Single-Molecule Sequencing Reveals the Chromosome-Scale Genomic Architecture of the Nematode Model Organism Pristionchus pacificus

Rödelsperger, Christian; Meyer, Jan M.; Prabh, Neel; Lanz, Christa; Bemm, Felix; Sommer, Ralf J.

doi:10.1016/j.celrep.2017.09.077

Cited by 81 publications

(155 citation statements)

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“…Finally, analyses of chromosome-scale assemblies allowed us to explore the distribution of genetic features throughout the genome and to speculate on the evolutionary events that have taken place to explain these distributions. For example, between species analyses have confirmed karyotype structures and/or revealed chromosomal rearrangements among rhabditine nematodes [65,66] , filarial nematodes [11] , and platyhelminths [67] . The V4…”

Section: Discussionmentioning

confidence: 99%

Extensive genomic and transcriptomic variation defines the chromosome-scale assembly ofHaemonchus contortus, a model gastrointestinal worm

Doyle

Tracey

Laing

et al. 2020

Preprint

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Background Haemonchus contortus is a globally distributed and economically important gastrointestinal pathogen of small ruminants, and has become the key nematode model for studying anthelmintic resistance and other parasite-specific traits among a wider group of parasites including major human pathogens. Two draft genome assemblies for H. contortus were reported in 2013, however, both were highly fragmented, incomplete, and differed from one another in important respects. While the introduction of long-read sequencing has significantly increased the rate of production and contiguity of de novo genome assemblies broadly, achieving high quality genome assemblies for small, genetically diverse, outcrossing eukaryotic organisms such as H. contortus remains a significant challenge. ResultsHere, we report using PacBio long read and OpGen and 10X Genomics long-molecule methods to generate a highly contiguous 283.4 Mbp chromosome-scale genome assembly including a resolved sex chromosome. We show a remarkable pattern of almost complete conservation of chromosome content (synteny) with Caenorhabditis elegans , but almost no conservation of gene order. Long-read transcriptome sequence data has allowed us to define coordinated transcriptional regulation throughout the life cycle of the parasite, and refine our understanding of cisand trans -splicing relative to that observed in C. elegans .Finally, we use this assembly to give a comprehensive picture of chromosome-wide genetic diversity both within a single isolate and globally. ConclusionsThe H. contortus MHco3(ISE).N1 genome assembly presented here represents the most contiguous and resolved nematode assembly outside of the Caenorhabditis genus to date, together with one of the highest-quality set of predicted gene features. These data provide a high-quality comparison for understanding the evolution and genomics of Caenorhabditis and other nematodes, and extends the experimental tractability of this model parasitic nematode in understanding pathogen biology, drug discovery and vaccine development, and important adaptive traits such as drug resistance.

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Section: Discussionmentioning

confidence: 99%

Extensive genomic and transcriptomic variation defines the chromosome-scale assembly ofHaemonchus contortus, a model gastrointestinal worm

Doyle

Tracey

Laing

et al. 2020

Preprint

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“…The genomes of C. elegans and P. pacificus are remarkably distinct. Detailed recent analysis using phylotranscriptomics, Illumina, and single molecule sequencing revealed striking differences in gene content and genome organization to more accurately date their divergence to ~100 million year ago Rodelsperger, 2018;Rodelsperger et al, 2017). In light of this divergence, the extent of similarities of nervous system patterning is remarkable.…”

Section: Discussionmentioning

confidence: 99%

“…pacificus Genome Assembly El_Paco (Rodelsperger et al, 2017) and C. elegans WS269. To confirm the assigned gene orthology, we looked for best reciprocal BLASTP hits between P. pacificus and C. elegans genomes, as well as 1-1 orthology in gene phylogeny trees.…”

Section: Scanning Electron Microscopymentioning

confidence: 99%

Evolution of neuronal anatomy and circuitry in two highly divergent nematode species

Hong

Riebesell

Bumbarger

et al. 2019

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The nematodes C. elegans and P. pacificus populate diverse habitats and display distinct patterns of behavior. To understand how their nervous systems have diverged, we undertook a detailed examination of the neuroanatomy of the chemosensory system of P. pacificus. Using independent features such as cell body position, axon projections and lipophilic dye uptake, we have assigned homologies between the amphid neurons, their first-layer interneurons, and several internal receptor neurons of P. pacificus and C. elegans. We found that neuronal number and soma position are highly conserved. However, the morphological elaborations of several amphid cilia are different between them, most notably in the absence of 'winged' cilia morphology in P. pacificus. We established a synaptic wiring diagram of amphid sensory neurons and amphid interneurons in P. pacificus and found striking patterns of conservation and divergence in connectivity relative to C. elegans, but very little changes in relative neighborhood of neuronal processes. Impact StatementThe substrate for evolutionary divergence does not lie in changes in neuronal cell number or targeting, but rather in sensory perception and synaptic partner choice within invariant, prepatterned neuronal processes.

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“…Probes for a central locus on chromosome IV and the left end of chromosome X were designed 507 based on two short tandem repeat motifs. Tandem Repeat Finder v4.09 (Benson, 1999) was used to 508 21 identify tandem repeats in P. pacificus "El Paco" genome assembly (Rödelsperger et al, 2017) using 509 default parameters and a maximum periodicity of 200 bp. The output was then filtered to identify repeats 510 that spanned more than 8 kb.…”

Section: Fish Probes 506mentioning

confidence: 99%

“…Libraries were pooled and sequenced on a HiSeq4000 (150bp, PE, QB3 Vincent J. Coates 561 Genomics Sequencing Laboratory). Reads were mapped to the "El Paco" genome assembly including 562 annotated splice sites(Rödelsperger et al, 2017) using STAR. To correct misannotated splice sites, a 563 transcriptome was then reconstructed de novo using StringTie.…”

mentioning

confidence: 99%

Analysis of meiosis in Pristionchus pacificus reveals plasticity in homolog pairing and synapsis in the nematode lineage

Rillo-Bohn¹,

Adilardi²,

Avşaroğlu³

et al. 2019

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1The goal of meiosis is to produce haploid gametes from diploid progenitor cells. While meiosis was likely 2 present in the last eukaryotic common ancestor (LECA), diversity in meiotic mechanisms has long been 3 observed among sexually reproducing eukaryotes. Here we describe a new, comparative model system for 4 molecular analysis of meiosis, the nematode Pristionchus pacificus, a distant relative of the widely 5 studied model organism Caenorhabditis elegans. Despite superficial similarities in germline organization 6 and meiotic progression between P. pacificus and C. elegans, we identify fundamental differences in the 7 molecular mechanisms underlying homolog pairing, synapsis, and crossover regulation. Whereas C. 8 elegans has lost the meiosis-specific recombinase Dmc1, P. pacificus expresses both DMC-1 and RAD-9 51, which localize sequentially to meiotic chromosomes during prophase. We find that Ppa-spo-11 and 10Ppa-dmc-1 are required for stable homolog pairing, synapsis, and crossover formation, while Ppa-rad-51 11 is dispensable for these key processes during early prophase and plays a supporting role in meiotic 12 double-strand break repair. Additionally, we show that elevated crossover recombination in P. pacificus 13 likely arises through a Class II pathway normally inactive in C. elegans, shedding light on crossover 14 control and the evolution of recombination rates. 15 16 17 model Mus musculus (Bishop et al., 1992;Couteau et al., 1999;Grelon, 2001;Pittman et al., 1998; 43 Rockmill et al., 1995;Yoshida et al., 1998). 44In contrast, recombination-independent mechanisms of pairing and synapsis have been 45 characterized in other prominent model systems, including the dipteran Drosophila melanogaster and the 46 nematode Caenorhabditis elegans. While recombination is essential for successful execution of meiosis 47 elegans, P. pacificus is an androdioecious species, characterized by a population of mostly self-fertilizing 61 hermaphrodites (XX) and a low frequency of males (XO) (Sommer et al., 1996). Like C. elegans, P. 62 pacificus has a short life cycle of 3.5 days, produces large broods of about 200 progeny by self-63 fertilization, and is easily cultured in the lab (Hong and Sommer, 2006). Although C. elegans and P. 64 pacificus diverged an estimated 200-300 million years ago (Pires-daSilva, 2004), they share the same 65 number of chromosomes (2n=12) and, with the exception of one major chromosomal translocation, 66 macrosynteny is maintained between the two species (Dieterich et al., 2008; Rödelsperger et al., 2017). P. 67 pacificus has been established as a model for comparative studies in development, evolution and ecology 68 4 (Sommer, 2015). Recent improvements in the genome assembly (Rödelsperger et al., 2017) and advances 69 in genome editing (Lo et al., 2013; Namai and Sugimoto, 2018; Witte et al., 2015) have facilitated 70 investigation of cell biological processes at a more mechanistic level. 71 In addition to these general features that make P. pacificus a tractable model system, previou...

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Single-Molecule Sequencing Reveals the Chromosome-Scale Genomic Architecture of the Nematode Model Organism Pristionchus pacificus

Cited by 81 publications

References 63 publications

Extensive genomic and transcriptomic variation defines the chromosome-scale assembly ofHaemonchus contortus, a model gastrointestinal worm

Extensive genomic and transcriptomic variation defines the chromosome-scale assembly ofHaemonchus contortus, a model gastrointestinal worm

Evolution of neuronal anatomy and circuitry in two highly divergent nematode species

Analysis of meiosis in Pristionchus pacificus reveals plasticity in homolog pairing and synapsis in the nematode lineage

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