A global multilocus analysis of the model fungus Neurospora reveals a single recent origin of a novel genetic system

Corcoran, Pádraic; Dettman, Jeremy R.; Sun, Yu; Luque, Eva M.; Corrochano, Luis M.; Taylor, John W.; Lascoux, Martin; Johannesson, Hanna

doi:10.1016/j.ympev.2014.05.007

Cited by 20 publications

(36 citation statements)

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“…Identification of orthologous genes and introns, and estimation of the intron gain and loss rates, in the Neurospora genomes We used the method outlined previously (Corcoran et al 2014) to detect orthologs between N. crassa and each of the other three well-annotated genomes. Our method to identify introns in these genes followed the basic principle of Nielsen et al (2004): The amino acid sequences for the orthologs were aligned by MAFFT (v 6.717b) with option LINSI (Katoh et al 2002).…”

Section: Methodsmentioning

confidence: 99%

“…a 59 positional biased intron distribution in the genome (Galagan et al 2003;Jeffares et al 2006). While most species forming the terminal clade in the genus are self-sterile (heterothallic) and thereby largely outcrossing (Ellison et al 2011a;Nygren et al 2011), one member of the genus, N. tetrasperma, has evolved pseudohomothallism, a mating system dependent on heterokaryosis for mating-type and intratetrad selfing (Dodge 1927;Corcoran et al 2014). Pseudohomothallism in N. tetrasperma is associated with a large region of suppressed recombination (;8 Mbp) on the matingtype chromosomes (Menkis et al 2008;Ellison et al 2011b;Sun et al 2012), while other regions are typically freely recombining.…”

Section: [Supplemental Materials Is Available For This Article]mentioning

confidence: 99%

“…Akashi and Schaeffer 1997;Przeworski et al 1999;Haddrill et al 2008) and refer to them herein as neutral SNPs. Furthermore, previous studies have shown that N. tetrasperma comprises multiple phylogenetically and reproductively isolated lineages (Menkis et al 2009;Corcoran et al 2014). Thus, we conducted separate frequency spectrum analyses for neutral SNPs, intron gains and intron losses polymorphic in each of three lineages represented with N > 10 in the resequenced N. tetrasperma samples (Supplemental Table S2): lineage 5, lineage 8, and lineage 10.…”

Section: Frequency Spectrum Of Derived Intron Gains and Lossesmentioning

confidence: 99%

“…See Supplemental Figure S3 for the frequency spectra of neutral SNPs in the R and SR regions of the genomes. For these three lineages, the mean Kst (Hudson et al 1992) over nine noncoding nuclear loci ranges from 0.10 to 0.37 (Corcoran et al 2014). When comparing the frequency distribution of SNPs and intron polymorphisms, we found that intron losses were significantly skewed toward high frequencies, as compared to neutral SNPs, in all three lineages (Wilcoxon-Mann-Whitney test, P < 0.01), while for gained introns, the frequencies were not skewed (P > 0.2) (Fig.…”

Section: Frequency Spectrum Of Derived Intron Gains and Lossesmentioning

confidence: 99%

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Intron evolution in Neurospora: the role of mutational bias and selection

et al. 2014

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We used comparative and population genomics to study intron evolutionary dynamics in the fungal model genus Neurospora. For our investigation, we used well-annotated genomes of N. crassa, N. discreta, and N. tetrasperma, and 92 resequenced genomes of N. tetrasperma from natural populations. By analyzing the four well-annotated genomes, we identified 9495 intron sites in 7619 orthologous genes. Our data supports nonhomologous end joining (NHEJ) and tandem duplication as mechanisms for intron gains in the genus and the RT-mRNA process as a mechanism for intron loss. We found a moderate intron gain rate (5.78-6.89 3 10 -13 intron gains per nucleotide site per year) and a high intron loss rate (7.53-13.76 3 10 -10 intron losses per intron sites per year) as compared to other eukaryotes. The derived intron gains and losses are skewed to high frequencies, relative to neutral SNPs, in natural populations of N. tetrasperma, suggesting that selection is involved in maintaining a high intron turnover. Furthermore, our analyses of the association between intron population-level frequency and genomic features suggest that selection is involved in shaping a 59 intron position bias and a low intron GC content. However, intron sequence analyses suggest that the gained introns were not exposed to recent selective sweeps. Taken together, this work contributes to our understanding of the importance of mutational bias and selection in shaping the intron distribution in eukaryotic genomes.

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Section: Methodsmentioning

confidence: 99%

Section: [Supplemental Materials Is Available For This Article]mentioning

confidence: 99%

Section: Frequency Spectrum Of Derived Intron Gains and Lossesmentioning

confidence: 99%

Section: Frequency Spectrum Of Derived Intron Gains and Lossesmentioning

confidence: 99%

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Intron evolution in Neurospora: the role of mutational bias and selection

et al. 2014

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“…Pseudohomothallism in N. tetrasperma is thought to have evolved from a heterothallic ancestor, for which sexual spores are of single mating type (Supplemental Fig. 1), about one million years ago (Corcoran et al 2014). To accomplish correct nuclear packaging in the spores of N. tetrasperma, crossing over is suppressed between the mat locus and the centromere, ensuring that mat A and mat a will segregate at the first division of meiosis.…”

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Introgression maintains the genetic integrity of the mating-type determining chromosome of the fungus Neurospora tetrasperma

et al. 2016

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Genome evolution is driven by a complex interplay of factors, including selection, recombination, and introgression. The regions determining sexual identity are particularly dynamic parts of eukaryotic genomes that are prone to molecular degeneration associated with suppressed recombination. In the fungus Neurospora tetrasperma, it has been proposed that this molecular degeneration is counteracted by the introgression of nondegenerated DNA from closely related species. In this study, we used comparative and population genomic analyses of 92 genomes from eight phylogenetically and reproductively isolated lineages of N. tetrasperma, and its three closest relatives, to investigate the factors shaping the evolutionary history of the genomes. We found that suppressed recombination extends across at least 6 Mbp (∼63%) of the mating-type (mat) chromosome in N. tetrasperma and is associated with decreased genetic diversity, which is likely the result primarily of selection at linked sites. Furthermore, analyses of molecular evolution revealed an increased mutational load in this region, relative to recombining regions. However, comparative genomic and phylogenetic analyses indicate that the mat chromosomes are temporarily regenerated via introgression from sister species; six of eight lineages show introgression into one of their mat chromosomes, with multiple Neurospora species acting as donors. The introgressed tracts have been fixed within lineages, suggesting that they confer an adaptive advantage in natural populations, and our analyses support the presence of selective sweeps in at least one lineage. Thus, these data strongly support the previously hypothesized role of introgression as a mechanism for the maintenance of mating-type determining chromosomal regions.

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Neurospora from Natural Populations: Population Genomics Insights into the Life History of a Model Microbial Eukaryote

Gladieux

Bellis

Hann‐Soden

et al. 2020

Methods in Molecular Biology

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The ascomycete filamentous fungus Neurospora crassa played a historic role in experimental biology and became a model system for genetic research. Stimulated by a systematic effort to collect wild strains initiated by Stanford geneticist David Perkins, the genus Neurospora has also become a basic model for the study of evolutionary processes, speciation, and population biology. In this chapter, we will first trace the history that brought Neurospora into the era of population genomics. We will then cover the major contributions of population genomic investigations using Neurospora to our understanding of microbial biogeography and speciation, and review recent work using population genomics and genome-wide association mapping that illustrates the unique potential of Neurospora as a model for identifying the genetic basis of (potentially adaptive) phenotypes in filamentous fungi. The advent of population genomics has contributed to firmly establish Neurospora as a complete model system and we hope our review will entice biologists to include Neurospora in their research.

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A global multilocus analysis of the model fungus Neurospora reveals a single recent origin of a novel genetic system

Cited by 20 publications

References 72 publications

Intron evolution in Neurospora: the role of mutational bias and selection

Intron evolution in Neurospora: the role of mutational bias and selection

Introgression maintains the genetic integrity of the mating-type determining chromosome of the fungus Neurospora tetrasperma

Neurospora from Natural Populations: Population Genomics Insights into the Life History of a Model Microbial Eukaryote

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