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Unidirectional evolutionary transitions in fungal mating systems and the role of transposable elements
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.
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2012 (English)In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 29, no 10, 3215-3226 p.Article in journal (Refereed) Published
Abstract [en]

In the fungal kingdom, the evolution of mating systems is highly dynamic, varying even among closely related species. Rearrangements in the mating-type (mat) locus, which contains the major regulators of sexual development, are expected to underlie the transitions between self-sterility (heterothallism) and self-fertility (homothallism). However, both the genetic mechanisms and the direction of evolutionary transitions in fungal mating systems are under debate. Here, we present new sequences of the mat locus of four homothallic and one heterothallic species of the model genus Neurospora (Ascomycota). By examining the patterns of synteny among these sequences and previously published data, we show that the locus is conserved among heterothallic species belonging to distinct phylogenetic clades, while different gene arrangements characterize the four homothallic species. These results allowed us to ascertain a heterothallic ancestor for the genus, confirming the prediction of the dead-end theory on unidirectional transitions toward selfing. We show that at least four shifts from heterothallism to homothallism have occurred in Neurospora, three of which involve the acquisition of sequences of both mating types into the same haploid genome. We present evidence for two genetic mechanisms allowing these shifts: translocation and unequal crossover. Finally, we identified two novel retrotransposons and suggest that these have played a major role in mating-system transitions, by facilitating multiple rearrangements of the mat locus.

Place, publisher, year, edition, pages
2012. Vol. 29, no 10, 3215-3226 p.
National Category
Natural Sciences
Identifiers
URN: urn:nbn:se:uu:diva-167869DOI: 10.1093/molbev/mss132ISI: 000309927900032OAI: oai:DiVA.org:uu-167869DiVA: diva2:488660
Available from: 2012-02-02 Created: 2012-02-02 Last updated: 2017-12-08Bibliographically approved
In thesis
1. On the Evolution of Reproductive Systems in Neurospora
Open this publication in new window or tab >>On the Evolution of Reproductive Systems in Neurospora
2012 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

The aim of this thesis was to study the evolution of reproductive systems and reproductive traits in the fungal genus Neurospora. More specifically, I have investigated the evolutionary forces shaping the genes involved in sexual reproduction, focusing on mating-type (mat) and pheromone receptor (pre) genes. Neurospora contains species exhibiting three different mating systems, i.e., heterothallism (self-incompatibility), homothallism (self-compatibility) and pseudohomothallism (partial self-incompatibility). First, a robust phylogeny of Neurospora was established. The phylogenetic analyses revealed multiple independent transitions in reproductive life style during the evolutionary history of the genus. We argued for a heterothallic ancestor of the genus, although our subsequent ancestral reconstruction analyses favored a homothallic ancestor. To be able to settle the ancestral mating system, we zoomed in on the structural architecture of the mat-locus in four homothallic species of Neurospora, thought to have arisen from independent transitions. Our results led us to suggest two different genetic mechanisms (translocation and unequal crossover) to explain the transitions in mating system from heterothallism to homothallism. We pointed out that the mating-system transitions in Neurospora are unidirectional, and suggested that transposable elements might be driving the transitions. In conclusion, we suggest a heterothallic ancestor for Neurospora, and that at least six transitions to homothallism and two transitions to pseudohomothallism have occurred in its evolutionary history. Further, we used the phylogeny of Neurospora as a framework to test if the evolution of pre-genes (pre-1 and pre-2) in hetero- and homothallic Neurospora is dependent on mating systems and/or even the homothallic clades themselves (i.e., mating-system and/or switch-dependent). The molecular evolution results suggest that pre-1 and pre-2 are overall functional in both homothallic and heterothallic Neurospora. The molecular evolution of pre-1 seems to be independent of mating-system or homothallic clade, and we detected signs for positive selection in the C-terminal tail. For pre-2 we found no support for mating-system dependent evolution, but indications for switch-dependent evolution. In this study we also included expression analyses of both pre- as well as mat-genes, with the prospect to assess functionality and regulation. During this thesis work, we also performed a phylogenetic study were we found that reproductive genes might be more permeable to introgression than other genes, which is in contrast to theoretical expectations. In the last study, we confirmed the co-existence of two alternative splice variants of the pheromone receptor gene pre-1 in Neurospora crassa, and performed expression profiles studies using quantitative RT-PCR. I hope this thesis work will further strengthen Neurospora as a model for research in evolutionary genetics.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2012. 41 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 895
Keyword
Neurospora, mating type, pheromone receptor, phylogeny, gene expression, heterothallism, homothallism, pseudohomothallism, alternative splicing
National Category
Natural Sciences
Research subject
Biology with specialization in Evolutionary Genetics
Identifiers
urn:nbn:se:uu:diva-167875 (URN)978-91-554-8265-7 (ISBN)
Public defence
2012-03-16, Lindahlsalen, EBC, Norbyvägen 14, Uppsala, 09:15 (English)
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Available from: 2012-02-24 Created: 2012-02-02 Last updated: 2012-03-01Bibliographically approved

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Gioti, AnastasiaJohannesson, Hanna

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