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

Abstract

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...

Unconventional conservation reveals structure-function relationships in the synaptonemal complex

“…While Pristionchus pacificus is an emerging model organism for evolutionary and developmental biology, its SC is poorly characterized. One SC protein, Ppa-SYP-4, has been identified based on a limited sequence similarity to the C-terminus of C. elegans SYP-4 (42). Notably, Ppa-SYP-4’s coiled-coil is predicted to be only 31nm long, too short to span the 100nm SC as a head-to-head dimer, suggesting that we have yet to identify a transverse filament protein in P. pacificus .…”

“…We used each of these 68 candidates as queries in a BLAST search against the strand-specific transcriptome to identify a gene name that corresponds to the RNA-tomography data, and selected genes that were gonad enriched. We were left with eight candidates, including Ppa-SYP-4 (42).…”