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  • 1.
    Anderson, Jennifer L
    et al.
    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.
    Nieuwenhuis, Bart P. S.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology. Division of Evolutionary Biology, Faculty of Biology, Ludwig- Maximilians-Universität München.
    Johannesson, Hanna
    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.
    Asexual reproduction and growth rate: independent and plastic lifehistory traits in Neurospora crassa2018In: The ISME Journal, ISSN 1751-7362, E-ISSN 1751-7370Article in journal (Refereed)
  • 2.
    Brännström, Ioana Onut
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
    Johannesson, Hanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
    Tibell, Leif
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
    Thamnolia tundrae sp nov., a cryptic species and putative glacial relict2018In: The Lichenologist, ISSN 0024-2829, E-ISSN 1096-1135, Vol. 50, no 1, p. 59-75Article in journal (Refereed)
    Abstract [en]

    The lichen species of the genus Thamnolia, with their striking wormlike thalli and frequent occurrence in arctic and tundra environments, have often been debated with regard to the use of chemistry in lichen taxonomy. Phylogenetic studies have arrived at different conclusions as to the recognition of species in the genus, but in a recent study based on the analyses of six nuclear markers (genes or noncoding regions) of a worldwide sample of Thamnolia, we showed the existence of three well-supported lineages with two different chemistries and geographical distributions. Here, we present two analyses based on ITS and three markers, respectively, which were extended from the study mentioned above to include type specimens and additional Thamnolia strains and taxa. In these analyses the same three clades were retrieved. A putative DEAD-box helicase is used here for the first time as an informative phylogenetic marker to provide taxonomic resolution at species level. The distribution of morphological and chemical characters across the phylogeny was analyzed and it was concluded that three morphologically cryptic, but genetically well supported, species occur: T. vermicularis s. str., T. subuliformis s. str. and T. tundrae sp. nov. Thamnolia vermicularis s. str. contains individuals with uniform secondary chemistry (producing thamnolic acid) and a rather limited distribution in the European Alps, Tatra Mts and the Western Carpathians, a distribution which might result from glacial survival in an adjacent refugium/refugia. Thamnolia subuliformis s. str. is widely distributed in all hemispheres and the samples contain two chemotypes (either with thamnolic or squamatic acids). Thamnolia tundrae is described as new; it produces baeomycesic and squamatic acids, and has a distribution limited to the arctic tundra of Eurasia extending to the Aleutian Islands in North America. It may have survived the latest glaciation in coastal refugia near its present distribution. Thus, secondary chemistry alone is not suitable for characterizing species in Thamnolia, secondary chemistry and geographical origin are informative, and the ITS region can be confidently used for species recognition. Nomenclatural notes are given on several other names that have been used in Thamnolia.

  • 3.
    Corcoran, Padraic
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology. Univ Sheffield, Dept Anim & Plant Sci, Sheffield S10 2TN, S Yorkshire, England.
    Anderson, Jennifer L
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
    Jacobson, David J
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology.
    Sun, Yu
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution.
    Ni, Peixiang
    BGI HongKong, Hong Kong, Hong Kong, Peoples R China.
    Lascoux, Martin
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Johannesson, Hanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
    Introgression maintains the genetic integrity of the mating-type determining chromosome of the fungus Neurospora tetrasperma.2016In: Genome Research, ISSN 1088-9051, E-ISSN 1549-5469, Vol. 26, no 4, p. 486-498Article in journal (Refereed)
    Abstract [en]

    Genome evolution is driven by a complex interplay of factors, including selection, recombination, and introgression. The regions determining sexual identity are particularly dynamic parts of eukaryotic genomes that are prone to molecular degeneration associated with suppressed recombination. In the fungus Neurospora tetrasperma, it has been proposed that this molecular degeneration is counteracted by the introgression of nondegenerated DNA from closely related species. In this study, we used comparative and population genomic analyses of 92 genomes from eight phylogenetically and reproductively isolated lineages of N. tetrasperma, and its three closest relatives, to investigate the factors shaping the evolutionary history of the genomes. We found that suppressed recombination extends across at least 6 Mbp (similar to 63%) of the mating-type (mat) chromosome in N. tetrasperma and is associated with decreased genetic diversity, which is likely the result primarily of selection at linked sites. Furthermore, analyses of molecular evolution revealed an increased mutational load in this region, relative to recombining regions. However, comparative genomic and phylogenetic analyses indicate that the mat chromosomes are temporarily regenerated via introgression from sister species; six of eight lineages show introgression into one of their mat chromosomes, with multiple Neurospora species acting as donors. The introgressed tracts have been fixed within lineages, suggesting that they confer an adaptive advantage in natural populations, and our analyses support the presence of selective sweeps in at least one lineage. Thus, these data strongly support the previously hypothesized role of introgression as a mechanism for the maintenance of mating-type determining chromosomal regions.

  • 4.
    Corcoran, Padraic
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Jacobson, David J.
    Bidartondo, Martin I.
    Hickey, Patrick C.
    Kerekes, Jennifer F.
    Taylor, John W.
    Johannesson, Hanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Quantifying functional heterothallism in the pseudohomothallic ascomycete Neurospora tetrasperma2012In: Fungal Biology, ISSN 1878-6146, E-ISSN 1878-6162, Vol. 116, no 9, p. 962-975Article in journal (Refereed)
    Abstract [en]

    Neurospora tetrasperma is a pseudohomothallic filamentous ascomycete that has evolved from heterothallic ancestors. Throughout its life cycle, it is predominantly heterokaryotic for mating type, and thereby self-fertile. However, studies of N. tetrasperma have revealed the occasional production of self-sterile asexual and sexual spores of a single-mating type, indicating that it can be functionally heterothallic. Here, we report the extensive sampling and isolation of natural, heterokaryotic, strains of N. tetrasperma from the United Kingdom (UK): 99 strains were collected from Surrey, England, and four from Edinburgh, Scotland. We verified by phylogenetic analyses that these strains belong to N. tetrasperma. We isolated cultures from single germinated asexual spores (conidia) from 17 of these newly sampled UK strains from Surrey, and 16 previously sampled strains of N. tetrasperma from New Zealand (NZ). Our results show that the N. tetrasperrna strains from the UK population produced a significantly greater proportion of self-sterile, homokaryotic conidia than the NZ population: the proportion of homokaryotic conidia was 42.6 % (133/312 spores) and 15.3 % (59/386) from the UK and the NZ populations, respectively. Although homokaryons recovered from several strains show a bias for one of the mating types, the total ratio of mat A to mat a mating type in homokaryons (UK: 72/61, NZ 28/31) did not deviate significantly from the expected 1:1 ratio for either of these populations. These results indicate that different populations exhibit differences in their life cycle characteristics, and that a higher degree of outcrossing might be expected from the UK population. This study points to the importance of studying multiple strains and populations when investigating life history traits of an organism with a complex life cycle, as previously undetected differences between populations may be revealed.

  • 5.
    Corcoran, Pádraic
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Dettman, Jeremy
    University of Ottawa.
    Sun, Yu
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Luque, Eva
    Universidad de Sevilla.
    Corrochano, Luis
    Universidad de Sevilla.
    Taylor, John
    University of California Berkeley.
    Lascoux, Martin
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Johannesson, Hanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    A global multilocus analysis of the model fungus Neurospora reveals a single recent origin of a novel genetic system2014In: Molecular Phylogenetics and Evolution, ISSN 1055-7903, E-ISSN 1095-9513, Vol. 78, p. 136-147Article in journal (Refereed)
    Abstract [en]

    The large diversity of mating systems observed in the fungal kingdom underlines the importance of mating system change in fungal evolution. The selfing species Neurospora tetrasperma has evolved a novel method of achieving self-fertility by a mating system referred to as pseudohomothallism. However, little is known about the origin of N. tetrasperma and its relationship to the self-sterile, heterothallic, Neurospora species. In this study, we used a combination of phylogenetic and population genetic analyses to reconstruct the evolutionary history of N. tetrasperma and its heterothallic relatives. We sequenced 9 unlinked nuclear loci from 106 strains of N. tetrasperma sampled from across the globe, and a sample of 28 heterothallic strains of Neurospora. Our analyses provide strong support for monophyly of N. tetrasperma, but reject the monophyly of N. crassa. We estimate that N. tetrasperma is of a recent origin and that it diverged from the heterothallic species ~1 million years ago. We also extend previous findings on the diversification within the N. tetrasperma clade, with 10 lineages identified. Taken together, these findings indicate that N. tetrasperma is younger than has been previously reported and that a rapid diversification of lineages has occurred within the N. tetrasperma clade.

  • 6.
    Gioti, Anastasia
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Mushegian, Alexandra A.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Strandberg, Rebecka
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics.
    Stajich, Jason E.
    Johannesson, Hanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Unidirectional evolutionary transitions in fungal mating systems and the role of transposable elements2012In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 29, no 10, p. 3215-3226Article in journal (Refereed)
    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.

  • 7.
    Gioti, Anastasia
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Stajich, Jason E.
    Johannesson, Hanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Neurospora and the dead-end hypothesis: genomic consequences of selfing in the model genus2013In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 67, no 12, p. 3600-3616Article in journal (Refereed)
    Abstract [en]

    It is becoming increasingly evident that adoption of different reproductive strategies, such as sexual selfing and asexuality, greatly impacts genome evolution. In this study, we test theoretical predictions on genomic maladaptation of selfing lineages using empirical data from the model fungus Neurospora. We sequenced the genomes of four species representing distinct transitions to selfing within the history of the genus, as well as the transcriptome of one of these, and compared with available data from three outcrossing species. Our results provide evidence for a relaxation of purifying selection in protein-coding genes and for a reduced efficiency of transposable element silencing by Repeat Induced Point mutation. A reduction in adaptive evolution was also identified in the form of reduced codon usage bias in highly expressed genes of selfing Neurospora, but this result may be confounded by mutational bias. Potentially counteracting these negative effects, the nucleotide substitution rate and the spread of transposons is reduced in selfing species. We suggest that differences in substitution rate relate to the absence, in selfing Neurospora, of the asexual pathway producing conidia. Our results support the dead-end theory and show that Neurospora genomes bear signatures of both sexual and asexual reproductive mode.

  • 8.
    Idnurm, Alexander
    et al.
    Univ Melbourne, Sch Biosci, Melbourne, Vic 3010, Australia..
    Hood, Michael E.
    Amherst Coll, Dept Biol, Amherst, MA 01002 USA..
    Johannesson, Hanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
    Giraud, Tatiana
    Univ Paris 11, Lab Ecol Systemat & Evolut, UMR 8079, F-91405 Orsay, France.;CNRS, F-91405 Orsay, France..
    Contrasted patterns in mating-type chromosomes in fungi: Hotspots versus coldspots of recombination2015In: Mycologist, ISSN 1749-4613, E-ISSN 1878-0253, Vol. 29, no 3-4, p. 220-229Article, review/survey (Refereed)
    Abstract [en]

    It is striking that, while central to sexual reproduction, the genomic regions determining sex or mating-types are often characterized by suppressed recombination that leads to a decrease in the efficiency of selection, shelters genetic load, and inevitably contributes to their genic degeneration. Research on model and lesser-explored fungi has revealed similarities in recombination suppression of the genomic regions involved in mating compatibility across eukaryotes, but fungi also provide opposite examples of enhanced recombination in the genomic regions that determine their mating types. These contrasted patterns of genetic recombination (sensu lato, including gene conversion and ectopic recombination) in regions of the genome involved in mating compatibility point to important yet complex processes occurring in their evolution. A number of pieces in this puzzle remain to be solved, in particular on the unclear selective forces that may cause the patterns of recombination, prompting theoretical developments and experimental studies. This review thus points to fungi as a fascinating group for studying the various evolutionary forces at play in the genomic regions involved in mating compatibility.

  • 9.
    James, Timothy Y.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Evolutionary Biology.
    Johansson, Stina B. K.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Evolutionary Biology.
    Johannesson, Hanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Evolutionary Biology.
    Trikaryon formation and nuclear selection in pairings between heterokaryons and homokaryons of the root rot pathogen Heterobasidion parviporum2009In: Mycological Research, ISSN 0953-7562, E-ISSN 1469-8102, Vol. 113, no 5, p. 583-590Article in journal (Refereed)
    Abstract [en]

    Pairings between heterokaryons and homokaryons of Agaricomycete fungi (he-ho pairings) can lead to either heterokaryotization of the homokaryon or displacement of the homokaryotic nucleus through migration of nuclei from the heterokaryon into the homokaryon. in species of Agaricomycetes with multinucleate cells (> 2 nuclei per cell), he-ho pairings could result in the stable or transient formation of a hypha with three genetically different nuclei (trikaryons). in this study, he-ho pairings were conducted using the multinucleate Agaricomycete Heterobasidion parviporum to determine whether trikaryons can be formed in the laboratory and whether nuclear genotype affects migration and heterokaryon formation. Nuclei were tracked by genotyping the heterokaryotic mycelium using nucleus-specific microsatellite markers. The data indicated that certain nuclear combinations were favored, and that nuclei from some strains had a higher rate of migration. A high percentage of trikaryons (19 %) displaying three microsatellite alleles per locus were identified among subcultures of the he-ho pairings. Using hyphal tip and conidial isolation, we verified that nuclei of three different mating types can inhabit the same mycelium, and one of the trikaryotic strains was judged to be semi-stable over multiple sub-culturing steps, with some hyphal tips that retained three alleles and others that reduced to two alleles per locus. These results demonstrate that nuclear competition and selection are possible outcomes of heterokaryon-homokaryon interactions in H. parviporum and confirm that ratios of component nuclei in heterokaryons are not strictly 1:1. The high rate of trikaryon formation in this study suggests that fungi with multinucleate cells may have the potential for greater genetic diversity and recombination relative to dikaryotic fungi.

  • 10.
    James, Timothy Y.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Evolutionary Biology.
    Olson, Åke
    Stenlid, Jan
    Johannesson, Hanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Evolutionary Biology.
    Evolutionary significance of imbalanced nuclear ratios within heterokaryons of the basidiomycete fungus Heterobasidion parviporum2008In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 62, no 9, p. 2279-2296Article in journal (Refereed)
    Abstract [en]

    Many fungi have heterokaryotic life stages in which genetically different nuclei inhabit the same cell. In basidiomycetes, the heterokaryon is the product of mating and represents a genomic union very similar to a diploid thallus, yet the maintenance of unfused nuclei suggests a more complex association of the two genomes relative to diploidy. In species with variable numbers of nuclei per heterokaryotic cell, nuclear ratios within a mycelium may possibly become imbalanced (differ from 1:1) due to nuclear competition. In this study, heterokaryons of the basidiomycete Heterobasidion parviporum were examined to determine the effects of genotype and environment on nuclear ratios within vegetative mycelia. The data reveal that nuclear ratios are frequently imbalanced, generally stable over time, and genetically determined. The nuclear ratios were affected by environment, but the observed nuclear ratios did not follow the expectations of strong selection acting on a population of nuclei. Instead, these ratios were largely driven by genetic effects and epigenetic effects. Finally, the data suggest that nuclear ratio imbalance also affects both gene transcription and growth rate, implying that heterokaryotic basidiomycetes are not functionally equivalent to diploid individuals and have a higher potential for genotypic and phenotypic variation.

  • 11.
    Johannesson, Hanna
    et al.
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Department of Evolution, Genomics and Systematics. Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Department of Evolution, Genomics and Systematics, Evolutionary Biology. Evolutionsbiologi.
    Townsend, Jeffrey P.
    Hung, Chiung-Yu
    Cole, Garry T.
    Taylor, John W
    Concerted evolution in the rpeats of an immunomodulating cell surface protein, SOWgp, of the human pathogenic fungi Coccidioides immitis and C. posadasii.2005In: GeneticsArticle in journal (Refereed)
    Abstract [en]

    Genome dynamics that allow pathogens to escape host immune responses are fundamental to our understanding of host-pathogen interactions. Here we present the first population-based study of the process of concerted evolution in the repetitive domain of a protein-coding gene. This gene, SOWgp, encodes the immunodominant protein in the parasitic phase of the human pathogenic fungi Coccidioides immitis and C. posadasii. We sequenced the entire gene from strains representing the geographic ranges of the two Coccidioides species. By using phylogenetic and genetic distance analyses we discovered that the repetitive part of SOWgp evolves by concerted evolution, predominantly by the mechanism of unequal crossing over. We implemented a mathematical model originally developed for multigene families to estimate the rate of homogenization and recombination of the repetitive array, and the results indicate that the pattern of concerted evolution is a result of homogenization of repeat units proceeding at a rate close to the nucleotide point mutation rate. The release of the SOWgp molecules by the pathogen during proliferation may mislead the host: we speculate that the pathogen benefits from concerted evolution of repeated domains in SOWgp by an enhanced ability to misdirect the host’s immune system.

  • 12.
    Johannesson, Henrik
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Evolutionary Biology.
    Kasuga, T
    Schaller, R A
    Good, B
    Gardner, M J
    Townsend, J P
    Cole, G T
    Taylor, J W
    Phase-specific gene expression underlying morphological adaptations of the dimorphic human pathogenic fungus, Coccidioides posadasii2006In: Fungal Genetics and Biology, ISSN 1087-1845, E-ISSN 1096-0937, Vol. 43, no 8, p. 545-559Article in journal (Refereed)
    Abstract [en]

    Coccidioides posadasii is a dimorphic fungal pathogen that grows as a Wlamentous saprobe in the soil and as endosporulating spheruleswithin the host. To identify genes speciWc to the pathogenic phase of Co. posadasii, we carried out a large-scale study of gene expression intwo isolates of the species. From the sequenced Co. posadasii genome, we chose 1000 open reading frames to construct a 70-mer microarray.RNA was recovered from both isolates at three life-cycle phases: hyphae, presegmented spherules, and spherules releasing endospores.Comparative hybridizations were conducted in a circuit design, permitting comparison between both isolates at all three life-cyclephases, and among all life-cycle phases for each isolate. By using this approach, we identiWed 92 genes that were diVerentially expressedbetween pathogenic and saprobic phases in both fungal isolates, and 43 genes with consistent diVerential expression between the two parasiticdevelopmental phases. Genes with elevated expression in the pathogenic phases of both isolates included a number of genes thatwere involved in the response to environmental stress as well as in the metabolism of lipids. The latter observation is in agreement withprevious studies demonstrating that spherules contain a higher proportion of lipids than saprobic phase tissue. Intriguingly, we discoveredstatistically signiWcant and divergent levels of gene expression between the two isolates proWled for 64 genes. The results suggest thatincorporating more than one isolate in the experimental design oVers a means of categorizing the large collection of candidate genes thattranscriptional proWling typically identiWes into those that are strain-speciWc and those that characterize the entire species.

  • 13.
    Karlsson, Magnus
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Evolutionary Biology.
    Nygren, Kristiina
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Evolutionary Biology.
    Johannesson, Hanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Evolutionary Biology.
    The evolution of the pheromonal signal system and its potential role for reproductive isolation in heterothallic neurospora2008In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 25, no 1, p. 168-178Article in journal (Refereed)
    Abstract [en]

    Comparative sequencing studies among a wide range of taxonomic groups, including fungi, provide the overall pattern that reproductive genes evolve more rapidly than other genes, and this divergence is believed to be important in the establishment of reproductive barriers between species. In this study, we investigated the molecular evolution of the pheromone receptor genes pre-1 and pre-2 of strains belonging to 12 and 13 heterothallic taxa, respectively, of the model genus Neurospora. Furthermore, we examined the regulatory pattern of both pheromone precursor and receptor genes during sexual crosses of Neurospora crassa and Neurospora intermedia, for which reinforcement of interspecific reproductive barriers in sympatry previously has been documented. We conclude that the part encoding the C-terminal intracellular domain of pre-1 and pre-2 genes evolves rapidly. Both stochastic and directional processes drive this divergence; both genes contain neutrally evolving codons, and in addition, pre-1 contains codons evolving under positive selection, whereas in pre-2 we found highly variable regions with numerous repeats encoding glycine, threonine, or aspartic acid. In addition, we found regulatory changes of the pheromone and receptor genes during crosses between N. crassa and N. intermedia with different reproductive success. Gene expression levels are higher in the interspecific sympatric crosses with low reproductive success than in their intraspecific and/or allopatric equivalents, both at the stage of initial communication and contact and later at postfertilization stages. Taken together, our data indicate that pheromones and receptors are important key players during reproductive isolation between Neurospora species, and this study provides a general framework for future studies on the role of reproductive proteins for reproductive isolation.

  • 14.
    Kronholm, Ilkka
    et al.
    Univ Jyvaskyla, Dept Biol & Environm Sci, Ctr Excellence Biol Interact, POB 35, FI-40014 Jyvaskyla, Finland..
    Johannesson, Hanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
    Ketola, Tarmo
    Univ Jyvaskyla, Dept Biol & Environm Sci, Ctr Excellence Biol Interact, POB 35, FI-40014 Jyvaskyla, Finland..
    Epigenetic Control of Phenotypic Plasticity in the Filamentous Fungus Neurospora crassa2016In: G3: Genes, Genomes, Genetics, ISSN 2160-1836, E-ISSN 2160-1836, Vol. 6, no 12, p. 4009-4022Article in journal (Refereed)
    Abstract [en]

    Phenotypic plasticity is the ability of a genotype to produce different phenotypes under different environmental or developmental conditions. Phenotypic plasticity is a ubiquitous feature of living organisms, and is typically based on variable patterns of gene expression. However, the mechanisms by which gene expression is influenced and regulated during plastic responses are poorly understood in most organisms. While modifications to DNA and histone proteins have been implicated as likely candidates for generating and regulating phenotypic plasticity, specific details of each modification and its mode of operation have remained largely unknown. In this study, we investigated how epigenetic mechanisms affect phenotypic plasticity in the filamentous fungus Neurospora crassa. By measuring reaction norms of strains that are deficient in one of several key physiological processes, we show that epigenetic mechanisms play a role in homeostasis and phenotypic plasticity of the fungus across a range of controlled environments. In general, effects on plasticity are specific to an environment and mechanism, indicating that epigenetic regulation is context dependent and is not governed by general plasticity genes. Specifically, we found that, in Neurospora, histone methylation at H3K36 affected plastic response to high temperatures, H3K4 methylation affected plastic response to pH, but H3K27 methylation had no effect. Similarly, DNA methylation had only a small effect in response to sucrose. Histone deacetylation mainly decreased reaction norm elevation, as did genes involved in histone demethylation and acetylation. In contrast, the RNA interference pathway was involved in plastic responses to multiple environments.

  • 15.
    Lindholm, Anna K.
    et al.
    Univ Zurich, Dept Evolutionary Biol & Environm Studies, Zurich, Switzerland..
    Dyer, Kelly A.
    Univ Georgia, Dept Genet, Athens, GA 30602 USA..
    Firman, Renee C.
    Univ Western Australia, Sch Anim Biol, Ctr Evolutionary Biol, Perth, WA 6009, Australia..
    Fishman, Lila
    Univ Montana, Div Biol Sci, Missoula, MT 59812 USA..
    Forstmeier, Wolfgang
    Max Planck Inst Ornithol, Dept Behav Ecol & Evolutionary Genet, D-82319 Seewiesen, Germany..
    Holman, Luke
    Australian Natl Univ, Res Sch Biol, Div Ecol Evolut & Genet, Canberra, ACT, Australia..
    Johannesson, Hanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
    Knief, Ulrich
    Max Planck Inst Ornithol, Dept Behav Ecol & Evolutionary Genet, D-82319 Seewiesen, Germany..
    Kokko, Hanna
    Univ Zurich, Dept Evolutionary Biol & Environm Studies, Zurich, Switzerland..
    Larracuente, Amanda M.
    Univ Rochester, Dept Biol, Rochester, NY 14627 USA..
    Manser, Andri
    Univ Zurich, Dept Evolutionary Biol & Environm Studies, Zurich, Switzerland..
    Montchamp-Moreau, Catherine
    Univ Paris Saclay, Univ Paris 11, CNRS, Evolut Genomes Comportement & Ecol,IRD, Gif Sur Yvette, France..
    Petrosyan, Varos G.
    Russian Acad Sci, Severtsov Inst Ecol & Evolut, Moscow 119071, Russia..
    Pomiankowski, Andrew
    UCL, Dept Genet Evolut & Environm, Gower St, London WC1E 6BT, England..
    Presgraves, Daven C.
    Univ Rochester, Dept Biol, Rochester, NY 14627 USA..
    Safronova, Larisa D.
    Russian Acad Sci, Severtsov Inst Ecol & Evolut, Moscow 119071, Russia..
    Sutter, Andreas
    Univ Zurich, Dept Evolutionary Biol & Environm Studies, Zurich, Switzerland..
    Unckless, Robert L.
    Cornell Univ, Dept Mol Biol & Genet, Ithaca, NY USA..
    Verspoor, Rudi L.
    Univ Liverpool, Inst Integrat Biol, Liverpool L69 7ZB, Merseyside, England..
    Wedell, Nina
    Univ Exeter, Biosci, Cornwall Campus, Penryn TR10 9FE, Cornwall, England..
    Wilkinson, Gerald S.
    Univ Maryland, Dept Biol, College Pk, MD 20742 USA..
    Price, Tom A. R.
    Univ Liverpool, Inst Integrat Biol, Liverpool L69 7ZB, Merseyside, England..
    The Ecology and Evolutionary Dynamics of Meiotic Drive2016In: Trends in Ecology & Evolution, ISSN 0169-5347, E-ISSN 1872-8383, Vol. 31, no 4, p. 315-326Article, review/survey (Refereed)
    Abstract [en]

    Meiotic drivers are genetic variants that selfishly manipulate the production of gametes to increase their own rate of transmission, often to the detriment of the rest of the genome and the individual that carries them. This genomic conflict potentially occurs whenever a diploid organism produces a haploid stage, and can have profound evolutionary impacts on gametogenesis, fertility, individual behaviour, mating system, population survival, and reproductive isolation. Multiple research teams are developing artificial drive systems for pest control, utilising the transmission advantage of drive to alter or exterminate target species. Here, we review current knowledge of how natural drive systems function, how drivers spread through natural populations, and the factors that limit their invasion.

  • 16. Lindner, Daniel L.
    et al.
    Vasaitis, Rimvydas
    Kubartova, Ariana
    Allmer, Johan
    Johannesson, Hanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Banik, Mark T.
    Stenlid, Jan
    Initial fungal colonizer affects mass loss and fungal community development in Picea abies logs 6 yr after inoculation2011In: Fungal ecology, ISSN 1754-5048, E-ISSN 1878-0083, Vol. 4, no 6, p. 449-460Article in journal (Refereed)
    Abstract [en]

    Picea abies logs were inoculated with Resinicium bicolor, Fomitopsis pinicola or left un-inoculated and placed in an old-growth boreal forest. Mass loss and fungal community data were collected after 6 yr to test whether simplification of the fungal community via inoculation affects mass loss and fungal community development. Three techniques were used to survey communities: (1) observation of fruiting structures; (2) culturing on media; and (3) cloning and sequencing of ITS rDNA. Fruit body surveys detected the smallest number of species (18, 3.8 per log), DNA-based methods detected the most species (72, 31.7 per log), and culturing detected an intermediate number (23, 7.2 per log). Initial colonizer affected community development and inoculation with F. pinicola led to significantly greater mass loss. Relationships among fungal community composition, community richness and mass loss are complex and further work is needed to determine whether simplification of fungal communities affects carbon sequestration in forests.

  • 17.
    Menkis, Audrius
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Evolutionary Biology.
    Bastiaans, E.
    Jacobson, J.
    Johannesson, Hanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Evolutionary Biology.
    Phylogenetic and biological species diversity within the Neurospora tetrasperma complex2009In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 22, no 9, p. 1923-1936Article in journal (Refereed)
    Abstract [en]

    The objective of this study was to explore the evolutionary history of the morphologically recognized filamentous ascomycete Neurospora tetrasperma, and to reveal the genetic and reproductive relationships among its individuals and populations. We applied both phylogenetic and biological species recognition to a collection of strains representing the geographic and genetic diversity of N. tetrasperma. First, we were able to confirm a monophyletic origin of N. tetrasperma. Furthermore, we found nine phylogenetic species within the morphospecies. When using the traditional broad biological species recognition all investigated strains of N. tetrasperma constituted a single biological species. In contrast, when using a quantitative measurement of the reproductive success, incorporating characters such as viability and fertility of offspring, we found a high congruence between the phylogenetic and biological species recognition. Taken together, phylogenetically and biologically defined groups of individuals exist in N. tetrasperma, and these should be taken into account in future studies of its life history traits.

  • 18. Menkis, Audrius
    et al.
    Burokiene, Daiva
    Gaitnieks, Talis
    Uotila, Antti
    Johannesson, Hanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Rosling, Anna
    Finlay, Roger D.
    Stenlid, Jan
    Vasaitis, Rimvydas
    Occurrence and impact of the root-rot biocontrol agent Phlebiopsis gigantea on soil fungal communities in Picea abies forests of northern Europe2012In: FEMS Microbiology Ecology, ISSN 0168-6496, E-ISSN 1574-6941, Vol. 81, no 2, p. 438-445Article in journal (Refereed)
    Abstract [en]

    The aim of this study was to assess belowground occurrence, persistence and possible impact of the biocontrol agent Phlebiopsis gigantea (Fr.) Julich on soil fungi. Sampling of soil and roots of Picea abies (L.) H. Karst. was carried out at 12 P.similar to gigantea-treated and five nontreated control sites representing 1- to 60-month-old clear-cuts and thinned forest sites in Finland and Latvia. The 454-sequencing of ITS rRNA from fine roots, humus and mineral soil resulted in 8626 high-quality fungal sequences. Phlebiopsis gigantea represented 1.3% of all fungal sequences and was found in 14 treated and nontreated sites and in all three substrates. In different substrates, the relative abundance of P.similar to gigantea at stump treatment sites either did not differ significantly or was significantly lower than in nontreated controls. No significant correlation was found between the time elapsed since the tree harvesting and/or application of the biocontrol and abundance of P.similar to gigantea in different substrates. In conclusion, the results demonstrate that P.similar to gigantea occasionally occurs belowground in forest ecosystems but that stump treatment with the biocontrol agent has little or no impact on occurrence and persistence of P.similar to gigantea belowground, and consequently no significant impact on soil fungi.

  • 19.
    Menkis, Audrius
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Evolutionary Biology.
    Jacobson, D.J.
    Gustafsson, Tim
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Evolutionary Biology.
    Johannesson, Hanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Evolutionary Biology.
    The mating-type chromosome in the filamentous ascomycete Neurospora tetrasperma represents a model for early evolution of sex chromosomes2008In: PLoS Genetics, ISSN 1553-7390, Vol. 4, no 3, p. e100030-Article in journal (Refereed)
    Abstract [en]

    We combined gene divergence data, classical genetics, and phylogenetics to study the evolution of the mating-type chromosome in the filamentous ascomycete Neurospora tetrasperma. In this species, a large non-recombining region of the mating-type chromosome is associated with a unique fungal life cycle where self-fertility is enforced by maintenance of a constant state of heterokaryosis. Sequence divergence between alleles of 35 genes from the two single mating-type component strains (i.e. the homokaryotic mat A or mat a-strains), derived from one N. tetrasperma heterokaryon ( mat A+mat a), was analyzed. By this approach we were able to identify the boundaries and size of the non- recombining region, and reveal insight into the history of recombination cessation. The non- recombining region covers almost 7 Mbp, over 75% of the chromosome, and we hypothesize that the evolution of the mating-type chromosome in this lineage involved two successive events. The first event was contemporaneous with the split of N. tetrasperma from a common ancestor with its outcrossing relative N. crassa and suppressed recombination over at least 6.6 Mbp, and the second was confined to a smaller region in which recombination ceased more recently. In spite of the early origin of the first "evolutionary stratum'', genealogies of five genes from strains belonging to an additional N. tetrasperma lineage indicate independent initiations of suppressed recombination in different phylogenetic lineages. This study highlights the shared features between the sex chromosomes found in the animal and plant kingdoms and the fungal mating-type chromosome, despite fungi having no separate sexes. As is often found in sex chromosomes of plants and animals, recombination suppression of the mating- type chromosome of N. tetrasperma involved more than one evolutionary event, covers the majority of the mating- type chromosome and is flanked by distal regions with obligate crossovers.

  • 20. Menkis, Audrius
    et al.
    Whittle, Carrie A.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Johannesson, Hanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Gene genealogies indicates abundant gene conversions and independent evolutionary histories of the mating-type chromosomes in the evolutionary history of Neurospora tetrasperma2010In: BMC Evolutionary Biology, ISSN 1471-2148, E-ISSN 1471-2148, Vol. 10, no 1, p. 234-Article in journal (Refereed)
    Abstract [en]

    Background: The self-fertile filamentous ascomycete Neurospora tetrasperma contains a large (similar to 7 Mbp) and young (< 6 MYA) region of suppressed recombination within its mating-type ( mat) chromosomes. The objective of the present study is to reveal the evolutionary history, including key genomic events, associated with the various regions of the mat chromosomes among ten strains representing all the nine known species ( lineages) contained within the N. tetrasperma species complex. Results: Comparative analysis of sequence divergence among alleles of 24 mat-linked genes ( mat A and mat a) indicates that a large region of suppressed recombination exists within the mat chromosome for each of nine lineages of N. tetrasperma sensu latu. The recombinationally suppressed region varies in size and gene composition among lineages, and is flanked on both ends by normally recombining regions. Genealogical analyses among lineages reveals that eight gene conversion events have occurred between homologous mat A and mat a-linked alleles of genes located within the region of restricted recombination during the evolutionary history of N. tetrasperma. Conclusions: We conclude that the region of suppressed recombination in the mat chromosomes has likely been subjected to independent contraction and/or expansion during the evolutionary history of the N. tetrasperma species complex. Furthermore, we infer that gene conversion events are likely a common phenomenon within this recombinationally suppressed genomic region. We argue that gene conversions might provide an efficient mechanism of adaptive editing of functional genes, including the removal of deleterious mutations, within the young recombinationally suppressed region of the mat chromosomes.

  • 21.
    Meunier, Cécile
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
    Hosseini, Sara
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
    Heidari, Nahid
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
    Maryush, Zaywa
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
    Johannesson, Hanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
    Multilevel Selection in the Filamentous Ascomycete Neurospora tetrasperma2018In: American Naturalist, ISSN 0003-0147, E-ISSN 1537-5323, Vol. 191, no 3, p. 290-305Article in journal (Refereed)
    Abstract [en]

    The history of life has been driven by evolutionary transitions in individuality, that is, the aggregation of autonomous individuals to form a new, higher-level individual. The fungus Neurospora tetrasperma has recently undergone an evolutionary transition in individuality from homokaryosis (one single type of nuclei in the same cytoplasm) to heterokaryosis (two genetically divergent and free-ranging nuclear types). In this species, selection can act at different levels: while nuclei can compete in their replication and transmission into short-lived asexual spores, at the level of the heterokaryotic individual, cooperation between nuclear types is required to produce the long-lived sexual spores. Conflicts can arise between these two levels of selection if the coevolution between nuclear types is disrupted. Here, we investigated the extent of multilevel selection in three strains of N. tetrasperma. We assessed the ratio between nuclear types under different conditions and measured fitness traits of homo- and heterokaryotic mycelia with varying nuclear ratios. We show that the two nuclei have complementary traits, consistent with division of labor and cooperation. In one strain, for which a recent chromosomal introgression was detected, we observed the occurrence of selfish nuclei, enjoying better replication and transmission than sister nuclei at the same time as being detrimental to the heterokaryon. We hypothesize that introgression has disrupted the coevolution between nuclear types in this strain.

  • 22.
    Nygren, Kristiina
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Strandberg, Rebecka
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Gioti, Anastasia
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Karlsson, Magnus
    Johannesson, Hanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Deciphering the relationship between mating system and pheromone receptor gene evolution in species of Neurospora2012In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 29, no 12, p. 3827-3842Article in journal (Refereed)
    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.

  • 23.
    Nygren, Kristiina
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Strandberg, Rebecka
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Wallberg, Andreas
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
    Nabholz, Benoit
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Gustafsson, Tim
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    García, Dania
    Unitat de Microbiologia, Facultat de Medicina i Ciències de la Salut, ISPV, Universitat Rovira i Virgili, 43201 Reus, Tarragona, Spain.
    Cano, José
    Unitat de Microbiologia, Facultat de Medicina i Ciències de la Salut, ISPV, Universitat Rovira i Virgili, 43201 Reus, Tarragona, Spain.
    Guarro, Josep
    Unitat de Microbiologia, Facultat de Medicina i Ciències de la Salut, ISPV, Universitat Rovira i Virgili, 43201 Reus, Tarragona, Spain.
    Johannesson, Hanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    A comprehensive phylogeny of Neurospora reveals a link between reproductive mode and molecular evolution in fungi2011In: Molecular Phylogenetics and Evolution, ISSN 1055-7903, E-ISSN 1095-9513, Vol. 59, no 3, p. 649-663Article in journal (Refereed)
    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.

  • 24.
    Nygren, Kristiina
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Wallberg, Andreas
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Biochemistry and Microbiology.
    Samils, Nicklas
    Stajich, Jason E.
    Townsend, Jeffrey P.
    Karlsson, Magnus
    Johannesson, Hanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Analyses of expressed sequence tags in Neurospora reveal rapid evolution of genes associated with the early stages of sexual reproduction in fungi2012In: BMC Evolutionary Biology, ISSN 1471-2148, E-ISSN 1471-2148, Vol. 12, p. 229-Article in journal (Refereed)
    Abstract [en]

    Background: The broadly accepted pattern of rapid evolution of reproductive genes is primarily based on studies of animal systems, although several examples of rapidly evolving genes involved in reproduction are found in diverse additional taxa. In fungi, genes involved in mate recognition have been found to evolve rapidly. However, the examples are too few to draw conclusions on a genome scale. Results: In this study, we performed microarray hybridizations between RNA from sexual and vegetative tissues of two strains of the heterothallic (self-sterile) filamentous ascomycete Neurospora intermedia, to identify a set of sex-associated genes in this species. We aligned Expressed Sequence Tags (ESTs) from sexual and vegetative tissue of N. intermedia to orthologs from three closely related species: N. crassa, N. discreta and N. tetrasperma. The resulting four-species alignments provided a dataset for molecular evolutionary analyses. Our results confirm a general pattern of rapid evolution of fungal sex-associated genes, compared to control genes with constitutive expression or a high relative expression during vegetative growth. Among the rapidly evolving sex-associated genes, we identified candidates that could be of importance for mating or fruiting-body development. Analyses of five of these candidate genes from additional species of heterothallic Neurospora revealed that three of them evolve under positive selection. Conclusions: Taken together, our study represents a novel finding of a genome-wide pattern of rapid evolution of sex-associated genes in the fungal kingdom, and provides a list of candidate genes important for reproductive isolation in Neurospora.

  • 25.
    Onuţ-Brännström, Ioana
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
    Benjamin, Mitchell
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
    Scofield, Douglas G.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Starri, Heiðmarsson
    Icelandic Institute of Natural History, Borgir Nordurslod, Iceland.
    Andersson, Martin G.I.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Limnology.
    Lindström, Eva S.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Limnology.
    Johannesson, Hanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
    Sharing of photobionts in sympatric populations of Thamnolia and Cetraria lichens: evidence from high-throughput sequencing2018In: Scientific Reports, ISSN 2045-2322, E-ISSN 2045-2322, Vol. 8, article id 4406Article in journal (Refereed)
    Abstract [en]

    In this study, we explored the diversity of green algal symbionts (photobionts) in sympatric populations of the cosmopolitan lichen-forming fungi Thamnolia and Cetraria. We sequenced with both Sanger and Ion Torrent High-Throughput Sequencing technologies the photobiont ITS-region of 30 lichen thalli from two islands: Iceland and Öland. While Sanger recovered just one photobiont genotype from each thallus, the Ion Torrent data recovered 10–18 OTUs for each pool of 5 lichen thalli, suggesting that individual lichens can contain heterogeneous photobiont populations. Both methods showed evidence for photobiont sharing between Thamnolia and Cetraria on Iceland. In contrast, our data suggest that on Öland the two mycobionts associate with distinct photobiont communities, with few shared OTUs revealed by Ion Torrent sequencing. Furthermore, by comparing our sequences with public data, we identified closely related photobionts from geographically distant localities. Taken together, we suggest that the photobiont composition in Thamnolia and Cetraria results from both photobiont-mycobiont codispersal and local acquisition during mycobiont establishment and/or lichen growth. We hypothesize that this is a successful strategy for lichens to be flexible in the use of the most adapted photobiont for the environment.

  • 26.
    Onuţ-Brännström, Ioana
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
    Tibell, Leif
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
    Johannesson, Hanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
    A worldwide phylogeography of the whiteworm lichens Thamnolia reveals three lineages with distinct habitats and evolutionary histories2017In: Ecology and Evolution, ISSN 2045-7758, E-ISSN 2045-7758, Vol. 7, no 10, p. 3602-3615Article in journal (Refereed)
    Abstract [en]

    Thamnolia is a lichenized fungus with an extremely wide distribution, being encountered in arctic and alpine environments in most continents. In this study, we used molecular markers to investigate the population structure of the fungal symbiont and the associated photosynthetic partner of Thamnolia. By analyzing molecular, morphological, and chemical variation among 253 specimens covering the species distribution range, we revealed the existence of three mycobiont lineages. One lineage (Lineage A) is confined to the tundra region of Siberia and the Aleutian Islands, a second (Lineage B) is found in the high alpine region of the Alps and the Carpathians Mountains, and a third (Lineage C) has a worldwide distribution and covers both the aforementioned ecosystems. Molecular dating analysis indicated that the split of the three lineages is older than the last glacial maximum, but the distribution ranges and the population genetic analyses suggest an influence of last glacial period on the present-day population structure of each lineage. We found a very low diversity of Lineage B, but a higher and similar one in Lineages A and C. Demographic analyses suggested that Lineage C has its origin in the Northern Hemisphere, possibly Scandinavia, and that it has passed through a bottleneck followed by a recent population expansion. While all three lineages reproduce clonally, recombination tests suggest rare or past recombination in both Lineages A and C. Moreover, our data showed that Lineage C has a comparatively low photobiont specificity, being found associated with four widespread Trebouxia lineages (three of them also shared with other lichens), while Lineages A and B exclusively harbor T. simplex s. lat. Finally, we did not find support for the recognition of taxa in Thamnolia based on either morphological or chemical characters.

  • 27.
    Pent, Mari
    et al.
    Univ Tartu, Inst Ecol & Earth Sci, Tartu, Estonia.
    Hiltunen, Markus
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
    Poldmaa, Kadri
    Univ Tartu, Inst Ecol & Earth Sci, Tartu, Estonia.
    Furneaux, Brendan R.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
    Hildebrand, Falk
    European Mol Biol Lab, Struct & Computat Biol, Heidelberg, Germany.
    Johannesson, Hanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
    Ryberg, Martin
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
    Bahram, Mohammad
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology. Univ Tartu, Inst Ecol & Earth Sci, Tartu, Estonia.
    Host genetic variation strongly influences the microbiome structure and function in fungal fruiting-bodies2018In: Environmental Microbiology, ISSN 1462-2912, E-ISSN 1462-2920, Vol. 20, no 5, p. 1641-1650Article in journal (Refereed)
    Abstract [en]

    Despite increasing knowledge on host-associated microbiomes, little is known about mechanisms underlying fungus-microbiome interactions. This study aimed to examine the relative importance of host genetic, geographic and environmental variations in structuring fungus-associated microbiomes. We analyzed the taxonomic composition and function of microbiomes inhabiting fungal fruiting-bodies in relation to host genetic variation, soil pH and geographic distance between samples. For this, we sequenced the metagenomes of 40 fruiting-bodies collected from six fairy rings (i.e., genets) of a sapro-trophic fungus Marasmius oreades. Our analyses revealed that fine genetic variations between host fungi could strongly affect their associated microbiome, explaining, respectively, 25% and 37% of the variation in microbiome structure and function, whereas geographic distance and soil pH remained of secondary importance. These results, together with the smaller genome size of fungi compared to other eukaryotes, suggest that fruiting-bodies are suitable for further genome-centric studies on hostmicrobiome interactions.

  • 28. Samils, Nicklas
    et al.
    Gioti, Anastasia
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Karlsson, Magnus
    Sun, Yu
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Kasuga, Takao
    Bastiaans, Eric
    Wang, Zheng
    Li, Ning
    Townsend, Jeffrey P.
    Johannesson, Hanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Sex-linked transcriptional divergence in the hermaphrodite fungus Neurospora tetrasperma2013In: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 280, no 1764, p. 20130862-Article in journal (Refereed)
    Abstract [en]

    In the filamentous ascomycete Neurospora tetrasperma, a large (approx. 7 Mbp) region of suppressed recombination surrounds the mating-type (mat) locus. While the remainder of the genome is largely homoallelic, this region of recombinational suppression, extending over 1500 genes, is associated with sequence divergence. Here, we used microarrays to examine how the molecular phenotype of gene expression level is linked to this divergent region, and thus to the mating type. Culturing N. tetrasperma on agar media that induce sexual/female or vegetative/male tissue, we found 196 genes significantly differentially expressed between mat A and mat a mating types. Our data show that the genes exhibiting mat-linked expression are enriched in the region genetically linked to mating type, and sequence and expression divergence are positively correlated. Our results indicate that the phenotype of mat A strains is optimized for traits promoting sexual/female development and the phenotype of mat a strains for vegetative/male development. This discovery of differentially expressed genes associated with mating type provides a link between genotypic and phenotypic divergence in this taxon and illustrates a fungal analogue to sexual dimorphism found among animals and plants.

  • 29. Samils, Nicklas
    et al.
    Oliva, Jonas
    Johannesson, Hanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Nuclear interactions in a heterokaryon: insight from the model Neurospora tetrasperma2014In: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 281, no 1786, p. UNSP 20140084-Article in journal (Refereed)
    Abstract [en]

    A heterokaryon is a tissue type composed of cells containing genetically different nuclei. Although heterokaryosis is commonly found in nature, an understanding of the evolutionary implications of this phenomenon is largely lacking. Here, we use the filamentous ascomycete Neurospora tetrasperma to study the interplay between nuclei in heterokaryons across vegetative and sexual developmental stages. This fungus harbours nuclei of two opposite mating types (mat A and mat a) in the same cell and is thereby self-fertile. We used pyrosequencing of mat-linked SNPs of three heterokaryons to demonstrate that the nuclear ratio is consistently biased for mat A-nuclei during mycelial growth (mean mat A/mat a ratio 87%), but evens out during sexual development (ratio ranging from 40 to 57%). Furthermore, we investigated the association between nuclear ratio and expression of alleles of mat-linked genes and found that expression is coregulated to obtain a tissue-specific bias in expression ratio: during mycelial extension, we found a strong bias in expression for mat A-linked genes, that was independent of nuclear ratio, whereas at the sexual stage we found an expression bias for genes of the mat a nuclei. Taken together, our data indicate that nuclei cooperate to optimize the fitness of the heterokaryon, via both altering their nuclear ratios and coregulation genes expressed in the different nuclei.

  • 30.
    Strandberg, Rebecka
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Nygren, Kristiina
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Menkis, Audrius
    Department of Forest Mycology and Pathology, Swedish University of Agricultural Sciences.
    James, Timothy Y.
    Department of Ecology and Evolutionary Biology, University of Michigan.
    Wik, Lotta
    Department of Biomedical Sciences and Veterinary Public Health, Swedish University of Agricultural Sciences.
    Stajich, Jason E.
    Department of Plant and Microbial Biology, University of California.
    Johannesson, Hanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Conflict between reproductive gene trees and species phylogeny among heterothallic and pseudohomothallic members of the filamentous ascomycete genus Neurospora2010In: Fungal Genetics and Biology, ISSN 1087-1845, E-ISSN 1096-0937, Vol. 47, no 10, p. 869-878Article in journal (Refereed)
    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.

  • 31.
    Strandberg, Rebecka
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Tzelepis, Georgios
    Johannesson, Hanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Karlsson, Magnus
    Coexistence and expression profiles of two alternative splice variants of the pheromone receptor gene pre-1 in Neurospora crassa2013In: Archives of Microbiology, ISSN 0302-8933, E-ISSN 1432-072X, Vol. 195, no 10-11, p. 773-780Article in journal (Refereed)
    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.

  • 32.
    Sun, Yu
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Corcoran, Padraic
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Menkis, Audrius
    Whittle, Carrie A.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Andersson, Siv G. E.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution.
    Johannesson, Hanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Large-Scale Introgression Shapes the Evolution of the Mating-Type Chromosomes of the Filamentous Ascomycete Neurospora tetrasperma2012In: PLOS Genetics, ISSN 1553-7390, E-ISSN 1553-7404, Vol. 8, no 7, p. e1002820-Article in journal (Refereed)
    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.

  • 33.
    Sun, Yu
    et al.
    South China Agr Univ, Coll Life Sci, Guangdong Prov Key Lab Prot Funct & Regulat Agr O, Guangzhou 510642, Guangdong, Peoples R China..
    Svedberg, Jesper
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
    Hiltunen, Markus
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
    Corcoran, Padraic
    Univ Sheffield, Dept Anim & Plant Sci, Sheffield S10 2TN, S Yorkshire, England..
    Johannesson, Hanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
    Large-scale suppression of recombination predates genomic rearrangements in Neurospora tetrasperma2017In: Nature Communications, ISSN 2041-1723, E-ISSN 2041-1723, Vol. 8, article id 1140Article in journal (Refereed)
    Abstract [en]

    A common feature of eukaryote genomes is large chromosomal regions where recombination is absent or strongly reduced, but the factors that cause this reduction are not well understood. Genomic rearrangements have often been implicated, but they may also be a consequence of recombination suppression rather than a cause. In this study, we generate eight high-quality genomic data sets of the filamentous ascomycete Neurospora tetrasperma, a fungus that lacks recombination over most of its largest chromosome. The genomes surprisingly reveal collinearity of the non-recombining regions and although large inversions are enriched in these regions, we conclude these inversions to be derived and not the cause of the suppression. To our knowledge, this is the first time that non-recombining, genic regions as large as 86% of a full chromosome (or 8 Mbp), are shown to be collinear. These findings are of significant interest for our understanding of the evolution of sex chromosomes and other supergene complexes.

  • 34.
    Sun, Yu
    et al.
    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 Cell and Molecular Biology, Molecular Evolution.
    Whittle, Carrie-Ann
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Corcoran, Pádraic
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Johannesson, Hanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Intron Evolution in Neurospora: the role of mutational bias and selection2015In: Genome Research, ISSN 1088-9051, E-ISSN 1549-5469, Vol. 25, no 1, p. 100-110Article in journal (Refereed)
    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.

  • 35.
    Svedberg, Jesper
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
    Hosseini, Sara
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
    Chen, Jun
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Vogan, Aaron A.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
    Mozgova, Iva
    Swedish Univ Agr Sci, Dept Plant Biol, POB 7080, SE-75007 Uppsala, Sweden;Swedish Univ Agr Sci, Linnean Ctr Plant Biol, POB 7080, SE-75007 Uppsala, Sweden;Czech Acad Sci, Inst Microbiol, Ctr Algatech, CZ-37981 Trebon, Czech Republic.
    Hennig, Lars
    Swedish Univ Agr Sci, Dept Plant Biol, POB 7080, SE-75007 Uppsala, Sweden;Swedish Univ Agr Sci, Linnean Ctr Plant Biol, POB 7080, SE-75007 Uppsala, Sweden.
    Manitchotpisit, Pennapa
    Illinois State Univ, Sch Biol Sci, Normal, IL 61790 USA.
    Abusharekh, Anna
    Illinois State Univ, Sch Biol Sci, Normal, IL 61790 USA.
    Hammond, Thomas M.
    Illinois State Univ, Sch Biol Sci, Normal, IL 61790 USA.
    Lascoux, Martin
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Johannesson, Hanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
    Convergent evolution of complex genomic rearrangements in two fungal meiotic drive elements2018In: Nature Communications, ISSN 2041-1723, E-ISSN 2041-1723, Vol. 9, article id 4242Article in journal (Refereed)
    Abstract [en]

    Meiotic drive is widespread in nature. The conflict it generates is expected to be an important motor for evolutionary change and innovation. In this study, we investigated the genomic consequences of two large multi-gene meiotic drive elements, Sk-2 and Sk-3, found in the filamentous ascomycete Neurospora intermedia. Using long-read sequencing, we generated the first complete and well-annotated genome assemblies of large, highly diverged, non-recombining regions associated with meiotic drive elements. Phylogenetic analysis shows that, even though Sk-2 and Sk-3 are located in the same chromosomal region, they do not form sister clades, suggesting independent origins or at least a long evolutionary separation. We conclude that they have in a convergent manner accumulated similar patterns of tandem inversions and dense repeat clusters, presumably in response to similar needs to create linkage between genes causing drive and resistance.

  • 36. Taylor, J W
    et al.
    Turner, E
    Pringle, A
    Dettman, J
    Johannesson, H
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Department of Evolution, Genomics and Systematics. Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Department of Evolution, Genomics and Systematics, Evolutionary Biology. Evolutionsbiologi.
    Fungal species: Thoughts on their recognition, maintenance and selection.2006In: Fungi in the Environment, Cambridge University Press, Cambridge , 2006Chapter in book (Refereed)
  • 37. Wang, Zheng
    et al.
    Kin, Koryu
    Lopez-Giraldez, Francesc
    Johannesson, Hanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Townsend, Jeffrey P.
    Sex-specific gene expression during asexual development of Neurospora crassa2012In: Fungal Genetics and Biology, ISSN 1087-1845, E-ISSN 1096-0937, Vol. 49, no 7, p. 533-543Article in journal (Refereed)
    Abstract [en]

    The impact of loci that determine sexual identity upon the asexual, dominant stage of fungal life history has been well studied. To investigate their impact, expression differences between strains of different mating type during asexual development were assayed, with RNA sampled from otherwise largely isogenic mat A and mat a strains of Neurospora crassa at early, middle, and late clonal stages of development. We observed significant differences in overall gene expression between mating types across clonal development, especially at late development stages. The expression levels of mating-type genes and pheromone genes were assayed by reverse transcription and quantitative PCR, revealing expression of pheromone and receptor genes in strains of both mating types in all development stages, and revealing that mating type (mat) genes were increasingly expressed over the course of asexual development. Interestingly, among differentially expressed genes, the mat A genotype more frequently exhibited a higher expression level than mat a, and demonstrated greater transcriptional regulatory dynamism. Significant up-regulation of expression was observed for many late light-responsive genes at late asexual development stages. Further investigation of the impact of light and the roles of light response genes in asexual development of both mating types are warranted.

  • 38.
    Whittle, Carrie A.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Johannesson, Hanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Evidence of the accumulation of allele-specific non-synonymous substitutions in the young region of recombination suppression within the mating-type chromosomes of Neurospora tetrasperma2011In: Heredity, ISSN 0018-067X, E-ISSN 1365-2540, Vol. 107, no 4, p. 305-314Article in journal (Refereed)
    Abstract [en]

    Currently, little is known about the origin and early evolution of sex chromosomes. This is largely due to the fact that ancient non-recombining sex chromosomes are highly degenerated, and thus provide little information about the early genomic events in their evolution. The Neurospora tetrasperma mating-type (mat) chromosomes contain a young (<6 Mya) and large region (>6.6 Mb) of suppressed recombination, thereby providing a model system to study early stages of sex chromosome evolution. Here, we examined alleles of 207 genes located on the N. tetrasperma mat a and mat A chromosomes to test for signs of genomic alterations at the protein level in the young region of recombination suppression. We report that the N. tetrasperma mat a and mat A chromosomes have each independently accumulated allele-specific non-synonymous codon substitutions in a time-dependent, and gene-specific manner in the recombinationally suppressed region. In addition, examination of the ratio (omega) of non-synonymous substitutions (dN) to synonymous substitutions (dS) using maximum likelihood analyses, indicates that such changes are associated with relaxed purifying selection, a finding consistent with genomic degeneration. We also reveal that sex specific biases in mutation rates or selection pressures are not necessary for genomic alterations in sex chromosomes, and that recombination suppression in itself is sufficient to explain these results. The present findings extend our current understanding of genomic events associated within the young region of recombination suppression in these fungal sex-regulating chromosomes.

  • 39.
    Whittle, Carrie A
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Johannesson, Hanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Evolution of Mating-Type Loci and Mating-Type Chromosomes in Model Species of Filamentous Ascomycetes2011In: THE MYCOTA XIV, Evolution of fungi and fungal-like organisms, Springer Verlag, Heidelberg , 2011Chapter in book (Other academic)
  • 40.
    Whittle, Carrie A.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Johannesson, Hanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Evolutionary Dynamics of Sex-Biased Genes in a Hermaphrodite Fungus2013In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 30, no 11, p. 2435-2446Article in journal (Refereed)
    Abstract [en]

    Differential gene expression is believed to largely explain sexually dichotomous phenotypes. This phenomenon is especially significant in hermaphrodites, in which male and female sexual tissues have identical genotypes. Sex differences in transcription have been linked to molecular evolution: genes with higher expression in male compared with female sexual tissues (i.e., male-biased genes) have been associated with rapid gene divergence in various animals and plants, implying that selective differences exist among the sexual structures. In the present investigation, we examined expressed sequence tags, microarrays, and gene sequence data from the hermaphroditic fungus Neurospora crassa and confirmed selective differences of genes with disparate expression among male versus female sexual structures in this organism. The results held across various genotypes and stages of sexual development. Furthermore, our data showed that N. crassa comprises a rare example of an organism where female-biased genes evolve rapidly; they exhibited faster evolution at the protein level and reduced optimal codon usage compared with male-biased genes, sexually unbiased genes, and vegetative genes. Female-biased genes also had a greater portion of sites that experienced positive selection and showed stronger signals of selective sweeps than male-biased genes, suggesting that the rapid evolution is at least partly driven by adaptive evolution. Distinctive aspects of the reproductive biology of N. crassa which might explain the rapid evolution of female-biased genes are discussed, particularly the propensity for female-female competition during mating, as well as the multifunctional nature of male structures. The present findings open new opportunities to test hypotheses about sex-biased gene expression and molecular evolution.

  • 41.
    Whittle, Carrie A.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Johannesson, Hanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Neurospora as a model to empirically test central hypotheses in eukaryotic genome evolution2012In: Bioessays, ISSN 0265-9247, E-ISSN 1521-1878, Vol. 34, no 11, p. 934-937Article in journal (Refereed)
    Abstract [en]

    The fungus Neurospora comprises a novel model for testing hypotheses involving the role of sex and reproduction in eukaryotic genome evolution. Its variation in reproductive mode, lack of sex-specific genotypes, availability of phylogenetic species, and young sex-regulating chromosomes make research in this genus complementary to animal and plant models.

  • 42.
    Whittle, Carrie A.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Nygren, Kristiina
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Johannesson, Hanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Consequences of reproductive mode on genome evolution in fungi2011In: Fungal Genetics and Biology, ISSN 1087-1845, E-ISSN 1096-0937, Vol. 48, no 7, p. 661-667Article, review/survey (Refereed)
    Abstract [en]

    An organism's reproductive mode is believed to be a major factor driving its genome evolution. In theory, sexual inbreeding and asexuality are associated with lower effective recombination levels and smaller effective population sizes than sexual outbreeding, giving rise to reduced selection efficiency and genetic hitchhiking. This, in turn, is predicted to result in the accumulation of deleterious mutations and other genomic changes, for example the accumulation of repetitive elements. Empirical data from plants and animals supporting/refuting these theories are sparse and have yielded few conclusive results. A growing body of data from the fungal kingdom, wherein reproductive behavior varies extensively within and among taxonomic groups, has provided new insights into the role of mating systems (e.g., homothallism, heterothallism, pseudohomothallism) and asexuality, on genome evolution. Herein, we briefly review the theoretical relationships between reproductive mode and genome evolution and give examples of empirical data on the topic derived to date from plants and animals. We subsequently focus on the available data from fungi, which suggest that reproductive mode alters the rates and patterns of genome evolution in these organisms, e.g., protein evolution, mutation rate, codon usage, frequency of genome rearrangements and repetitive elements, and variation in chromosome size.

  • 43.
    Whittle, Carrie A.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Sun, Yu
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Johannesson, Hanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Dynamics of transcriptome evolution in the model eukaryote Neurospora2014In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 27, no 6, p. 1125-1135Article in journal (Refereed)
    Abstract [en]

    Mounting evidence indicates that changes in the transcriptome contribute significantly to the phenotypic differentiation of closely related species. Nonetheless, further genome-wide studies, spanning a broad range of organisms, are needed to decipher the factors driving transcriptome evolution. The model Neurospora (Ascomycota) comprises a simple system for empirically studying the evolutionary dynamics of the transcriptome. Here, we studied the evolution of gene expression in Neurospora crassa and Neurospora tetrasperma and show that patterns of transcriptome evolution are connected to genome evolution, tissue type and sexual identity (mating types, mat A and mat a) in these eukaryotes. Based on the comparisons of inter- and intraspecies expression divergence, our data reveal that rapid expression divergence is more apt to occur in sexual/female (SF) than vegetative/male (VM) tissues. In addition, interspecies gene expression and protein sequence divergence were strongly correlated for SF, but not VM, tissue. A correlation between transcriptome and protein evolution parallels findings from certain animals, but not yeast, and add support for the theory that expression evolution differs fundamentally among multicellular and unicellular eukaryotes. Finally, we found that sexual identity in these hermaphroditic Neurospora species is connected to interspecies expression divergence in a tissue-dependent manner: rapid divergence occurred for mat A- and mat a-biased genes from SF and VM tissues, respectively. Based on these findings, it is hypothesized that rapid interspecies transcriptome evolution is shifting the mating types of Neurospora towards distinct female and male phenotypes, that is, sexual dimorphism.

  • 44.
    Whittle, Carrie A.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Sun, Yu
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Johannesson, Hanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Evolution of Synonymous Codon Usage in Neurospora tetrasperma and Neurospora discreta2011In: Genome Biology and Evolution, ISSN 1759-6653, E-ISSN 1759-6653, Vol. 3, p. 332-343Article in journal (Refereed)
    Abstract [en]

    Neurospora comprises a primary model system for the study of fungal genetics and biology. In spite of this, little is known about genome evolution in Neurospora. For example, the evolution of synonymous codon usage is largely unknown in this genus. In the present investigation, we conducted a comprehensive analysis of synonymous codon usage and its relationship to gene expression and gene length (GL) in Neurospora tetrasperma and Neurospora discreta. For our analysis, we examined codon usage among 2,079 genes per organism and assessed gene expression using large-scale expressed sequenced tag (EST) data sets (279,323 and 453,559 ESTs for N. tetrasperma and N. discreta, respectively). Data on relative synonymous codon usage revealed 24 codons (and two putative codons) that are more frequently used in genes with high than with low expression and thus were defined as optimal codons. Although codon-usage bias was highly correlated with gene expression, it was independent of selectively neutral base composition (introns); thus demonstrating that translational selection drives synonymous codon usage in these genomes. We also report that GL (coding sequences [CDS]) was inversely associated with optimal codon usage at each gene expression level, with highly expressed short genes having the greatest frequency of optimal codons. Optimal codon frequency was moderately higher in N. tetrasperma than in N. discreta, which might be due to variation in selective pressures and/or mating systems.

  • 45.
    Whittle, Carrie A.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Sun, Yu
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Johannesson, Hanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Genome-Wide Selection on Codon Usage at the Population Level in the Fungal Model Organism Neurospora crassa2012In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 29, no 8, p. 1975-1986Article in journal (Refereed)
    Abstract [en]

    Many organisms exhibit biased codon usage in their genome, including the fungal model organism Neurospora crassa. The preferential use of subset of synonymous codons (optimal codons) at the macroevolutionary level is believed to result from a history of selection to promote translational efficiency. At present, few data are available about selection on optimal codons at the microevolutionary scale, that is, at the population level. Herein, we conducted a large-scale assessment of codon mutations at biallelic sites, spanning more than 5,100 genes, in 2 distinct populations of N. crassa: the Caribbean and Louisiana populations. Based on analysis of the frequency spectra of synonymous codon mutations at biallelic sites, we found that derived (nonancestral) optimal codon mutations segregate at a higher frequency than derived nonoptimal codon mutations in each population; this is consistent with natural selection favoring optimal codons. We also report that optimal codon variants were less frequent in longer genes and that the fixation of optimal codons was reduced in rapidly evolving long genes/proteins, trends suggestive of genetic hitchhiking (Hill-Robertson) altering codon usage variation. Notably, nonsynonymous codon mutations segregated at a lower frequency than synonymous nonoptimal codon mutations (which impair translational efficiency) in each N. crassa population, suggesting that changes in protein composition are more detrimental to fitness than mutations altering translation. Overall, the present data demonstrate that selection, and partly genetic interference, shapes codon variation across the genome in N. crassa populations.

  • 46.
    Whittle, Carrie
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Sun, Yu
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Johannesson, Hanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Degeneration in Codon Usage within the Region of Suppressed Recombination in the Mating-Type Chromosomes of Neurospora tetrasperma2011In: Eukaryotic Cell, ISSN 1535-9778, E-ISSN 1535-9786, Vol. 10, no 4, p. 594-603Article in journal (Refereed)
    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.

  • 47. Wik, Lotta
    et al.
    Karlsson, Magnus
    Johannesson, Hanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Evolutionary Biology.
    The evolutionary trajectory of the mating-type (mat) genes in Neurospora relates to reproductive behavior of taxa2008In: BMC Evolutionary Biology, ISSN 1471-2148, E-ISSN 1471-2148, Vol. 8, no 1, p. 109-Article in journal (Refereed)
    Abstract [en]

    Background: Comparative sequencing studies among a wide range of taxonomic groups, including fungi, have led to the discovery that reproductive genes evolve more rapidly than other genes. However, for fungal reproductive genes the question has remained whether the rapid evolution is a result of stochastic or deterministic processes. The mating-type (mat) genes constitute the master regulators of sexual reproduction in filamentous ascomycetes and here we present a study of the molecular evolution of the four mat-genes (mat a-1, mat A-1, mat A-2 and mat A-3) of 20 Neurospora taxa. Results: We estimated nonsynonymous and synonymous substitution rates of genes to infer their evolutionary rate, and confirmed that the mat-genes evolve rapidly. Furthermore, the evolutionary trajectories are related to the reproductive modes of the taxa; likelihood methods revealed that positive selection acting on specific codons drives the diversity in heterothallic taxa, while among homothallic taxa the rapid evolution is due to a lack of selective constraint. The latter finding is supported by presence of stop codons and frame shift mutations disrupting the open reading frames of mat a-1, mat A-2 and mat A-3 in homothallic taxa. Lower selective constraints of matgenes was found among homothallic than heterothallic taxa, and comparisons with nonreproductive genes argue that this disparity is not a nonspecific, genome-wide phenomenon. Conclusion: Our data show that the mat-genes evolve rapidly in Neurospora. The rapid divergence is due to either adaptive evolution or lack of selective constraints, depending on the reproductive mode of the taxa. This is the first instance of positive selection acting on reproductive genes in the fungal kingdom, and illustrates how the evolutionary trajectory of reproductive genes can change after a switch in reproductive behaviour of an organism.

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