The Pheromone and Pheromone Receptor Mating-Type Locus Is Involved in Controlling Uniparental Mitochondrial Inheritance in Cryptococcus.

Mitochondria are inherited uniparentally during sexual reproduction in the majority of eukaryotic species studied, including humans, mice, and nematodes, as well as many fungal species. Mitochondrial uniparental inheritance (mito-UPI) could be beneficial in that it avoids possible genetic conflicts...

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Publicado en:Genetics Vol. 214; no. 3; pp. 703 - 718
Autores principales: Sheng Sun, Ci Fu, Ianiri, Giuseppe, Heitman, Joseph
Formato: pictorial research tables/charts Journal Article
Publicado: Oxford University Press / USA Mar2020
Acceso en línea:Ver este registro en EBSCOhost
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      dt: Mar2020
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      pub: Oxford University Press / USA
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        10.1534/genetics.119.302824
        142162564
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        atl: The Pheromone and Pheromone Receptor Mating-Type Locus Is Involved in Controlling Uniparental Mitochondrial Inheritance in Cryptococcus.
      aug:
        au:
          Sheng Sun
          Ci Fu
          Ianiri, Giuseppe
          Heitman, Joseph
        affil: Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, North Carolina 27710
      sug:
        subj:
          Biological Factors Metabolism
          Receptors, Cell Surface Metabolism
          Alleles
          Mitochondria Metabolism
          Cryptococcus Metabolism
          Reproduction
          Genes
          Transcription Factors Metabolism
          Cell Movement
          Cell Nucleus Physiology
          Zygote
      ab: Mitochondria are inherited uniparentally during sexual reproduction in the majority of eukaryotic species studied, including humans, mice, and nematodes, as well as many fungal species. Mitochondrial uniparental inheritance (mito-UPI) could be beneficial in that it avoids possible genetic conflicts between organelles with different genetic backgrounds, as recently shown in mice, and it could prevent the spread of selfish genetic elements in the mitochondrial genome. Despite the prevalence of observed mito-UPI, the underlying mechanisms and the genes involved in controlling this non-Mendelian inheritance are poorly understood in many species. In Cryptococcus neoformans, a human pathogenic basidiomyceteous fungus, mating types (MATα and MATa) are defined by alternate alleles at the single MAT locus that evolved from fusion of the two MAT loci (P/R encoding pheromones and pheromone receptors, and HD encoding homeodomain transcription factors) that are the ancestral state in the basidiomycota. Mitochondria are inherited uniparentally from the MATa parent in C. neoformans, and this requires the SXI1a and SXI2a HD factors encoded by MAT. However, there is evidence that additional genes contribute to the control of mito-UPI in Cryptococcus. Here, we show that in C. amylolentus, a sibling species of C. neoformans with unlinked P/R and HD MAT loci, mito-UPI is controlled by the P/R locus and is independent of the HD locus. Consistently, by replacing the MATa alleles of the pheromones (MF) and pheromone receptor (STE3) with the MATa alleles, we show that these P/R locus-defining genes indeed affect mito-UPI in C. neoformans during sexual reproduction. Additionally, we show that during early stages of C. neoformans sexual reproduction, conjugation tubes are always produced by the MATa cells, resulting in unidirectional migration of the MATα nucleus into the MATa cell during zygote formation. This process is controlled by the P/R locus and could serve to physically restrict movement of MATα mitochondria in the zygotes, and thereby contribute to mito-UPI. We propose a model in which both physical and genetic mechanisms function in concert to prevent the coexistence of mitochondria from the two parents in the zygote, and subsequently in the meiotic progeny, thus ensuring mito-UPI in pathogenic Cryptococcus, as well as in closely related nonpathogenic species. The implications of these findings are discussed in the context of the evolution of mito-UPI in fungi and other more diverse eukaryotes.
      pubtype: Academic Journal
      doctype:
        pictorial
        research
        tables/charts
        Journal Article
      ougenre: Article
    language: English
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