Evolution of the Schlafen genes, a gene family associated with embryonic lethality, meiotic drive, immune processes and orthopoxvirus virulence

Gene ◽  
2009 ◽  
Vol 447 (1) ◽  
pp. 1-11 ◽  
Author(s):  
Olivia Bustos ◽  
Saijal Naik ◽  
Gayle Ayers ◽  
Claudio Casola ◽  
Maria A. Perez-Lamigueiro ◽  
...  
2011 ◽  
Vol 2 (3) ◽  
pp. 159-169 ◽  
Author(s):  
Elena de la Casa-Esperón

AbstractThe Schlafen genes have been associated with proliferation control and with several differentiation processes, as well as with disparate phenotypes such as immune response, embryonic lethality and meiotic drive. They constitute a gene family with widespread distribution in mammals, where they are expressed in several tissues, predominantly those of the immune system. Moreover, horizontal transfer of these genes to orthopoxviruses suggests a role of the viral Schlafens in evasion to the host immune response. The expression and functional studies of this gene family will be reviewed under the prism of their evolution and diversification, the challenges they pose and the future avenues of research.


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.


2019 ◽  
Vol 36 (6) ◽  
pp. 1201-1214 ◽  
Author(s):  
Michael T Eickbush ◽  
Janet M Young ◽  
Sarah E Zanders

2018 ◽  
Author(s):  
Michael T. Eickbush ◽  
Janet M. Young ◽  
Sarah E. Zanders

AbstractNatural selection works best when the two alleles in a diploid organism are transmitted to offspring at equal frequencies. Despite this, selfish loci known as meiotic drivers that bias their own transmission into gametes are found throughout eukaryotes. Drive is thought to be a powerful evolutionary force, but empirical evolutionary analyses of drive systems are limited by low numbers of identified meiotic drive genes. Here, we analyze the evolution of the wtf gene family of Schizosaccharomyces pombe that contains both killer meiotic drive genes and suppressors of drive. We completed assemblies of all wtf genes for two S. pombe strains, as well as a subset of wtf genes from over 50 strains. We find that wtf copy number can vary greatly between strains, and that amino acid substitutions, expansions and contractions of DNA sequence repeats, and nonallelic gene conversion between family members all contribute to dynamic wtf gene evolution. This work demonstrates the power of meiotic drive to foster rapid evolution and identifies a recombination mechanism through which transposons can indirectly mobilize meiotic drivers.


2019 ◽  
Author(s):  
María Angélica Bravo Núñez ◽  
Ibrahim M. Sabbarini ◽  
Michael T. Eickbush ◽  
Yue Liang ◽  
Jeffrey J. Lange ◽  
...  

AbstractMeiotic drivers are selfish genetic loci that force their transmission into more than 50% of the viable gametes made by heterozygotes. Meiotic drivers are known to cause infertility in a diverse range of eukaryotes and are predicted to affect the evolution of genome structure and meiosis. The wtf gene family of Schizosaccharomyces pombe includes both meiotic drivers and drive suppressors and thus offers a tractable model organism to study drive systems. Currently, only a handful of wtf genes have been functionally characterized and those genes only partially reflect the diversity of the wtf gene family. In this work, we functionally test 22 additional wtf genes. We identify eight new drivers that share between 30-90% amino acid identity with previously characterized drivers. Despite the vast divergence between these genes, they generally drive into >85% gametes when heterozygous. We also find three new wtf genes that suppress drive, including two that also act as autonomous drivers. Additionally, we find that wtf genes do not underlie a weak (64%) transmission bias caused by a locus or loci on chromosome 1. Finally, we find that some Wtf proteins have expression or localization patterns that are distinct from the poison and antidote proteins encoded by drivers and suppressors, suggesting some wtf genes may have non-meiotic drive functions. Overall, this work expands our understanding of the wtf gene family and the burden selfish driver genes impose on S. pombe.Article SummaryDuring gametogenesis, the two gene copies at a given locus, known as alleles, are each transmitted to 50% of the gametes (e.g. sperm). However, some alleles cheat so that they are found in more than the expected 50% of gametes, often at the expense of fertility. This selfish behavior is known as meiotic drive. Some members of the wtf gene family in the fission yeast, Schizosaccharomyces pombe, kill the gametes (spores) that do not inherit them, resulting in meiotic drive favoring the wtf allele. Other wtf genes act as suppressors of drive. However, the wtf gene family is diverse and only a small subset of the genes has been characterized. Here we analyze the functions of other members of this gene family and found eight new drivers as well as three new suppressors of drive. Surprisingly, we find that drive is relatively insensitive to changes in wtf gene sequence as highly diverged wtf genes execute gamete killing with similar efficiency. Finally, we also find that the expression and localization of some Wtf proteins are distinct from those of known drivers and suppressors, suggesting that these proteins may have non-meiotic drive functions.


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

AbstractMeiotic drive is the preferential transmission of a particular allele at a given locus during sexual reproduction. The phenomenon is observed as spore killing in a variety of fungal lineages, includingPodospora. In natural populations ofPodospora anserina, seven spore killers (Psks) have been identified through classical genetic analyses. Here we show that theSpokgene family underlie thePskspore killers. The combination of the variousSpokgenes at different chromosomal locations defines the spore killers and creates a killing hierarchy within the same population. We identify two novelSpokhomologs that are located within a complex region (theSpokblock) that reside in different chromosomal locations in given natural strains. We confirm that the individual SPOK proteins perform both the killing and resistance functions and show that these activities are dependent on distinct domains, a nuclease and a kinase domain respectively. Genomic data and phylogenetic analysis across ascomycetes suggest that theSpokgenes disperse via cross-species transfer, and evolve by duplication and diversification within several lineages.


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