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On the Evolution of Reproductive Systems in Neurospora
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics.
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 [en]
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: urn:nbn:se:uu:diva-167875ISBN: 978-91-554-8265-7 (print)OAI: oai:DiVA.org:uu-167875DiVA: diva2:488663
Public defence
2012-03-16, Lindahlsalen, EBC, Norbyvägen 14, Uppsala, 09:15 (English)
Opponent
Supervisors
Available from: 2012-02-24 Created: 2012-02-02 Last updated: 2012-03-01Bibliographically approved
List of papers
1. A comprehensive phylogeny of Neurospora reveals a link between reproductive mode and molecular evolution in fungi
Open this publication in new window or tab >>A comprehensive phylogeny of Neurospora reveals a link between reproductive mode and molecular evolution in fungi
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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.

National Category
Natural Sciences
Identifiers
urn:nbn:se:uu:diva-167868 (URN)http://dx.doi.org/10.1016/j.ympev.2011.03.023 (DOI)
Available from: 2012-02-02 Created: 2012-02-02 Last updated: 2017-12-08Bibliographically approved
2. Unidirectional evolutionary transitions in fungal mating systems and the role of transposable elements
Open this publication in new window or tab >>Unidirectional evolutionary transitions in fungal mating systems and the role of transposable elements
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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.

National Category
Natural Sciences
Identifiers
urn:nbn:se:uu:diva-167869 (URN)10.1093/molbev/mss132 (DOI)000309927900032 ()
Available from: 2012-02-02 Created: 2012-02-02 Last updated: 2017-12-08Bibliographically approved
3. Deciphering the relationship between mating system and pheromone receptor gene evolution in species of Neurospora
Open this publication in new window or tab >>Deciphering the relationship between mating system and pheromone receptor gene evolution in species of Neurospora
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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.

Keyword
Neurospora, pheromones, receptors, homothallism
National Category
Natural Sciences
Identifiers
urn:nbn:se:uu:diva-167871 (URN)10.1093/molbev/mss193 (DOI)000310970000019 ()
Available from: 2012-02-02 Created: 2012-02-02 Last updated: 2017-12-08Bibliographically approved
4. Conflict between reproductive gene trees and species phylogeny among heterothallic and pseudohomothallic members of the filamentous ascomycete genus Neurospora
Open this publication in new window or tab >>Conflict between reproductive gene trees and species phylogeny among heterothallic and pseudohomothallic members of the filamentous ascomycete genus Neurospora
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2010 (English)In: Fungal Genetics and Biology, ISSN 1087-1845, E-ISSN 1096-0937, Vol. 47, no 10, 869-878 p.Article in journal (Refereed) Published
Abstract [en]

In this study, we investigated the genealogies of genes important for sexual identity, i.e. mating-type (mat) and pheromone-receptor (pre) genes, among heterothallic and peudohomothallic taxa of Neurospora. The resulting genealogies were compared with the species phylogeny derived from non-coding sequences. We found conflicting topologies between the reproductive genealogies and the species phylogeny, and these conflicts were supported by both node support analyses and likelihood tests on the relative fit of datasets to alternative phylogenetic hypotheses. We argue that reproductive genes are more permeable to gene flow, i.e. are more often introgressed between species of Neurospora, than other parts of the genome. Certain conflicts between the species phylogeny and both mat genealogies were observed, suggesting that the two mating-type idiomorphs were selectively introgressed into a species from a single ancestral source. Taken together, the results presented here highlight complex evolutionary trajectories of reproductive genes in the fungal kingdom, which may be of importance for reproductive behavior in natural populations.

Keyword
Ascomycota, Evolution, Heterothallism, Mating type, Pheromone receptor, Pseudohomothallism
National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-167867 (URN)10.1016/j.fgb.2010.06.008 (DOI)000281999900009 ()20601044 (PubMedID)
Available from: 2012-02-02 Created: 2012-02-02 Last updated: 2017-12-08Bibliographically approved
5. Coexistence and expression profiles of two alternative splice variants of the pheromone receptor gene pre-1 in Neurospora crassa
Open this publication in new window or tab >>Coexistence and expression profiles of two alternative splice variants of the pheromone receptor gene pre-1 in Neurospora crassa
2013 (English)In: Archives of Microbiology, ISSN 0302-8933, E-ISSN 1432-072X, Vol. 195, no 10-11, 773-780 p.Article in journal (Refereed) Published
Abstract [en]

In this study, we show that two splice variants of the pheromone receptor gene (pre-1) transcript coexist in vegetative and reproductive tissues of the filamentous ascomycete fungus Neurospora crassa. The two splice variants differ by intron retention of the last intron, which is predicted to result in a premature stop codon and loss of 322 amino acids in the C-terminal cytosolic region of PRE-1. Using quantitative PCR, we show that expression of the variants is influenced by mating type (mat), with a higher proportion of intron-spliced transcripts in a mat A strain and a higher proportion of the intron-retained variant in a mat a strain. The intron-retained PRE-1 variant is predicted to lack 6 ubiquitination sites that may influence receptor function. In conclusion, N. crassa produce two pre-1 splice variants that display different transcription profiles.

Keyword
Alternative splicing, Gene expression, Neurospora, Pheromone receptor gene
National Category
Natural Sciences
Identifiers
urn:nbn:se:uu:diva-167872 (URN)10.1007/s00203-013-0923-5 (DOI)000325816300011 ()
Available from: 2012-02-02 Created: 2012-02-02 Last updated: 2017-12-08Bibliographically approved

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Citation style
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  • modern-language-association-8th-edition
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Output format
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