| 1. |
- Vogan, Aaron A., et al.
(författare)
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Meiotic drive is associated with sexual incompatibility in Neurospora
- 2022
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Ingår i: Evolution. - : Wiley. - 0014-3820 .- 1558-5646. ; 76:11, s. 2687-2696
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Tidskriftsartikel (refereegranskat)abstract
- Evolution of Bateson-Dobzhansky-Muller (BDM) incompatibilities is thought to represent a key step in the formation of separate species. They are incompatible alleles that have evolved in separate populations and are exposed in hybrid offspring as hybrid sterility or lethality. In this study, we reveal a previously unconsidered mechanism promoting the formation of BDM incompatibilities, meiotic drive. Theoretical studies have evaluated the role that meiotic drive, the phenomenon whereby selfish elements bias their transmission to progeny at ratios above 50:50, plays in speciation, and have mostly concluded that drive could not result in speciation on its own. Using the model fungus Neurospora, we demonstrate that the large meiotic drive haplotypes, Sk-2 and Sk-3, contain putative sexual incompatibilities. Our experiments revealed that although crosses between Neurospora intermedia and Neurospora metzenbergii produce viable progeny at appreciable rates, when strains of N. intermedia carry Sk-2 or Sk-3 the proportion of viable progeny drops substantially. Additionally, it appears that Sk-2 and Sk-3 have accumulated different incompatibility phenotypes, consistent with their independent evolutionary history. This research illustrates how meiotic drive can contribute to reproductive isolation between populations, and thereby speciation.
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| 2. |
- Vogan, Aaron A., et al.
(författare)
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The spore killers, fungal meiotic driver elements
- 2022
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Ingår i: Mycologia. - : Informa UK Limited. - 0027-5514 .- 1557-2536. ; 114:1, s. 1-23
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Tidskriftsartikel (refereegranskat)abstract
- During meiosis, both alleles of any given gene should have equal chances of being inherited by the progeny. There are a number of reasons why, however, this is not the case, with one of the most intriguing instances presenting itself as the phenomenon of meiotic drive. Genes that are capable of driving can manipulate the ratio of alleles among viable meiotic products so that they are inherited in more than half of them. In many cases, this effect is achieved by direct antagonistic interactions, where the driving allele inhibits or otherwise eliminates the alternative allele. In ascomycete fungi, meiotic products are packaged directly into ascospores; thus, the effect of meiotic drive has been given the nefarious moniker, "spore killing." In recent years, many of the known spore killers have been elevated from mysterious phenotypes to well-described systems at genetic, genomic, and molecular levels. In this review, we describe the known diversity of spore killers and synthesize the varied pieces of data from each system into broader trends regarding genome architecture, mechanisms of resistance, the role of transposable elements, their effect on population dynamics, speciation and gene flow, and finally how they may be developed as synthetic drivers. We propose that spore killing is common, but that it is under-observed because of a lack of studies on natural populations. We encourage researchers to seek new spore killers to build on the knowledge that these remarkable genetic elements can teach us about meiotic drive, genomic conflict, and evolution more broadly.
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| 3. |
- Svedberg, Jesper, et al.
(författare)
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An introgressed gene causes meiotic drive in Neurospora sitophila
- 2021
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Ingår i: Proceedings of the National Academy of Sciences of the United States of America. - : Proceedings of the National Academy of Sciences (PNAS). - 0027-8424 .- 1091-6490. ; 118:17
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Tidskriftsartikel (refereegranskat)abstract
- Meiotic drive elements cause their own preferential transmission following meiosis. In fungi, this phenomenon takes the shape of spore killing, and in the filamentous ascomycete Neurospora sitophila, the Sk-1 spore killer element is found in many natural populations. In this study, we identify the gene responsible for spore killing in Sk-1 by generating both long- and short-read genomic data and by using these data to perform a genome-wide association test. We name this gene Spk-1. Through molecular dissection, we show that a single 405-nt-long open reading frame generates a product that both acts as a poison capable of killing sibling spores and as an antidote that rescues spores that produce it. By phylogenetic analysis, we demonstrate that the gene has likely been introgressed from the closely related species Neurospora hispaniola, and we identify three subclades of N. sitophila, one where Sk-1 is fixed, another where Sk-1 is absent, and a third where both killer and sensitive strain are found. Finally, we show that spore killing can be suppressed through an RNA interference-based genome defense pathway known as meiotic silencing by unpaired DNA. Spk-1 is not related to other known meiotic drive genes, and similar sequences are only found within Neurospora. These results shed light on the diversity of genes capable of causing meiotic drive, their origin and evolution, and their interaction with the host genome.
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| 4. |
- Rhoades, Nicholas A., et al.
(författare)
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Identification of rfk-1, a Meiotic Driver Undergoing RNA Editing in Neurospora
- 2019
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Ingår i: Genetics. - : GENETICS SOCIETY AMERICA. - 0016-6731 .- 1943-2631. ; 212:1, s. 93-110
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Tidskriftsartikel (refereegranskat)abstract
- Sk-2 is a meiotic drive element that was discovered in wild populations of Neurospora fungi over 40 years ago. While early studies quickly determined that Sk-2 transmits itself through sexual reproduction in a biased manner via spore killing, the genetic factors responsible for this phenomenon have remained mostly unknown. Here, we identify and characterize rfk-1, a gene required for Sk-2-based spore killing. The rfk-1 gene contains four exons, three introns, and two stop codons, the first of which undergoes RNA editing to a tryptophan codon during sexual development. Translation of an unedited rfk-1 transcript in vegetative tissue is expected to produce a 102-amino acid protein, whereas translation of an edited rfk-1 transcript in sexual tissue is expected to produce a protein with 130 amino acids. These findings indicate that unedited and edited rfk-1 transcripts exist and that these transcripts could have different roles with respect to the mechanism of meiotic drive by spore killing. Regardless of RNA editing, spore killing only succeeds if rfk-1 transcripts avoid silencing caused by a genome defense process called meiotic silencing by unpaired DNA (MSUD). We show that rfk-1's MSUD avoidance mechanism is linked to the genomic landscape surrounding the rfk-1 gene, which is located near the Sk-2 border on the right arm of chromosome III. In addition to demonstrating that the location of rfk-1 is critical to spore-killing success, our results add to accumulating evidence that MSUD helps protect Neurospora genomes from complex meiotic drive elements.
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| 5. |
- Vogan, Aaron A., et al.
(författare)
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Combinations of Spok genes create multiple meiotic drivers in Podospora
- 2019
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Ingår i: eLIFE. - : ELIFE SCIENCES PUBLICATIONS LTD. - 2050-084X. ; 8
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Tidskriftsartikel (refereegranskat)abstract
- Meiotic drive is the preferential transmission of a particular allele during sexual reproduction. The phenomenon is observed as spore killing in multiple fungi. In natural populations of Podospora anserina, seven spore killer types (Psks) have been identified through classical genetic analyses. Here we show that the Spok gene family underlies the Psks. The combination of Spok genes at different chromosomal locations defines the spore killer types and creates a killing hierarchy within a population. We identify two novel Spok homologs located within a large (74-167 kbp) region (the Spok block) that resides in different chromosomal locations in different strains. We confirm that the SPOK protein performs both killing and resistance functions and show that these activities are dependent on distinct domains, a predicted nuclease and kinase domain. Genomic and phylogenetic analyses across ascomycetes suggest that the Spok genes disperse through cross-species transfer, and evolve by duplication and diversification within lineages.
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| 6. |
- Svedberg, Jesper, et al.
(författare)
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Convergent evolution of complex genomic rearrangements in two fungal meiotic drive elements
- 2018
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Ingår i: Nature Communications. - : NATURE PUBLISHING GROUP. - 2041-1723. ; 9
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Tidskriftsartikel (refereegranskat)abstract
- 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.
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| 7. |
- Sun, Yu, et al.
(författare)
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Large-scale suppression of recombination predates genomic rearrangements in Neurospora tetrasperma
- 2017
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Ingår i: Nature Communications. - : Springer Science and Business Media LLC. - 2041-1723. ; 8
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Tidskriftsartikel (refereegranskat)abstract
- 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.
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| 8. |
- Svedberg, Jesper, 1981-
(författare)
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Catching the Spore killers : Genomic conflict and genome evolution in Neurospora
- 2017
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Doktorsavhandling (övrigt vetenskapligt/konstnärligt)abstract
- A genome is shaped by many different forces. Recombination can for instance both create and maintain genetic diversity, but the need to locally reduce recombination rates will also leave specific signatures. Genetic elements can act selfishly and spreading at the expense of the rest of the genome can leave marks of their activity, as can mechanisms that suppresses them, in a phenomenon known as genomic conflict. In this thesis, I have studied the forces driving genome evolution, using modern genome sequencing techniques and with a special focus on a class of selfish genetic elements known as Spore killers found in the fungus Neurospora. First, we show novel findings on large-scale suppression of recombination by non-structural means in the N. tetrasperma genomes. In contrary, in the genomic region harbouring the spore killer elements Sk-2 and Sk-3 of N. intermedia, a dense set of inversions that are interspersed with transposable elements have accumulated. The inversions are unique for each killer type, showing that they have a long separated evolutionary history and likely have established themselves independently. For the Sk-2 haplotype, where we have polymorphism data, we see signs of relaxed selection, which is consistent with the hypothesis that recombination suppression reduces the efficacy of selection in this region. These results show the strong effects the divergent selective forces of genomic conflicts can have on chromosome architecture. Furthermore, we investigate the hypothesis that spore killing can drive reproductive isolation, by comparing the fertility of crosses between N. metzenbergii and either killer or non-killer N. intermedia strains. We show that crosses with spore killer strains have lower fertility, which cannot be explained by the killing itself, but is potentially caused by an incompatibility gene captured in the non-recombining region. Finally, we identified the genetic element responsible for causing spore killing in the Sk-1 spore killer strains found in N. sitophila. Unlike the Sk-2 and Sk-3 elements, Sk-1 is not connected to a large, non-recombining region, but is caused by a single locus, and we also find indications that this locus was introgressed from N. hispaniola.
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| 9. |
- Haddad Momeni, Majid, et al.
(författare)
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Structural, Biochemical, and Computational Characterization of the Glycoside Hydrolase Family 7 Cellobiohydrolase of the Tree-killing Fungus Heterobasidion irregulare
- 2013
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Ingår i: Journal of Biological Chemistry. - 0021-9258 .- 1083-351X. ; 288:8, s. 5861-5872
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Tidskriftsartikel (refereegranskat)abstract
- Root rot fungi of the Heterobasidion annosum complex are the most damaging pathogens in temperate forests, and the recently sequenced Heterobasidion irregulare genome revealed over 280 carbohydrate-active enzymes. Here, H. irregulare was grown on biomass, and the most abundant protein in the culture filtrate was identified as the only family 7 glycoside hydrolase in the genome, which consists of a single catalytic domain, lacking a linker and carbohydrate-binding module. The enzyme, HirCel7A, was characterized biochemically to determine the optimal conditions for activity. HirCel7A was crystallized and the structure, refined at 1.7 angstrom resolution, confirms that HirCel7A is a cellobiohydrolase rather than an endoglucanase, with a cellulose-binding tunnel that is more closed than Phanerochaete chrysosporium Cel7D and more open than Hypocrea jecorina Cel7A, suggesting intermediate enzyme properties. Molecular simulations were conducted to ascertain differences in enzyme-ligand interactions, ligand solvation, and loop flexibility between the family 7 glycoside hydrolase cellobiohydrolases from H. irregulare, H. jecorina, and P. chrysosporium. The structural comparisons and simulations suggest significant differences in enzyme-ligand interactions at the tunnel entrance in the -7 to -4 binding sites and suggest that a tyrosine residue at the tunnel entrance of HirCel7A may serve as an additional ligand-binding site. Additionally, the loops over the active site in H. jecorina Cel7A are more closed than loops in the other two enzymes, which has implications for the degree of processivity, endo- initiation, and substrate dissociation. Overall, this study highlights molecular level features important to understanding this biologically and industrially important family of glycoside hydrolases.
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| 10. |
- Svedberg, Jesper, 1981-, et al.
(författare)
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A single gene causes meiotic drive in Neurospora sitophila
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Annan publikation (övrigt vetenskapligt/konstnärligt)abstract
- Meiotic drive in Neurospora was first identified in Neurospora sitophila over forty years ago. Since drive in this fungus results in “spore killing”, the drive was designated Sk-1. The locus responsible for killing has until now been unknown. Here we sequenced 56 N. sitophila strains from natural populations, using paired-end sequencing on the Illumina HiSeq platform, and used this population genomic data to identify a locus on chromosome VI that significantly associates with the killing phenotypewe have used Illumina technology to generate whole genome sequence data for 56 wild N. sitophila strains. Using a genome wide association test we have identified the locus responsible for the Sk-1 phenotype on chromosome VI. We call the locus nkl1. By using the PacBio RSII platform, we generated high quality genome assemblies of four N. sitophila strains (two Sk-1 killers and two sensitives) and verified that no structural rearrangements were found in this region or on other chromosomes. We verified by laboratory crosses that the allelic variants of nkl1 show segregation distortion, and generated deletion mutants to demonstrate that the locus is responsible both for killing and resistance. We show demonstrate that the element is likely to have been introgressed from the closely related species, N. hispaniola. We identified three subclades in N. sitophila is split up into three subclades, in one of which Sk-1 is fixed for Sk-1, one another where Sk-1 is absent, and a third where killers and sensitives appear to intermix. This indicates that Sk-1 is currently invading N. sitophila through matings between diverged lineages.
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