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Genome Evolution of Neurospora tetrasperma
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
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 [en]
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: urn:nbn:se:uu:diva-207330ISBN: 978-91-554-8753-9 (print)OAI: oai:DiVA.org:uu-207330DiVA: diva2:647873
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
List of papers
1. Large-Scale Introgression Shapes the Evolution of the Mating-Type Chromosomes of the Filamentous Ascomycete Neurospora tetrasperma
Open this publication in new window or tab >>Large-Scale Introgression Shapes the Evolution of the Mating-Type Chromosomes of the Filamentous Ascomycete Neurospora tetrasperma
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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.

National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-181143 (URN)10.1371/journal.pgen.1002820 (DOI)000306840400034 ()
Available from: 2012-09-18 Created: 2012-09-17 Last updated: 2017-12-07Bibliographically approved
2. Intron Evolution in Neurospora: the role of mutational bias and selection
Open this publication in new window or tab >>Intron Evolution in Neurospora: the role of mutational bias and selection
2015 (English)In: Genome Research, ISSN 1088-9051, E-ISSN 1549-5469, Vol. 25, no 1, 100-110 p.Article in journal (Refereed) Published
Abstract [en]

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 (5.78-6.89x10(-13) intron gains per nucleotide site per year) and a high intron loss rate (7.53-13.76x10(-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 5' 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.

National Category
Evolutionary Biology Genetics
Research subject
Biology with specialization in Evolutionary Genetics
Identifiers
urn:nbn:se:uu:diva-207325 (URN)10.1101/gr.175653.114 (DOI)000347373200009 ()25342722 (PubMedID)
Available from: 2013-09-12 Created: 2013-09-12 Last updated: 2017-12-06Bibliographically approved
3. Lineage-specific chromosomal inversions in Neurospora tetrasperma
Open this publication in new window or tab >>Lineage-specific chromosomal inversions in Neurospora tetrasperma
Show others...
(English)Manuscript (preprint) (Other academic)
National Category
Evolutionary Biology Genetics
Research subject
Biology with specialization in Evolutionary Genetics
Identifiers
urn:nbn:se:uu:diva-207328 (URN)
Available from: 2013-09-12 Created: 2013-09-12 Last updated: 2014-01-23
4. Degeneration in Codon Usage within the Region of Suppressed Recombination in the Mating-Type Chromosomes of Neurospora tetrasperma
Open this publication in new window or tab >>Degeneration in Codon Usage within the Region of Suppressed Recombination in the Mating-Type Chromosomes of Neurospora tetrasperma
2011 (English)In: Eukaryotic Cell, ISSN 1535-9778, E-ISSN 1535-9786, Vol. 10, no 4, 594-603 p.Article in journal (Refereed) Published
Abstract [en]

The origin and early evolution of sex chromosomes are currently poorly understood. The Neurospora tetrasperma mating-type (mat) chromosomes have recently emerged as a model system for the study of early sex chromosome evolution, since they contain a young (< 6 million years ago [Mya]), large (> 6.6-Mb) region of suppressed recombination. Here we examined preferred-codon usage in 290 genes (121,831 codon positions) in order to test for early signs of genomic degeneration in N. tetrasperma mat chromosomes. We report several key findings about codon usage in the region of recombination suppression, including the following: (i) this region has been subjected to marked and largely independent degeneration among gene alleles; (ii) the level of degeneration is magnified over longer periods of recombination suppression; and (iii) both mat a and mat A chromosomes have been subjected to deterioration. The frequency of shifts from preferred codons to nonpreferred codons is greater for shorter genes than for longer genes, suggesting that short genes play an especially significant role in early sex chromosome evolution. Furthermore, we show that these degenerative changes in codon usage are best explained by altered selection efficiency in the recombinationally suppressed region. These findings demonstrate that the fungus N. tetrasperma provides an effective system for the study of degenerative genomic changes in young regions of recombination suppression in sex-regulating chromosomes.

National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-152908 (URN)10.1128/EC.00284-10 (DOI)000289408900015 ()21335530 (PubMedID)
Available from: 2011-05-03 Created: 2011-05-03 Last updated: 2017-12-11Bibliographically approved

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