Faculty Opinions recommendation of Molecular dissection of Neurospora Spore killer meiotic drive elements.

Author(s):  
Matthew Sachs ◽  
Xiaorong Lin
2021 ◽  
Author(s):  
Nicholas A. Rhoades ◽  
Thomas M. Hammond

ABSTRACTNeurospora Sk-2 is a complex meiotic drive element that is transmitted to offspring through sexual reproduction in a biased manner. Sk-2’s biased transmission mechanism involves spore killing, and recent evidence has demonstrated that spore killing is triggered by a gene called rfk-1. However, a second gene, rsk, is also critically important for meiotic drive by spore killing because it allows offspring with an Sk-2 genotype to survive the toxic effects of rfk-1. Here, we present evidence demonstrating that rfk-1 encodes two protein variants: a 102 amino acid RFK-1A and a 130 amino acid RFK-1B, but only RFK-1B is toxic. We also show that expression of RFK-1B requires an early stop codon in rfk-1 mRNA to undergo adenosine-to-inosine (A-to-I) mRNA editing. Finally, we demonstrate that RFK-1B is toxic when expressed within vegetative tissue of Spore killer sensitive (SkS) strains, and that this vegetative toxicity can be overcome by co-expressing Sk-2’s version of RSK. Overall, our results demonstrate that Sk-2 uses RNA editing to control when its spore killer is produced, and that the primary killing and resistance functions of Sk-2 can be conferred upon an SkS strain by the transfer of only two genes.


eLife ◽  
2019 ◽  
Vol 8 ◽  
Author(s):  
Aaron A Vogan ◽  
S Lorena Ament-Velásquez ◽  
Alexandra Granger-Farbos ◽  
Jesper Svedberg ◽  
Eric Bastiaans ◽  
...  

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.


Author(s):  
Jesper Svedberg ◽  
Aaron A. Vogan ◽  
Nicholas A. Rhoades ◽  
Dilini Sarmarajeewa ◽  
David J. Jacobson ◽  
...  

AbstractMeiotic 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. Through molecular dissection, we show that a single 405 nucleotide 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 is likely to have been introgressed from the closely related species N. 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 new light on the diversity of genes capable of causing meiotic drive, their origin and evolution and their interaction with the host genome.Significance StatementIn order to survive, most organisms have to deal with parasites. Such parasites can be other organisms, or sometimes, selfish genes found within the host genome itself. While much is known about parasitic organisms, the interaction with their hosts and their ability to spread within and between species, much less is known about selfish genes. We here identify a novel selfish “spore killer” gene in the fungus Neurospora sitophila. The gene appears to have evolved within the genus, but has entered the species through hybridization and introgression. We also show that the host can counteract the gene through RNA interference. These results shed new light on the diversity of selfish genes in terms of origin, evolution and host interactions.


Genetics ◽  
2000 ◽  
Vol 156 (2) ◽  
pp. 593-605 ◽  
Author(s):  
Marijn van der Gaag ◽  
Alfons J M Debets ◽  
Jessica Oosterhof ◽  
Marijke Slakhorst ◽  
Jessica A G M Thijssen ◽  
...  

Abstract In fungi, meiotic drive is observed as spore killing. In the secondarily homothallic ascomycete Podospora anserina it is characterized by the abortion of two of the four spores in the ascus. We have identified seven different types of meiotic drive elements (Spore killers). Among 99 isolates from nature, six of these meiotic drive elements occurred in a local population. Spore killers comprise 23% of the natural population of P. anserina in Wageningen, The Netherlands, sampled from 1991 to 1997. One Spore-killer type was also found in a French strain dating from 1937. All other isolates found so far are sensitive to spore killing. All seven Spore killer types differ in the percentage of asci that show killing and in their mutual interactions. Interactions among Spore killer types showed either mutual resistance or dominant epistasis. Most killer elements could be assigned to linkage group III but are not tightly linked to the centromere.


2016 ◽  
Author(s):  
Jay Pyle ◽  
Tejas Patel ◽  
Brianna Merril ◽  
Chabu Nsokoshi ◽  
Morgan McCall ◽  
...  

ABSTRACTFusarium verticillioidesis an agriculturally important fungus because of its association with maize and its propensity to contaminate grain with toxic compounds. Some isolates of the fungus harbor a meiotic drive element known as Sporekiller(SkK) that causes nearly all surviving meiotic progeny from anSkK× Spore killer-susceptible (SkS) cross to inherit theSkKallele.SkKhas been mapped to chromosome V but the genetic element responsible for meiotic drive and spore killing has yet to be identified. In this study, we used cleaved amplified polymorphic sequence markers to genotype individual progeny from anSkK×SkSmapping population. We also sequenced the genomes of three progeny from the mapping population to determine their single nucleotide polymorphisms. These techniques allowed us to refine the location ofSkKto a contiguous 102-kb region of chromosome V, herein referred to as theSklocus. Relative toSkSgenotypes,SkKgenotypes have one extra gene within this locus for a total of 42 genes. The additional gene inSkKgenotypes, named SKL1 forSpore Killer Locus 1, is the most highly expressed gene from theSklocus during early stages of sexual development. TheSklocus also has three hypervariable regions, the longest of which includesSKL1. The possibility thatSKL1, or another gene from theSklocus, is an essential component of meiotic drive and spore killing is discussed.


Genome ◽  
1987 ◽  
Vol 29 (1) ◽  
pp. 129-135 ◽  
Author(s):  
Joseph L. Campbell ◽  
Barbara C. Turner

Spore killers Sk-2K and Sk-3K are chromosomal meiotic drive factors in Neurospora. In heterozygous crosses, ascospores not contining the Spore killer die. Sk-2K and Sk-3K, which differ in killing specificity, were found to be associated with suppression of recombination in a centromere-spanning region of linkage group III, and investigation of that recombination block is reported here. The block covers a region that is normally 30 to 40 map units long. A locus (r(Sk-2)) conferring resistance to Sk-2K maps to the left end of the recombination block. Recombination is normal in r(Sk-2) × Sk sensitive but blocked in Sk-2K × r(Sk-2); so the block does not depend upon killing. By selective plating, SkK stocks carrying genetic markers within the block were obtained at frequencies on the order of 10−5 or 10−6. Since this tight block is far beyond what has been observed for genetic reduction of recombination, a structural basis is assumed. No evidence of chromosome rearrangement was obtained. Crosses homozygous for Sk-2K show normal crossing-over and map order for the flanking markers cum and his-7 and three included markers (acr-7, acr-2, and leu-1). Results would be consistent with a divergence of sequence great enough to interfere with homologous pairing. Key words: meiotic drive, Neurospora, crossover suppressor.


2012 ◽  
Vol 109 (30) ◽  
pp. 12093-12098 ◽  
Author(s):  
Thomas M. Hammond ◽  
David G. Rehard ◽  
Hua Xiao ◽  
Patrick K. T. Shiu

2018 ◽  
Author(s):  
Nicholas A. Rhoades ◽  
Austin M. Harvey ◽  
Dilini A. Samarajeewa ◽  
Jesper Svedberg ◽  
Aykhan Yusifov ◽  
...  

ABSTRACTMeiotic drive elements like Spore killer-2 (Sk-2) in Neurospora are transmitted through sexual reproduction to the next generation in a biased manner. Sk-2 achieves this biased transmission through spore killing. Here, we identify rfk-1 as a gene required for the spore killing mechanism. The rfk-1 gene is associated with a 1,481 bp DNA interval (called AH36) near the right border of the 30 cM Sk-2 element, and its deletion eliminates the ability of Sk-2 to kill spores. The rfk-1 gene also appears to be sufficient for spore killing because its insertion into a non-Sk-2 isolate disrupts sexual reproduction after the initiation of meiosis. Although the complete rfk-1 transcript has yet to be defined, our data indicate that rfk-1 encodes a protein of at least 39 amino acids and that rfk-1 has evolved from a partial duplication of gene ncu07086. We also present evidence that rfk-1’s location near the right border of Sk-2 is critical for the success of spore killing. Increasing the distance of rfk-1 from the right border of Sk-2 causes it to be inactivated by a genome defense process called meiotic silencing by unpaired DNA (MSUD), adding to accumulating evidence that MSUD exists, at least in part, to protect genomes from meiotic drive.


Genetics ◽  
1991 ◽  
Vol 129 (1) ◽  
pp. 25-37 ◽  
Author(s):  
N B Raju ◽  
D D Perkins

Abstract It was shown previously that when a chromosomal Spore killer factor is heterozygous in Neurospora species with eight-spored asci, the four sensitive ascospores in each ascus die and the four survivors are all killers. Sk-2K and Sk-3K are nonrecombining haplotypes that segregate with the centromere of linkage group III. No killing occurs when either one of these killers is homozygous, but each is sensitive to killing by the other in crosses of Sk-2K x Sk-3K. In the present study, Sk-2K and Sk-3K were transferred by recurrent backcrosses from the eight-spored species Neurospora crassa into Neurospora tetrasperma, a pseudohomothallic species which normally makes asci with four large spores, each heterokaryotic for mating type and for any other centromere-linked genes that are heterozygous in the cross. The action of Sk-2K and Sk-3K in N. tetrasperma is that predicted from their behavior in eight-spored species. A sensitive nucleus is protected from killing if it is enclosed in the same ascospore with a killer nucleus. Crosses of Sk-2K x Sk-2S, Sk-3K x Sk-3S, and Sk-sK x Sk-3K all produce four-spored asci that are wild type in appearance, with the ascospores heterokaryotic and viable. The Eight-spore gene E, which shows variable penetrance, was used to obtain N. tetrasperma asci in which two to eight spores are small and homokaryotic. When killer and sensitive alleles are segregating in the presence of E, only those ascospores that contain a killer allele survive. Half of the small ascospores are killed. In crosses of Sk-2K x Sk-3K (with E heterozygous), effectively all small ascospores are killed. The ability of N. tetrasperma to carry killer elements in cryptic condition suggests a possible role for Spore killers in the origin of pseudohomothallism, with adoption of the four-spored mode restoring ascospore viability of crosses in which killing would otherwise occur.


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