The Selfish<i>Segregation Distorter</i>Gene Complex of<i>Drosophila melanogaster</i>

Larracuente, Amanda M.; Presgraves, Daven C.

doi:10.1534/genetics.112.141390

Cited by 229 publications

(297 citation statements)

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“…Other meiotic drivers are known to favor their own transmission through DNA condensation perturbation, and sometimes the interaction with a specific satellite DNA (26)(27)(28). Similarly, the discrete distribution of HP1D2 on the Y chromosome suggests an impact of this protein on the chromatin organization of specific repeated sequences.…”

Section: Resultsmentioning

confidence: 99%

Rapid evolution of a Y-chromosome heterochromatin protein underlies sex chromosome meiotic drive

Helleu

Gérard

Dubruille

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Sex chromosome meiotic drive, the non-Mendelian transmission of sex chromosomes, is the expression of an intragenomic conflict that can have extreme evolutionary consequences. However, the molecular bases of such conflicts remain poorly understood. Here, we show that a young and rapidly evolving X-linked heterochromatin protein 1 (HP1) gene, HP1D2, plays a key role in the classical Paris sex-ratio (SR) meiotic drive occurring in Drosophila simulans. Driver HP1D2 alleles prevent the segregation of the Y chromatids during meiosis II, causing female-biased sex ratio in progeny. HP1D2 accumulates on the heterochromatic Y chromosome in male germ cells, strongly suggesting that it controls the segregation of sister chromatids through heterochromatin modification. We show that Paris SR drive is a consequence of dysfunctional HP1D2 alleles that fail to prepare the Y chromosome for meiosis, thus providing evidence that the rapid evolution of genes controlling the heterochromatin structure can be a significant source of intragenomic conflicts. meiotic drive | intragenomic conflict | heterochromatin | sex chromosomes

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Section: Resultsmentioning

confidence: 99%

Rapid evolution of a Y-chromosome heterochromatin protein underlies sex chromosome meiotic drive

Helleu

Gérard

Dubruille

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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“…Single-locus segregation distorters usually rely on the tight genetic linkage of several interacting genes, leading to their transmission as self-sufficient loci. Such loci have been documented in animals, especially in Drosophila (Orr et al 2007;Larracuente and Presgraves 2012), and in Ascomycetes (Turner and Perkins 1979;Raju 1994). In plants, after the first description of a PK in a hybrid between two Solanum species (Cameron and Moav 1957), gamete killers (most often PKs) have been reported, especially in hybrids between cultivated plants and their wild relatives, where they often constitute obstacles to the breeding of desirable traits (Maan 1975;Sano 1990).…”

Section: Discussionmentioning

confidence: 99%

Genomic Conflicts that Cause Pollen Mortality and Raise Reproductive Barriers inArabidopsis thaliana

et al. 2016

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Species differentiation and the underlying genetics of reproductive isolation are central topics in evolutionary biology. Hybrid sterility is one kind of reproductive barrier that can lead to differentiation between species. Here, we analyze the complex genetic basis of the intraspecific hybrid male sterility that occurs in the offspring of two distant natural strains of Arabidopsis thaliana, Shahdara and Mr-0, with Shahdara as the female parent. Using both classical and quantitative genetic approaches as well as cytological observation of pollen viability, we demonstrate that this particular hybrid sterility results from two causes of pollen mortality. First, the Shahdara cytoplasm induces gametophytic cytoplasmic male sterility (CMS) controlled by several nuclear loci. Second, several segregation distorters leading to allele-specific pollen abortion (pollen killers) operate in hybrids with either cytoplasm. The complete sterility of the hybrid with the Shahdara cytoplasm results from the genetic linkage of the two causes of pollen mortality, i.e., CMS nuclear determinants and pollen killers. Furthermore, natural variation at these loci in A. thaliana is associated with different malesterility phenotypes in intraspecific hybrids. Our results suggest that the genomic conflicts that underlie segregation distorters and CMS can concurrently lead to reproductive barriers between distant strains within a species. This study provides a new framework for identifying molecular mechanisms and the evolutionary history of loci that contribute to reproductive isolation, and possibly to speciation. It also suggests that two types of genomic conflicts, CMS and segregation distorters, may coevolve in natural populations.

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“…Although we cannot rule out that other mechanisms may cause the apparent nonrandom association between P/R (A) and HD (B) loci in L. scottii, we highlight two possibilities in particular. First, a meiotic drive mechanism (Larracuente and Presgraves 2012;Grognet et al 2014) could be in effect, whereby each equal-to-parental pair of P/R-and HD-harboring chromosomes tend to segregate together. Second, the viability and/or fertility of cells carrying associations of MAT alleles reciprocal to those of their parents could be compromised.…”

Section: Genotypic Analysis Of L Scottii Meiotic Progenymentioning

confidence: 99%

Evolution of Mating Systems in Basidiomycetes and the Genetic Architecture Underlying Mating-Type Determination in the YeastLeucosporidium scottii

et al. 2015

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In most fungi, sexual reproduction is bipolar; that is, two alternate sets of genes at a single mating-type (MAT) locus determine two mating types. However, in the Basidiomycota, a unique (tetrapolar) reproductive system emerged in which sexual identity is governed by two unlinked MAT loci, each of which controls independent mechanisms of self/nonself recognition. Tetrapolar-to-bipolar transitions have occurred on multiple occasions in the Basidiomycota, resulting, for example, from linkage of the two MAT loci into a single inheritable unit. Nevertheless, owing to the scarcity of molecular data regarding tetrapolar systems in the earliest-branching lineage of the Basidiomycota (subphylum Pucciniomycotina), it is presently unclear if the last common ancestor was tetrapolar or bipolar. Here, we address this question, by investigating the mating system of the Pucciniomycotina yeast Leucosporidium scottii. Using whole-genome sequencing and chromoblot analysis, we discovered that sexual reproduction is governed by two physically unlinked gene clusters: a multiallelic homeodomain (HD) locus and a pheromone/receptor (P/R) locus that is biallelic, thereby dismissing the existence of a third P/R allele as proposed earlier. Allele distribution of both MAT genes in natural populations showed that the two loci were in strong linkage disequilibrium, but independent assortment of MAT alleles was observed in the meiotic progeny of a test cross. The sexual cycle produces fertile progeny with similar proportions of the four mating types, but approximately 2/3 of the progeny was found to be nonhaploid. Our study adds to others in reinforcing tetrapolarity as the ancestral state of all basidiomycetes.KEYWORDS sexual reproduction; mating type; mating-type determination; fungi; Basidiomycota S EXUAL reproduction has a pivotal role in the biology of many eukaryotes and is likely a defining evolutionary innovation of this lineage (Dacks and Roger 1999;Goodenough and Heitman 2014). In addition to promoting genetic variation, required for adaptation to fluctuating environments and longterm survival, sexual reproduction in many fungal species, in particular, has a central role in pathogenic development (Bakkeren et al. 2008;Nadal et al. 2008;Heitman 2010;Heitman et al. 2014). It is thus not surprising that recent advances in genome sequencing have revealed that most fungal species have retained the machinery for sexual reproduction and meiosis (Halary et al. 2011;Dyer and O'Gorman 2012;Gioti et al. 2013;Heitman et al. 2014). However, this resilience to keep sexual competence intact comes with an extremely dynamic evolution of sexual behaviors and mating type-determining mechanisms, which may influence important evolutionary and ecological processes, such as adaptation and speciation (Billiard et al. 2011;Heitman et al. 2013;Nieuwenhuis et al. 2013).In the phylum Basidiomycota, sexual reproduction is often dictated by two independent sets of mating-type (MAT)-specific genes that control different stages of the sexual cycle. These...

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The SelfishSegregation DistorterGene Complex ofDrosophila melanogaster

Cited by 229 publications

References 119 publications

Rapid evolution of a Y-chromosome heterochromatin protein underlies sex chromosome meiotic drive

Rapid evolution of a Y-chromosome heterochromatin protein underlies sex chromosome meiotic drive

Genomic Conflicts that Cause Pollen Mortality and Raise Reproductive Barriers inArabidopsis thaliana

Evolution of Mating Systems in Basidiomycetes and the Genetic Architecture Underlying Mating-Type Determination in the YeastLeucosporidium scottii

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