Insertion bias and purifying selection of retrotransposons in the Arabidopsis thalianagenome

Pereira, Vini

doi:10.1186/gb-2004-5-10-r79

Cited by 144 publications

(84 citation statements)

References 66 publications

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“…The short arms of chromosomes 2 and 4 were removed for clarity (33). Circles, triangles, and stars mark the first, second, and third quartiles, respectively.…”

Section: Discussionmentioning

confidence: 99%

PolIVb influences RNA-directed DNA methylation independently of its role in siRNA biogenesis

Mosher

Schwach

Studholme

et al. 2008

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

250

290

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DNA-dependent RNA polymerase (Pol)IV in Arabidopsis exists in two isoforms (PolIVa and PolIVb), with NRPD1a and NRPD1b as their respective largest subunits. Both isoforms are implicated in production and activity of siRNAs and in RNA-directed DNA methylation (RdDM). Deep sequence analysis of siRNAs in WT Arabidopsis flowers and in nrpd1a and nrpd1b mutants identified >4,200 loci producing siRNAs in a PolIV-dependent manner, with PolIVb reinforcing siRNA production by PolIVa. Transposable element identity and pericentromeric localization are both features that predispose a locus for siRNA production via PolIV proteins and determine the extent to which siRNA production relies on PolIVb. Detailed analysis of DNA methylation at PolIV-dependent loci revealed unexpected deviations from the previously noted association of PolIVb-dependent siRNA production and RdDM. Notably, PolIVb functions independently in DNA methylation and siRNA generation. Additionally, we have uncovered siRNA-directed loss of DNA methylation, a process requiring both PolIV isoforms. From these findings, we infer that the role of PolIVb in siRNA production is secondary to a role in chromatin modification and is influenced by chromatin context.

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“…The short arms of chromosomes 2 and 4 were removed for clarity (33). Circles, triangles, and stars mark the first, second, and third quartiles, respectively.…”

Section: Discussionmentioning

confidence: 99%

PolIVb influences RNA-directed DNA methylation independently of its role in siRNA biogenesis

Mosher

Schwach

Studholme

et al. 2008

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

250

290

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“…Assuming that 18-22% of the rice genome is composed of LTR retrotransposons (30,37), LTR retrotransposons are at least 3-or 4-fold enriched in centromeric region compared with most noncentromeric regions. Although the evolutionary mechanisms behind preferential insertion and͞or retention bias for LTR retrotransposons in centromeric regions are still poorly understood, the nonrandom distribution of LTR retrotransposons should at least partly reflect the action of purifying selection against the deleterious effects of LTR-retrotransposon insertion into genes (45).…”

Section: Discussionmentioning

confidence: 99%

Recombination, rearrangement, reshuffling, and divergence in a centromeric region of rice

Bennetzen

2005

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

126

134

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Centromeres have many unusual biological properties, including kinetochore attachment and severe repression of local meiotic recombination. These properties are partly an outcome, partly a cause, of unusual DNA structure in the centromeric region. Although several plant and animal genomes have been sequenced, most centromere sequences have not been completed or analyzed in depth. To shed light on the unique organization, variability, and evolution of centromeric DNA, detailed analysis of a 1.97-Mb sequence that includes centromere 8 (CEN8) of japonica rice was undertaken. Thirty-three long-terminal repeat (LTR)-retrotransposon families (including 11 previously unknown) were identified in the CEN8 region, totaling 245 elements and fragments that account for 67% of the region. The ratio of solo LTRs to intact elements in the CEN8 region is Ϸ0.9:1, compared with Ϸ2.2:1 in noncentromeric regions of rice. However, the ratio of solo LTRs to intact elements in the core of the CEN8 region (Ϸ2.5:1) is higher than in any other region investigated in rice, suggesting a hotspot for unequal recombination. Comparison of the CEN8 region of japonica and its orthologous segments from indica rice indicated that Ϸ15% of the intact retrotransposons and solo LTRs were inserted into CEN8 after the divergence of japonica and indica from a common ancestor, compared with Ϸ50% for previously studied euchromatic regions. Frequent DNA rearrangements were observed in the CEN8 region, including a 212-kb subregion that was found to be composed of three rearranged tandem repeats. Phylogenetic analysis also revealed recent segmental duplication and extensive rearrangement and reshuffling of the CentO satellite repeats.CentO repeats ͉ DNA evolution ͉ nucleotide substitution ͉ unequal conversion T he centromeres of eukaryotic chromosomes are essential for precise chromosome segregation during mitosis and meiosis. Although this function is conserved, the DNA content, organization, and complexity of centromeres vary considerably across different organisms (1-3). Budding yeast (Saccharomyces cerevisiae) centromeres consist of only Ϸ125 bp of unique sequence (4, 5). In contrast, centromeres from most multicellular eukaryotes, including Arabidopsis (6-8), rice (9-12), maize (13, 14), Drosophila (15), and human (16, 17) are much more complex. These large heterochromatic centromeres consist of large arrays of satellite repeats that are usually arranged in a tandem head-totail fashion, intermixed with additional repeats, including transposable elements. Although tandem repeats of some sort appear to be necessary for efficient centromere function in most eukaryotes, the direct effector of kinetochore formation is the assembly of an altered chromatin state in the centromere, associated with a unique H3 histone (CENH3) (18).In all plant centromeres investigated, the sizes of satellite repeat units (also called monomers) are relatively consistent, ranging from Ϸ150 to Ϸ180 bp [e.g., 155 bp for rice CentO (9), 156 bp for maize CentC (13), and 180 bp for Arabi...

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“…In species such as A. thaliana where blocks of euchromatin and heterochromatin are distinct and well characterized, Ty3/gypsy retrotransposons (of which the chromoviruses are a member) show a significant association with heterochromatin compared with Ty1/copia retrotransposons (Pereira 2004;Peterson-Burch et al 2004). This holds true for insertions of our representative group II chromovirus, Tma, which are clustered in pericentromeric regions (Supplemental Fig.…”

Section: Retrotransposons With Chromodomains Are Associated With Repementioning

confidence: 99%

Chromodomains direct integration of retrotransposons to heterochromatin

Gao¹,

Hou²,

et al. 2008

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The enrichment of mobile genetic elements in heterochromatin may be due, in part, to targeted integration. The chromoviruses are Ty3/gypsy retrotransposons with chromodomains at their integrase C termini. Chromodomains are logical determinants for targeting to heterochromatin, because the chromodomain of heterochromatin protein 1 (HP1) typically recognizes histone H3 K9 methylation, an epigenetic mark characteristic of heterochromatin. We describe three groups of chromoviruses based on amino acid sequence relationships of their integrase C termini. Genome sequence analysis indicates that representative chromoviruses from each group are enriched in gene-poor regions of the genome relative to other retrotransposons, and when fused to fluorescent marker proteins, the chromodomains target proteins to specific subnuclear foci coincident with heterochromatin. The chromodomain of the fungal element, MAGGY, interacts with histone H3 dimethyl-and trimethyl-K9, and when the MAGGY chromodomain is fused to integrase of the Schizosaccharomyces pombe Tf1 retrotransposon, new Tf1 insertions are directed to sites of H3 K9 methylation. Repetitive sequences such as transposable elements trigger the RNAi pathway resulting in their epigenetic modification. Our results suggest a dynamic interplay between retrotransposons and heterochromatin, wherein mobile elements recognize heterochromatin at the time of integration and then perpetuate the heterochromatic mark by triggering epigenetic modification.[Supplemental material is available online at www.genome.org.] (Girard et al. 2006;Grivna et al. 2006;Vagin et al. 2006). Mobile element insertions that decorate eukaryotic genomes, therefore, frequently define unique chromatin domains. Whereas the genetic consequences of transposition in terms of mutation and genome rearrangement have long been recognized, the biological consequences of their epigenetic marks, which include effects on gene expression and the formation of heterochromatin, are only beginning to be appreciated (Slotkin and Martienssen 2007).Underlying the genetic and epigenetic impact of mobile elements is integration site choice. Although forces such as selection or recombination contribute to the nonrandom distribution of mobile elements in eukaryotic genomes, an increasing number of studies indicate that many mobile elements target integration to specific chromosomal sites (Bushman 2003). For some elements, target sites are determined by recognizing specific DNA sequences, whereas for others, including several retrotransposons and retroviruses, chromatin impacts target site choice. The Ty1 and Ty3 retrotransposons of Saccharomyces cerevisiae, for example, integrate near sites of RNA polymerase III (pol III) transcription by recognizing pol III transcription complexes or chromatin states associated with pol III transcription (Yieh et al. 2000(Yieh et al. , 2002Bachman et al. 2005;Mou et al. 2006). The Tf1 retrotransposon of Schizosaccharomyces pombe recognizes certain RNA polymerase II (pol II) promoters (Singleton and L...

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Insertion bias and purifying selection of retrotransposons in the Arabidopsis thalianagenome

Cited by 144 publications

References 66 publications

PolIVb influences RNA-directed DNA methylation independently of its role in siRNA biogenesis

PolIVb influences RNA-directed DNA methylation independently of its role in siRNA biogenesis

Recombination, rearrangement, reshuffling, and divergence in a centromeric region of rice

Chromodomains direct integration of retrotransposons to heterochromatin

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