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The centromeric retrotransposons of rice are transcribed and differentially processed by RNA interference.

ABSTRACT: Retrotransposons consist of significant portions of many complex eukaryotic genomes and are often enriched in heterochromatin. The centromeric retrotransposon (CR) family in grass species is colonized in the centromeres and highly conserved among species that have been diverged for >50 MY. These unique characteristics have inspired scientists to speculate about the roles of CR elements in organization and function of centromeric chromatin. Here we report that the CRR (CR of rice) elements in rice are highly enriched in chromatin associated with H3K9me2, a hallmark for heterochromatin. CRR elements were transcribed in root, leaf, and panicle tissues, suggesting a constitutive transcription of this retrotransposon family. However, the overall transcription level was low and the CRR transcripts appeared to be derived from relatively few loci. The majority of the CRR transcripts had chimerical structures and contained only partial CRR sequences. We detected small RNAs (smRNAs) cognate to nonautonomous CRR1 (noaCRR1) and CRR1, but not CRR2 elements. This result was also confirmed by in silico analysis of rice smRNA sequences. These results suggest that different CRR subfamilies may play different roles in the RNAi-mediated pathway for formation and maintenance of centromeric heterochromatin.

SUBMITTER: Neumann P

PROVIDER: S-EPMC1894605 | biostudies-literature | 2007 Jun

REPOSITORIES: biostudies-literature

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The centromeric retrotransposons of rice are transcribed and differentially processed by RNA interference.

Neumann Pavel P Yan Huihuang H Jiang Jiming J

Genetics 20070403 2

Retrotransposons consist of significant portions of many complex eukaryotic genomes and are often enriched in heterochromatin. The centromeric retrotransposon (CR) family in grass species is colonized in the centromeres and highly conserved among species that have been diverged for >50 MY. These unique characteristics have inspired scientists to speculate about the roles of CR elements in organization and function of centromeric chromatin. Here we report that the CRR (CR of rice) elements in ric ...[more]

PMID: 17409063

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Project description:BackgroundTandem repeats are ubiquitous and abundant in higher eukaryotic genomes and constitute, along with transposable elements, much of DNA underlying centromeres and other heterochromatic domains. In maize, centromeric satellite repeat (CentC) and centromeric retrotransposons (CR), a class of Ty3/gypsy retrotransposons, are enriched at centromeres. Some satellite repeats have homology to retrotransposons and several mechanisms have been proposed to explain the expansion, contraction as well as homogenization of tandem repeats. However, the origin and evolution of tandem repeat loci remain largely unknown.ResultsCRM1TR and CRM4TR are novel tandem repeats that we show to be entirely derived from CR elements belonging to two different subfamilies, CRM1 and CRM4. Although these tandem repeats clearly originated in at least two separate events, they are derived from similar regions of their respective parent element, namely the long terminal repeat (LTR) and untranslated region (UTR). The 5' ends of the monomer repeat units of CRM1TR and CRM4TR map to different locations within their respective LTRs, while their 3' ends map to the same relative position within a conserved region of their UTRs. Based on the insertion times of heterologous retrotransposons that have inserted into these tandem repeats, amplification of the repeats is estimated to have begun at least ~4 (CRM1TR) and ~1 (CRM4TR) million years ago. Distinct CRM1TR sequence variants occupy the two CRM1TR loci, indicating that there is little or no movement of repeats between loci, even though they are separated by only ~1.4 Mb.ConclusionsThe discovery of two novel retrotransposon derived tandem repeats supports the conclusions from earlier studies that retrotransposons can give rise to tandem repeats in eukaryotic genomes. Analysis of monomers from two different CRM1TR loci shows that gene conversion is the major cause of sequence variation. We propose that successive intrastrand deletions generated the initial repeat structure, and gene conversions increased the size of each tandem repeat locus.

Project description:BACKGROUND:The centromeric and pericentromeric regions of plant chromosomes are colonized by Ty3/gypsy retrotransposons, which, on the basis of their reverse transcriptase sequences, form the chromovirus CRM clade. Despite their potential importance for centromere evolution and function, they have remained poorly characterized. In this work, we aimed to carry out a comprehensive survey of CRM clade elements with an emphasis on their diversity, structure, chromosomal distribution and transcriptional activity. RESULTS:We have surveyed a set of 190 CRM elements belonging to 81 different retrotransposon families, derived from 33 host species and falling into 12 plant families. The sequences at the C-terminus of their integrases were unexpectedly heterogeneous, despite the understanding that they are responsible for targeting to the centromere. This variation allowed the division of the CRM clade into the three groups A, B and C, and the members of each differed considerably with respect to their chromosomal distribution. The differences in chromosomal distribution coincided with variation in the integrase C-terminus sequences possessing a putative targeting domain (PTD). A majority of the group A elements possess the CR motif and are concentrated in the centromeric region, while members of group C have the type II chromodomain and are dispersed throughout the genome. Although representatives of the group B lack a PTD of any type, they appeared to be localized preferentially in the centromeres of tested species. All tested elements were found to be transcriptionally active. CONCLUSIONS:Comprehensive analysis of the CRM clade elements showed that genuinely centromeric retrotransposons represent only a fraction of the CRM clade (group A). These centromeric retrotransposons represent an active component of centromeres of a wide range of angiosperm species, implying that they play an important role in plant centromere evolution. In addition, their transcriptional activity is consistent with the notion that the transcription of centromeric retrotransposons has a role in normal centromere function.

Dataset Information

The centromeric retrotransposons of rice are transcribed and differentially processed by RNA interference.

Publications

The centromeric retrotransposons of rice are transcribed and differentially processed by RNA interference.

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