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Comparative Study
.2008 Apr;18(4):571-84.
doi: 10.1101/gr.6897308. Epub 2008 Mar 6.

Comparative analysis of the small RNA transcriptomes of Pinus contorta and Oryza sativa

Affiliations
Comparative Study

Comparative analysis of the small RNA transcriptomes of Pinus contorta and Oryza sativa

Ryan D Morin et al. Genome Res.2008 Apr.

Abstract

The diversity of microRNAs and small-interfering RNAs has been extensively explored within angiosperms by focusing on a few key organisms such as Oryza sativa and Arabidopsis thaliana. A deeper division of the plants is defined by the radiation of the angiosperms and gymnosperms, with the latter comprising the commercially important conifers. The conifers are expected to provide important information regarding the evolution of highly conserved small regulatory RNAs. Deep sequencing provides the means to characterize and quantitatively profile small RNAs in understudied organisms such as these. Pyrosequencing of small RNAs from O. sativa revealed, as expected, approximately 21- and approximately 24-nt RNAs. The former contained known microRNAs, and the latter largely comprised intergenic-derived sequences likely representing heterochromatin siRNAs. In contrast, sequences from Pinus contorta were dominated by 21-nt small RNAs. Using a novel sequence-based clustering algorithm, we identified sequences belonging to 18 highly conserved microRNA families in P. contorta as well as numerous clusters of conserved small RNAs of unknown function. Using multiple methods, including expressed sequence folding and machine learning algorithms, we found a further 53 candidate novel microRNA families, 51 appearing specific to the P. contorta library. In addition, alignment of small RNA sequences to the O. sativa genome revealed six perfectly conserved classes of small RNA that included chloroplast transcripts and specific types of genomic repeats. The conservation of microRNAs and other small RNAs between the conifers and the angiosperms indicates that important RNA silencing processes were highly developed in the earliest spermatophytes. Genomic mapping of all sequences to the O. sativa genome can be viewed at http://microrna.bcgsc.ca/cgi-bin/gbrowse/rice_build_3/.

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Figures

Figure 1.
Figure 1.
Lengths of unique small RNA sequences fromP. contorta (black bars, 58,466 sequences) andO. sativa (gray bars, 8615 sequences). The bulk ofP. contorta small RNAs are 21 nt long with low variance (σ = 8.1). The rice sequences have a major peak at 24 nt and a minor peak at 21 nt, yielding a median of 22 nt and a higher variance (σ = 20.0). The 21-nt peak becomes more prominent when sequence degeneracy is considered (not shown).
Figure 2.
Figure 2.
Length distribution of uniqueP. contorta (black bars) andO. sativa (gray bars) small RNAs sorted by class and that map perfectly to at least one genomic locus in theO. sativa genome. A total of 5129 uniqueP. contorta sequences mapped to theO. sativa genome. TheY-axis reflects the fraction of sequences of the stated annotation residing within each length bin. (A) Genomic repeats as annotated by RepeatMasker using RepBase, v. 9.04. Two distinct lobes are observable, the first due mainly to the high probability of shorter sequences occurring by chance in the genome. The second lobe peaks for both species with 24-nt sequences, suggesting an over-representation of conserved sequences that are 24 nt in length. (B) Conserved miRNAs matching sequences in miRBase release 9.1. These miRNAs are almost exclusively 20–22 nt in length in both species. (C) rRNA as identified by overlap with annotated rRNA genes in the rice genome. The relative lack of ribosomal fragments below 18 nt likely corresponds to the cutoff imposed by gel purification. (D) tRNA as annotated by tRNAscan-SE. (E) Un-annotated, small RNAs not overlapping with sequences annotated by the aforementioned methods. Again, a peak is observed at 24 nt forP. contorta sequences, revealing a higher proportion of evolutionarily conserved sequences in this class reside in the 24-nt fraction than in the 23- or 25-nt fractions.
Figure 3.
Figure 3.
Degenerate alignment density ofO. sativa 24- and 21-nt small RNAs to the nuclear genome. All distinctO. sativa small RNA sequences were aligned to all 12 chromosomes allowing degenerate alignments (see Methods). The 24-nt (positive axis) and 21-nt sequences (negative axis) demonstrated distinctive alignment patterns. Specifically, “hot spots” of 24-nt sequences include the heterochromatic regions including most centromeres (blue) as well as some clusters of ribosomal RNA genes (red). Positions of known miRNA genes are also marked (black).
Figure 4.
Figure 4.
Summary of four novel miRNA clusters identified by two separate methods. Structures and sequence logos are shown for four novel miRNA clusters identified by either EST folding (A) or support vector machine (SVM) techniques (B). Sequence logos were generated from the multiple-sequence alignment of all small RNA sequences in the cluster. Folded structure (as predicted by RNAFold) includes positioning of the mature miRNA sequence (highlighted in red). The most abundant (highest count) sequence from each cluster was considered the most reliable representative mature miRNA and was used to search for EST (for those identified by SVM) and potential homologs in miRBase. The alignment of each of these sequences to either its best hit or hit(s) in miRBase is included.
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