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Deciphering the relationship between mating system and pheromone receptor gene evolution in species of Neurospora
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: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 29, no 12, 3827-3842 p.Article in journal (Refereed) Published
Abstract [en]

Here, we present a study of the molecular evolution of the pheromone receptor genes (pre-1 and pre-2) in Neurospora taxa with different mating systems. We focus on comparisons between heterothallic and homothallic taxa, reproducing sexually by outcrossing and by intrahaploid selfing, respectively. Our general aim was to use a phylogenetic framework to investigate whether the evolutionary trajectory of the pheromone and receptor genes in Neurospora differs between heterothallic and homothallic taxa, and among the homothallic lineages/clades previously indicated to represent independent switches from heterothallism to homothallism in the evolutionary history of the genus. We complemented molecular evolution analyses with an expression study of the pre genes and their upstream regulators, the mating-type (mat) genes, in homothallic taxa. Our analyses suggest that the pheromone receptor gene pre-1 is functionally conserved in both heterothallic and homothallic taxa. Moreover, we found evidence of positive selection for a small fraction of codons in the cytoplasmic signal-transducing C-terminal region of the protein PRE-1. Distribution of positively selected codons differs between heterothallic and homothallic groups, suggesting functional divergence associated with mating system. The gene pre-2 was shown to evolve under high selective constraints, with no strong evidence for positive selection. Although our data suggest that both pre-1 and pre-2 are overall functional in homothallic taxa, individual taxa display frame-shift mutations causing premature stop codons, which might indicate loss of function. Transcriptional patterns of pre and mat genes in six homothallic taxa, selected to represent six different switches from heterothallism to homothallism, do not support a universal pattern of regulation of these genes during reproductive tissue development. Taken together, our analyses suggest that the pheromone receptor genes pre-1 and pre-2 are in general functional in homothallic Neurospora taxa, in contrast with the situation for the mat genes that are generally degenerate in these taxa.

Place, publisher, year, edition, pages
2012. Vol. 29, no 12, 3827-3842 p.
Keyword [en]
Neurospora, pheromones, receptors, homothallism
National Category
Natural Sciences
Identifiers
URN: urn:nbn:se:uu:diva-167871DOI: 10.1093/molbev/mss193ISI: 000310970000019OAI: oai:DiVA.org:uu-167871DiVA: diva2:488661
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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