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A comprehensive phylogeny of Neurospora reveals a link between reproductive mode and molecular evolution in fungi
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 Organismal Biology, Systematic Biology.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
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2011 (English)In: Molecular Phylogenetics and Evolution, ISSN 1055-7903, E-ISSN 1095-9513, Vol. 59, no 3, 649-663 p.Article in journal (Refereed) Published
Abstract [en]

The filamentous ascomycete genus Neurospora encompasses taxa with a wide range of reproductive modes. Sexual reproduction in this genus can be divided into three major modes; heterothallism (self-incompatibility), homothallism (self-compatibility) and pseudohomothallism (partial self-compatibility). In addition to the sexual pathway, most of the heterothallic taxa propagate with morphologically distinct, vegetative dissemination propagules (macroconidia), while this feature is undetected in the majority of the homothallic taxa. In this study, we used sequence information of seven nuclear gene loci from 43 taxa (295 of the possible 301 locus-by-taxon combinations) to create a phylogeny of Neurospora. The results suggest that transitions in reproductive mode have occurred at multiple times within this group of fungi. Although a homothallic ancestor would imply fewer switches in reproductive mode, we argue that the ancestor of Neurospora was likely heterothallic and that homothallism has evolved independently at least six times in the evolutionary history of the genus. Furthermore, the two pseudohomothallic taxa of Neurospora (N. tetrasperma and N. tetraspora) represent two independent origins of pseudohomothallism. Likelihood ratio tests of substitution rates among branches in the phylogeny indicate that reproductive mode is an important factor driving genome evolution in Neurospora. First, an increased level of non-synonymous/synonymous substitutions in branches delineating homothallic taxa was found, suggesting a reduced efficiency of purifying selection in these taxa. Furthermore, elevated nucleotide substitution rates were found in heterothallic, conidia-producing, lineages as compared to the homothallic non-conidiating lineages. The latter finding is likely due to the presence of conidia, i.e., a higher rate of mitotic divisions inducing mutations, and/or that the homothallic taxa have evolved a lower mutation rate to avoid genomic degeneration.

Place, publisher, year, edition, pages
2011. Vol. 59, no 3, 649-663 p.
Keyword [en]
Outcrossing, Selfing, Conidia, Mutation rate, dN/dS, Ancestral character state, Dead end theory
National Category
Biological Systematics
Research subject
Biology with specialization in Evolutionary Genetics
Identifiers
URN: urn:nbn:se:uu:diva-152948DOI: 10.1016/j.ympev.2011.03.023ISI: 000290609000010PubMedID: 21439389OAI: oai:DiVA.org:uu-152948DiVA: diva2:414569
Available from: 2011-05-03 Created: 2011-05-03 Last updated: 2017-12-11Bibliographically approved
In thesis
1. Evolutionary Consequences of Reproductive Strategies: Testing Theory on Sex and Reproductive Gene Evolution in the Fungal Model Neurospora
Open this publication in new window or tab >>Evolutionary Consequences of Reproductive Strategies: Testing Theory on Sex and Reproductive Gene Evolution in the Fungal Model Neurospora
2011 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

In this thesis, I used the filamentous ascomycete genus Neurospora as a model to test theoretical predictions on the evolutionary consequences of different reproductive strategies and reproductive gene evolution. The genus Neurospora contains taxa representing a diversity of reproductive strategies, and here I constructed a phylogeny by which I was able to show that several independent transitions in reproductive mode have occurred in the evolutionary history of the genus. This feature makes Neurospora a suitable model for the evolution of reproductive modes. Molecular evolutionary analysis of housekeeping genes revealed an accelerated protein evolution in the highly inbreeding homothallic taxa, in accordance with theory predictions of lower efficiency of selection in asexual and highly inbreeding taxa. Furthermore, self-sterile (heterothallic) taxa capable of asexual propagation was found to be associated with a three-fold higher neutral substitution rate, indicative of a higher mutation accumulation due to elevated number of cell divisions per unit time in these taxa.

Further, I have shown a general pattern of rapid evolution of genes involved in reproduction in Neurospora, thus extending the pattern of general high divergence of reproductive genes previously well known in animals, to fungi. Two rapidly evolving reproductive genes: the pheromone receptor genes pre-1 and pre-2 involved in mate recognition were studied in detail. For the gene pre-1 the rapid divergence was found to be driven by positive selection in both heterothallic and homothallic taxa. The rapid divergence of the pheromone receptor gene pre-2 cannot be explained by positive selection and for this gene a subtle differences in evolutionary constraints between heterothallic and homothallic taxa were found. The general similarity in evolutionary constraints of pre-genes in taxa of both mating-systems indicates that these genes serve other functions beside mate recognition.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2011. 45 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 839
National Category
Biological Sciences
Research subject
Biology with specialization in Evolutionary Genetics
Identifiers
urn:nbn:se:uu:diva-152953 (URN)978-91-554-8102-5 (ISBN)
Public defence
2011-06-10, Zootissalen, Evolutionsmuseet (Museum of Evolution), Villavägen 9, Uppsala, 10:00 (English)
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Available from: 2011-05-19 Created: 2011-05-03 Last updated: 2011-07-01Bibliographically approved

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Johannesson, Hanna

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