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Large-Scale Introgression Shapes the Evolution of the Mating-Type Chromosomes of the Filamentous Ascomycete Neurospora tetrasperma
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
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2012 (English)In: PLOS Genetics, ISSN 1553-7390, E-ISSN 1553-7404, Vol. 8, no 7, e1002820- p.Article in journal (Refereed) Published
Abstract [en]

The significance of introgression as an evolutionary force shaping natural populations is well established, especially in animal and plant systems. However, the abundance and size of introgression tracts, and to what degree interspecific gene flow is the result of adaptive processes, are largely unknown. In this study, we present medium coverage genomic data from species of the filamentous ascomycete Neurospora, and we use comparative genomics to investigate the introgression landscape at the genomic level in this model genus. We revealed one large introgression tract in each of the three investigated phylogenetic lineages of Neurospora tetrasperma (sizes of 5.6 Mbp, 5.2 Mbp, and 4.1 Mbp, respectively). The tract is located on the chromosome containing the locus conferring sexual identity, the mating-type (mat) chromosome. The region of introgression is confined to the region of suppressed recombination and is found on one of the two mat chromosomes (mat a). We used Bayesian concordance analyses to exclude incomplete lineage sorting as the cause for the observed pattern, and multilocus genealogies from additional species of Neurospora show that the introgression likely originates from two closely related, freely recombining, heterothallic species (N. hispaniola and N. crassa/N. perkinsii). Finally, we investigated patterns of molecular evolution of the mat chromosome in Neurospora, and we show that introgression is correlated with reduced level of molecular degeneration, consistent with a shorter time of recombination suppression. The chromosome specific (mat) and allele specific (mat a) introgression reported herein comprise the largest introgression tracts reported to date from natural populations. Furthermore, our data contradicts theoretical predictions that introgression should be less likely on sex-determining chromosomes. Taken together, the data presented herein advance our general understanding of introgression as a force shaping eukaryotic genomes.

Place, publisher, year, edition, pages
2012. Vol. 8, no 7, e1002820- p.
National Category
Biological Sciences
Identifiers
URN: urn:nbn:se:uu:diva-181143DOI: 10.1371/journal.pgen.1002820ISI: 000306840400034OAI: oai:DiVA.org:uu-181143DiVA: diva2:553171
Available from: 2012-09-18 Created: 2012-09-17 Last updated: 2017-12-07Bibliographically approved
In thesis
1. Genome Evolution of Neurospora tetrasperma
Open this publication in new window or tab >>Genome Evolution of Neurospora tetrasperma
2013 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

In this thesis work, I have used a comparative genomics approach to study a fungal model organism, Neurospora tetrasperma. My specific focus has been on genomic introgression, intron evolution, chromosomal structural rearrangements and codon usage. All of the studies are based on large-scale dataset generated by next-generation sequencing technology (NGS), combined with other techniques, such as Optical Mapping. In the introgression study, we detected large-scale introgression tracts in three N. tetrasperma lineages, and the introgression showed allele-specific and chromosomal-specific pattern. In the study of introns, we found indications of mRNA mediated intron loss and non-homologous end joining (NHEJ) mediated intron gains in N. tetrasperma. We found that selection is involved in shaping intron gains and losses, and associated with intron position, intron phase and GC content. In the study of chromosomal structural rearrangements, we found a lineage specific chromosomal inversion pattern in N. tetrasperma, which indicates that inversions are unlikely to associate with the origin of the suppressed recombination and the mating system transition in N. tetrasperma. The result suggests inversions are the consequences, rather than the causes, of suppressed recombination on the mating-type chromosome of N. tetrasperma. In the final study, analyses of codon usage indicated that the region of suppressed recombination in N. tetrasperma is subjected to genomic degeneration, and selection efficiency has been much reduced in this region.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2013. 32 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1075
Keyword
Neurospora tetrasperma, next-generation sequencing, introgression, intron, chromosomal inversion, codon usage
National Category
Evolutionary Biology Genetics
Research subject
Biology with specialization in Evolutionary Genetics
Identifiers
urn:nbn:se:uu:diva-207330 (URN)978-91-554-8753-9 (ISBN)
Public defence
2013-10-28, Zootissalen EBC, Norbyvägen 14, Uppsala, 09:00 (English)
Opponent
Supervisors
Available from: 2013-10-07 Created: 2013-09-12 Last updated: 2014-01-23
2. Neurospora tetrasperma from Natural Populations: Toward the Population Genomics of a Model Fungus
Open this publication in new window or tab >>Neurospora tetrasperma from Natural Populations: Toward the Population Genomics of a Model Fungus
2013 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

The study of DNA sequence variation is a powerful approach to study genome evolution, and to reconstruct evolutionary histories of species. In this thesis, I have studied genetic variation in the fungus Neurospora tetrasperma and other closely related Neurospora species. I have focused on N. tetrasperma in my research because it has large regions of suppressed recombination on its mating-type chromosomes, had undergone a recent change in reproductive mode and is composed of multiple reproductively isolated lineages. Using DNA sequence data from a large sample set representing multiple species of Neurospora I estimated that N. tetrasperma evolved ~1 million years ago and that it is composed of at least 10 lineages. My analysis of the type of asexual spores produced using newly described N. tetrasperma populations in Britain revealed that lineages differ considerably in life history characteristics that may have consequences for their evolution. A comparative genomic analysis using three genomes of N. tetrasperma and the genome of N. crassa revealed that the mat a chromosomes in the lineages examine have been introgressed from other Neurospora species and that this introgression has reduced levels of molecular degeneration on the mating-type chromosomes. Finally, I generated a population genomic dataset composed of 92 N. tetrasperma genomes and two genomes of other Neurospora species. Analysis of these genomes revealed that all strains of N. tetrasperma have large regions of suppressed recombination on their mating-type chromosomes ranging from 69-84% of the chromosome and that the extent of divergence between mating-type chromosomes within lineages varies greatly (from 1.3 to 3.2%). I concluded that the source of this great divergence mating-type chromosome is large-scale introgression from other Neurospora species, and that these introgressed tracts have become fixed within N. tetrasperma lineages. I also discovered that genes within non-recombining introgressed regions of the mating-type chromosome have severely reduced levels of genetic variation as compared to the autosomes, and exhibit signatures of reduced molecular degeneration. My analysis of variation in coding regions revealed that positive selection on the introgressed regions has resulted in the removal of deleterious mutations and is responsible for the reductions in molecular degeneration observed.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2013. 52 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1084
Keyword
Neurospora, poulation genetics, genomes, introgression
National Category
Evolutionary Biology Genetics
Research subject
Evolutionary Genetics
Identifiers
urn:nbn:se:uu:diva-208791 (URN)978-91-554-8771-3 (ISBN)
Public defence
2013-11-22, Zootisalen, EBC, Uppsala, 09:00 (English)
Opponent
Supervisors
Available from: 2013-10-31 Created: 2013-10-07 Last updated: 2014-01-23

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Sun, YuCorcoran, PadraicWhittle, Carrie A.Andersson, Siv G. E.Johannesson, Hanna

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