Evolution of the Caenorhabditis elegans Genome

Cutter, Asher D.; Dey, Alivia; Murray, Rosalind L.

doi:10.1093/molbev/msp048

Cited by 111 publications

(135 citation statements)

References 371 publications

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“…Each of the four species is morphologically similar; however, their genomic sequences are highly divergent, with common ancestry ;110 million generations ago ( Fig. 1B; Cutter et al 2009). We constructed 18-to 28-nt small RNA libraries from synchronized populations of young gravid adult hermaphrodites for the androdioecious (male/hermaphrodite) species C. elegans and C. briggsae and from mixed populations of adult males and females for the gonochoristic (male/female) species C. remanei and C. brenneri.…”

Section: Resultsmentioning

confidence: 99%

High-throughput sequencing reveals extraordinary fluidity of miRNA, piRNA, and siRNA pathways in nematodes

Shi

Montgomery

et al. 2013

Genome Res.

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The nematode Caenorhabditis elegans contains each of the broad classes of eukaryotic small RNAs, including microRNAs (miRNAs), endogenous small-interfering RNAs (endo-siRNAs), and piwi-interacting RNAs (piRNAs). To better understand the evolution of these regulatory RNAs, we deep-sequenced small RNAs from C. elegans and three closely related nematodes: C. briggsae, C. remanei, and C. brenneri. The results reveal a fluid landscape of small RNA pathways with essentially no conservation of individual sequences aside from a subset of miRNAs. We identified 54 miRNA families that are conserved in each of the four species, as well as numerous miRNAs that are species-specific or shared between only two or three species. Despite a lack of conservation of individual piRNAs and siRNAs, many of the features of each pathway are conserved between the different species. We show that the genomic distribution of 26G siRNAs and the tendency for piRNAs to cluster is conserved between C. briggsae and C. elegans. We also show that, in each species, 26G siRNAs trigger stage-specific secondary siRNA formation. piRNAs in each species also trigger secondary siRNA formation from targets containing up to three mismatches. Finally, we show that the production of male-and female-specific piRNAs is conserved in all four species, suggesting distinct roles for piRNAs in male and female germlines.

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Section: Resultsmentioning

confidence: 99%

High-throughput sequencing reveals extraordinary fluidity of miRNA, piRNA, and siRNA pathways in nematodes

Shi

Montgomery

et al. 2013

Genome Res.

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“…A clear expectation of the presence of internal promoters would be that genes downstream of internal promoters would have increased expression compared with the gene just upstream. However, expression of operon genes drops somewhat going from the 59 to the 39 end of the cluster (Cutter et al 2009). This could be due to inefficient processing of the polycistronic precursor or failure of transcription.…”

Section: Sl Percentage and Internal Operon Promotersmentioning

confidence: 99%

A global analysis of C. elegans trans-splicing

Allen¹,

Hillier²,

Waterston³

et al. 2010

Genome Res.

158

256

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Trans-splicing of one of two short leader RNAs, SL1 or SL2, occurs at the 59 ends of pre-mRNAs of many C. elegans genes. We have exploited RNA-sequencing data from the modENCODE project to analyze the transcriptome of C. elegans for patterns of trans-splicing. Transcripts of~70% of genes are trans-spliced, similar to earlier estimates based on analysis of far fewer genes. The mRNAs of most trans-spliced genes are spliced to either SL1 or SL2, but most genes are not transspliced to both, indicating that SL1 and SL2 trans-splicing use different underlying mechanisms. SL2 trans-splicing occurs in order to separate the products of genes in operons genome wide. Shorter intercistronic distance is associated with greater use of SL2. Finally, increased use of SL1 trans-splicing to downstream operon genes can indicate the presence of an extra promoter in the intercistronic region, creating what has been termed a ''hybrid'' operon. Within hybrid operons the presence of the two promoters results in the use of the two SL classes: Transcription that originates at the promoter upstream of another gene creates a polycistronic pre-mRNA that receives SL2, whereas transcription that originates at the internal promoter creates transcripts that receive SL1. Overall, our data demonstrate that >17% of all C. elegans genes are in operons.[Supplemental material is available for this article. The sequence data from this study have been submitted to the NCBI Sequence Read Archive (http://www.ncbi.nlm.nih.gov/Traces/sra/sra.cgi) under accession nos. SRA008646 and SRA003622.] C. elegans uses two RNA processing features that distinguish it from other model organisms. First, the transcripts of many genes are trans-spliced to a spliced leader (SL). Trans-splicing is a process in which an SL replaces the 59 end of a transcript by spliceosomal splicing. The 22-nucleotide (nt) SL is donated by an ;100-nt SL snRNP (small nuclear ribonucleoprotein) to a pre-mRNA with an intron-like region, the outron, containing an unpaired 39 splice site located near the 59 end. The second distinguishing feature is that many genes are transcribed in polycistronic units, known as operons, where a single promoter serves several genes. The operons can be up to eight genes long, and the polycistronic pre-mRNAs are separated into individual cistrons by 39 end formation accompanied by SL trans-splicing.These two features have important implications for C. elegans research. For instance, deletions/insertions within an operon may affect not only the expression of the gene containing the mutation, but also the genes downstream from it in the operon (Cui et al. 2008). Similarly, in a strain with enhanced RNAi sensitivity, RNAi of an operon gene can also affect expression of genes downstream (Guang et al. 2010). Finally, the trans-splice site is at the 59 end of the mRNA, not the pre-mRNA, and thus, the promoter is often not directly adjacent to the gene, but rather upstream of the outron or the entire operon (Blumenthal and Spieth 1996). SL trans-splicing has been repor...

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“…Several plant taxa, in particular, provide some of the most well-described population genetics systems that are composed of both selfing and outcrossing species in the same genus [e.g., Arabidopsis (Ross-Ibarra et al 2008), Capsella (St. Onge et al 2011), Eichornia (Ness et al 2010), Mimulus (Sweigart and Willis 2003), and Solanum (Arunyawat et al 2007)]. Animal population genetics models of such transitions are rare, with the notable exception of Caenorhabditis nematodes (Cutter et al 2009). But even in Caenorhabditis, multipopulation and global population genetic studies have been limited primarily to selfing species.…”

mentioning

confidence: 99%

Global Population Genetic Structure of Caenorhabditis remanei Reveals Incipient Speciation

Dey¹,

Jeon²,

Wang

et al. 2012

Genetics

111

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Mating system transitions dramatically alter the evolutionary trajectories of genomes that can be revealed by contrasts of species with disparate modes of reproduction. For such transitions in Caenorhabditis nematodes, some major causes of genome variation in selfing species have been discerned. And yet, we have only limited understanding of species-wide population genetic processes for their outcrossing relatives, which represent the reproductive state of the progenitors of selfing species. Multilocusmultipopulation sequence polymorphism data provide a powerful means to uncover the historical demography and evolutionary processes that shape genomes. Here we survey nucleotide polymorphism across the X chromosome for three populations of the outcrossing nematode Caenorhabditis remanei and demonstrate its divergence from a fourth population describing a closely related new species from China, C. sp. 23. We find high genetic variation globally and within each local population sample. Despite geographic barriers and moderate genetic differentiation between Europe and North America, considerable gene flow connects C. remanei populations. We discovered C. sp. 23 while investigating C. remanei, observing strong genetic differentiation characteristic of reproductive isolation that was confirmed by substantial F 2 hybrid breakdown in interspecific crosses. That C. sp. 23 represents a distinct biological species provides a cautionary example of how standard practice can fail for mating tests of species identity in this group. This species pair permits full application of divergence population genetic methods to obligately outcrossing species of Caenorhabditis and also presents a new focus for interrogation of the genetics and evolution of speciation with the Caenorhabditis model system.

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Evolution of the Caenorhabditis elegans Genome

Cited by 111 publications

References 371 publications

High-throughput sequencing reveals extraordinary fluidity of miRNA, piRNA, and siRNA pathways in nematodes

High-throughput sequencing reveals extraordinary fluidity of miRNA, piRNA, and siRNA pathways in nematodes

A global analysis of C. elegans trans-splicing

Global Population Genetic Structure of Caenorhabditis remanei Reveals Incipient Speciation

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