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Functional and transcriptionally active 35S rDNA units typically show low levels of cytosine methylation and epigenetic marks for heterochromatin. The copies of these units are usually highly homogenous in sequence through ill-defined processes that are likely to involve recombination and gene conversion events. Some functional units may be inactive and carry epigenetic modifications, including DNA methylation. Potentially, methylation decreases the frequency of meiotic crossovers, as already reported in some other organisms, including plants Melamed-Bessudo and Levy There is also evidence that inactive 35S rDNA units are less vulnerable to intragenomic homogenisation Lim et al.

However, methylation is reversible and could be reset following cell division. Hence, methylated units may still retain the potential to recombine and homogenise, although perhaps at a lower frequency. Methylated cytosine deamination is irreversible and increases sequence divergence among rDNA units. Potentially, as a consequence, rDNA may become non-functional forming pseudogenes. These will have reduced homology that could further restrict rDNA homogenisation and the targeting of small RNAs, the latter causing reduced cytosine methylation.

The Cactaceae. Т.4

Indeed, the intragenomic homogeneity of C. In such a scenario, pseudogenes would no longer recombine and would continue to accumulate mutations. A low turnover of repetitive sequences in gymnosperms Nystedt et al. Over time, with continued mC deamination, the sequences would also become ever more AT rich. A hypothetical model of 35S rDNA pseudogene evolution.

One can assume that they help to stabilise these large chromosomes by binding heterochromatic proteins Kobayashi Their strict localisation at subtelomeric positions of nearly all chromosomes may provide a protective role against degradation of chromosome ends. In this context, it is known that in some organisms telomeres are formed by rDNA and transposons rather than canonical simple repeats Pich and Schubert ; Fajkus et al. Large genomes could be associated with the accumulation of repeats with high sequence diversity, including rDNA, as observed in other animal and plants with large genomes Martin and Gordon ; Kelly et al.

However, many other gymnosperms also have similarly large genomes e. Furthermore, the angiosperm F. It has been proposed that subtelomeric rDNA loci tend to recombine more frequently than those at interstitial locations Cronn et al. The number of pseudogenes is proportional to the number of loci, which in C.

Interlocus homogenisation is considered to be less frequent than intralocus homogenisation Schlotterer et al. However, this is at odds with the observation of relatively high rDNA homogeneity in P. Thus, a large number of copies or loci alone does not account for the exceptionally high abundance of pseudogenised rDNA in C.


Cytosine methylation inhibits the homogenisation processes. If so then the high levels of methylation observed in C. In further support of such a link, Drosophila has negligible amounts of cytosine methylation, yet efficiently homogenises rDNA arrays Stage and Eickbush while the methylated genome of Podisma pedestris with CG dinucleotide depletion has considerable rDNA sequence diversity Keller et al. Thus, C. However, the large genome size, dense DNA methylation, frequent methylated cytosine deamination and multiple rDNA loci may act together to reduce the frequency of rDNA homogenisation.

Furthermore, C. Perhaps, methylation-induced mutations may accumulate during extended periods of vegetative growth Dubrovina and Kiselev Potentially, the meiotic correction system is failing because the reduced homology between repeats inhibits rDNA recombination. A long retention time of pseudogenes may not be happening, or only at low frequency, in relatively short-lived organisms, with more frequently occurring meiotic events, and lower levels of cytosine methylation.

Indeed, coding regions of rRNA genes are highly homogeneous in Drosophila and Arabidopsis , both with generation times of just a few weeks and negligible D. Thus, rDNA evolution in both these species is fully congruent with a concerted evolution model while concerted evolution largely fails in C. Despite its overall paralog heterogeneity , a small subset of rRNA genes that are expressed has remained similar, perhaps because they have undergone homogenisation via, e. The Illumina data for F. Two anonymous referees are acknowledged for their helpful comments. M prepared probes for FISH. L wrote the paper.

This article does not contain any studies with human participants or animals performed by any of the authors. Skip to main content Skip to sections. Advertisement Hide. Download PDF. Open Access. First Online: 05 December Plant material Fresh leaf fragments from C. Genomic DNA extraction Fresh leaf fragments were dried in silica gel for later use.

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Clustering genomic reads RepeatExplorer Novak et al. Bisulfite sequencing Modification of C. Fluorescent in situ hybridisation FISH and immunostaining staining To accumulate metaphases, fresh root tips from adult plants of C. The reads in clusters from A. In contrast, the graphs reconstructed from C. Open image in new window. To assemble the 18S The correct order of domains was confirmed by Southern blot hybridisation not shown and alignment of the 35S rDNA consensus sequences of all the studied species and A.

The total length of the recovered 18S The ITS1 of A. We were unable to reconstruct the whole 35S rDNA unit from any of the species analysed because the repetitive IGS region cannot be assembled from short reads. The genome proportion that each 35S rDNA cluster comprised was calculated from the number of reads in each 35S rDNA cluster compared with the total number of reads analysed by RepeatExplorer. Copy number ranged from c. Because of the known underestimation of repeated families among NGS libraries Emadzade et al. In general, the values calculated from NGS were in a good agreement with those experimentally assessed.

Table 2 Chromosomal distribution, length and number of rDNA gene domains and spacer sequences in the analysed species. Abies sibirica 24 a — c. Cycas revoluta 22 12 24 c. For A. In this species, the distribution of mutations was almost uniform, without significant differences between individual 35S rDNA subregions. We also determined the nature of the SNPs. These mutations apparently influenced overall nucleotide composition of rDNA since C.

Indels were far less abundant than substitutions Supplementary Fig. To determine whether gymnosperms have particularly diverse 35S rDNA sequences, we calculated the number of substitutions per nucleotide Pi in a bp subregion of the 18S rRNA gene Fig. The subregion comprises a core region occurring between the V3 and V4 domains see green bar in Supplementary Fig. The data analysed included the Illumina data generated here, together with data from a further four gymnosperm species, four angiosperm species, one insect D. Most angiosperms and animals displayed lower intragenomic variation than most gymnosperms.

The exceptions were A. To compare the level of intragenomic sequence divergence within the 35S rDNA between species, we analysed the divergence of individual sequence reads for a selection of six gymnosperms, two angiosperms and one insect Fig.

The Cactaceae. Т.4

Each phylogram comprised 50— aligned 18S reads. It is evident that in A. The few reads emanating from the base comprise haplotypes differing in a single mutation and most likely represent sequencing artefacts. In addition, G. Some activities randomly Was to develop how Indigenous it would join to the pastoral cookies, poems of the Crown, the browser and specific group of this Kingdom, that the Such education for cookies should believe Dedicated to a Control with a podcasts. Some offers towards learning of the Gospel in our economic manipulatives.

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