Proc. Natl. Acad. Sci. U.S.A.

246

240

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(1, 2), a line that had been used extensively in genetic analyses, with that of the unrelated standard inbred B73 (3) revealed unexpected differences between them. First, retrotransposon clusters, which make up the bulk of the maize genome (4-6), differed in composition and location relative to the genes in the region so that the two sequences could be aligned only at the genes they had in common. Second, and most strikingly, some genes present in McC were absent from B73, indicating that genetic colinearity was violated within the species. Noncolinear haplotypes were also found in a comparison of the genomic intervals containing the z1C zein gene cluster in B73 and BSSS53, inbred lines derived from the same synthetic population (7). The lengths of the z1C regions in the two inbreds varied by 50% because of differences in the number of zein and other genes and in the sizes of the retrotransposon clusters flanking them. Similar extensive nonhomologies were reported between the allelic regions of inbreds B73 and Mo17 at three additional chromosomal locations in the genome (8). That study established that more than one-third of the predicted genes were present in just one inbred at the loci examined, although many of the unshared genes appeared to be truncated. The observation that genes not shared between inbreds violate the maize-rice colinearity usually displayed by shared genes prompted the authors to speculate that unshared genes originated from insertions of a yet-unknown nature rather than deletions.High intraspecific haplotype variability is not restricted to maize, having been recently described in barley, another species with a large amount of repetitive DNA. A comparison of the Rph7 locus in two barley cultivars established that colinearity was restricted to Ͻ35% of the two sequences, principally because of differences in retrotransposon blocks (9). Interestingly, a gene encoding a truncated helicase was present in only one of the two cultivars. On the other hand, no cases of gene acquisition or loss were found in a comparison of two different orthologous regions between rice subspecies (10, 11). This finding suggests that the type of variation detected in maize and barley may not be a general feature of plant genomes. The functional significance of the ''plus-minus'' type of variation is also unclear, because the genes that vary among accessions of the same species are present in multiple copies (3), and many of them are clearly pseudogenes or gene fragments (8, 9). Independent of its generality or functional significance, the described variation raises an important question: How did it arise? Evidence presented here indicates that the apparent intraspecific violations of genetic colinearity in maize and, probably, barley, arise from the movement of genes or gene fragments by Helitrons, a recently discovered type of eukaryotic transposon (12).Helitrons were found by computational analysis of genomic sequences from Arabidopsis, rice, and Caenorhabditis elegans (12) and were later reported to be the caus...

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“…A version of the maize retroposon Bs1 contains sequences similar to a portion of the spliced transcript of a plasma membrane H ϩ -ATPase (Bureau et al, 1994;Jin and Bennetzen, 1994;Palmgren, 1994). The recent discovery of two additional genes transduced by Bs1 suggests that capture of multiple genes by retroelements may facilitate gene evolution by the formation of new hybrid genes (Elrouby and Bureau, 2001).…”

Section: The Maize Mutation Sh2-7527 Most Likely Was Caused By a Helimentioning

confidence: 99%

The Maize Genome Contains a Helitron Insertion

et al. 2003

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The maize mutation sh2-7527 was isolated in a conventional maize breeding program in the 1970s. Although the mutant contains foreign sequences within the gene, the mutation is not attributable to an interchromosomal exchange or to a chromosomal inversion. Hence, the mutation was caused by an insertion. Sequences at the two Sh2 borders have not been scrambled or mutated, suggesting that the insertion is not caused by a catastrophic reshuffling of the maize genome. The insertion is large, at least 12 kb, and is highly repetitive in maize. As judged by hybridization, sorghum contains only one or a few copies of the element, whereas no hybridization was seen to the Arabidopsis genome. The insertion acts from a distance to alter the splicing of the sh2 pre-mRNA. Three distinct intron-bearing maize genes were found in the insertion. Of most significance, the insertion bears striking similarity to the recently described DNA helicase-bearing transposable elements termed Helitrons . Like Helitrons , the inserted sequence of sh2-7527 is large, lacks terminal repeats, does not duplicate host sequences, and was inserted between a host dinucleotide AT. Like Helitrons , the maize element contains 5 TC and 3 CTRR termini as well as two short palindromic sequences near the 3 terminus that potentially can form a 20-bp hairpin. Although the maize element lacks sequence information for a DNA helicase, it does contain four exons with similarity to a plant DEAD box RNA helicase. A second Helitron insertion was found in the maize genomic database. These data strongly suggest an active Helitron in the present-day maize genome.

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A Novel Hybrid Open Reading Frame Formed by Multiple Cellular Gene Transductions by a Plant Long Terminal Repeat Retroelement

Cited by 32 publications

References 56 publications

Highly abundant pea LTR retrotransposon Ogre is constitutively transcribed and partially spliced

Highly abundant pea LTR retrotransposon Ogre is constitutively transcribed and partially spliced

Gene movement by Helitron transposons contributes to the haplotype variability of maize

The Maize Genome Contains a Helitron Insertion

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