Crossing-Over in a Hypervariable Species Preferentially Occurs in Regions of High Local Similarity

Abstract

Recombination between double-stranded DNA molecules is a key genetic process which occurs in a wide variety of organisms. Usually, crossing-over (CO) occurs during meiosis between genotypes with 98.0–99.9% sequence identity, because within-population nucleotide diversity only rarely exceeds 2%. However, some species are hypervariable and it is unclear how CO can occur between genotypes with less than 90% sequence identity. Here, we study CO in Schizophyllum commune, a hypervariable cosmopolitan basidiomycete mushroom, a frequently encountered decayer of woody substrates. We crossed two haploid individuals, from the United States and from Russia, and obtained genome sequences for their 17 offspring. The average genetic distance between the parents was 14%, making it possible to study CO at very high resolution. We found reduced levels of linkage disequilibrium between loci flanking the CO sites indicating that they are mostly confined to hotspots of recombination. Furthermore, CO events preferentially occurred in regions under stronger negative selection, in particular within exons that showed reduced levels of nucleotide diversity. Apparently, in hypervariable species CO must avoid regions of higher divergence between the recombining genomes due to limitations imposed by the mismatch repair system, with regions under strong negative selection providing the opportunity for recombination. These patterns are opposite to those observed in a number of less variable species indicating that population genomics of hypervariable species may reveal novel biological phenomena.

Variants in RNA-Seq data show a continued mutation rate during strain preservation ofSchizophyllum commune

“…Based on the mutation pattern near the mating loci, we expect a high chromosomal recombination frequency for S. commune. Previously it has been shown that S. commune performs crossover at regions of high homology (Seplyarskiy et al, 2014), and we see that S. commune also recombined very closely to mating type regions. A. bisporus (for which S. commune serves as a model for mushroom formation) performs crossover only near the telomeric regions (Sonnenberg et al, 2016).…”

“…The H4-8b strain was achieved through 9 backcrosses between H4-8a and 4.40, selecting in each stage for a crossing that had a compatible mating type to H4-8a. During meiosis, the chromosomes are exchanged and (often) undergo crossover at locations of genetic similarity (Seplyarskiy et al, 2014). The exact efficiency of this backcrossing procedure in terms of homozygosity, especially in the chromosomes containing the mating type loci is unknown.…”

A Resequencing-Based Ultradense Genetic Map of Hericium erinaceus for Anchoring Genome Sequences and Identifying Genetic Loci Associated With Monokaryon Growth

“…Despite the increase in the number of edible mushrooms that have been sequenced or resequenced (Grigoriev et al, 2014), the application of genotyping-by-sequencing in mushroom genetic studies is rare. High-throughput genotyping strategies have only recently been utilized in rapid genotyping of mushrooms (Au et al, 2013;Seplyarskiy et al, 2014;Gao et al, 2018). In H. erinaceus, no application of genotyping-bysequencing in genetic studies has been reported.…”

Mutation rate analysis via parent–progeny sequencing of the perennial peach. II. No evidence for recombination-associated mutation

“…If recombination is mutagenic, then we expect domains of high recombination to be domains of high rates of new mutations. The hypothesis has proven highly controversial, with indirect evidence both consistent [13–16] and inconsistent [17–20] with the hypothesis. The best indirect data, however, argue against the possibility.…”

“…Were recombination mutagenic, we might also predict that species with higher recombination rates should have a higher mutational input. However, higher divergence might in turn lead to reduced recombination rates [20] making prediction harder. There are numerous alternative suggested determinants of intragenomic variation in the mutation rate: for example, it correlates with local sequence context [26], including presence of insertion/deletions (indels) [27], replication timing [28], as well as possibly epigenetic effects such as chromatin organization [29].…”