Mitochondrial inheritance in fungi

Basse, Christoph W.

doi:10.1016/j.mib.2010.09.003

Cited by 114 publications

(109 citation statements)

References 58 publications

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“…Moreover, this study has revealed further insight into the requirement of mitochondrial fission for mitophagy. Lga2 is decisive for uniparental mtDNA inheritance in U. maydis (2,8). Future studies need to address whether LTM plays an underlying role either directly or to dispose of affected organelles having lost their DNA.…”

Section: Discussionmentioning

confidence: 99%

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The Mitochondrial Dnm1-Like Fission Component Is Required for lga2 -Induced Mitophagy but Dispensable for Starvation-Induced Mitophagy in Ustilago maydis

2012

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Selective elimination of mitochondria by autophagy (mitophagy) is a crucial developmental process to dispose of disintegrated or superflous organelles. However, little is known about underlying regulatory mechanisms. We have investigated mitophagy in response to conditional overexpression of the a2 mating-type locus gene lga2, which encodes a small mitochondrial protein critically involved in uniparental mitochondrial DNA inheritance during sexual development of Ustilago maydis. In this study, we show that conditional overexpression of lga2 efficiently triggers mitophagy that is dependent on atg8 and atg11, consistent with selective autophagy. lga2-triggered mitophagy is preceded by mitochondrial dysfunction, including depletion of mitochondrial RNA transcripts, and is mechanistically distinct from starvation-induced mitophagy despite a common requirement for atg11. In particular, lga2-triggered mitophagy strongly depends on the mitochondrial fission factor Dnm1, but it is only slightly affected by N-acetylcysteine, which is an inhibitor of starvation-induced mitophagy. To further delineate the role of mitochondrial fission, we analyzed lga2 effects in ⌬fis1 mutants. This revealed that mitochondrial fragmentation was only attenuated and mitophagy was largely unaffected. In further support of a Fis1-independent role for Dnm1, mitochondrial association of green fluorescent protein-tagged Dnm1 as well as Dnm1-opposed mitochondrial fusion during sexual development were fis1 independent. In conclusion, our results specify the role of the mitochondrial fission factor Dnm1 in mitophagy and uncover differences between mitophagy pathways in the same cellular system.

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Section: Discussionmentioning

confidence: 99%

“…Recently, we identified the mitochondrial protein Lga2 as a central component of uniparental mtDNA inheritance in the maize smut fungus U. maydis (2,8). The lga2 gene resides on the a2 mating-type locus and is highly upregulated during sexual development in response to formation of an active b transcription factor complex in dikaryotic cells (3,6,41).…”

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confidence: 99%

The Mitochondrial Dnm1-Like Fission Component Is Required for lga2 -Induced Mitophagy but Dispensable for Starvation-Induced Mitophagy in Ustilago maydis

2012

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“…Two other species of fungi with UPI linked to their mating type alleles are worth comparing with Phycomyces (8). In the first, Ustilago maydis, the pheromone MAT locus controls uniparental inheritance; however, this is mediated by two genes within the locus, neither of which is required for pheromone biosynthesis or in determining the cell type (17,18).…”

Section: Resultsmentioning

confidence: 99%

“…Similarly, some basidiomycete mushroom species initiate their sexual cycle through the fusion of equally sized cells, and depending on the species they can exhibit the inheritance of the mitochondrial genome from just one or either parent. In species with uniparental inheritance, the complex genetic makeup of their mating type systems have prevented implicating sex-determining genes directly, with some exceptions that are discussed below (7,8). Phycomyces blakesleeanus is a fungus in the subphylum Mucoromycotina that is a distant relative of the ascomycete and basidiomycete species.…”

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confidence: 99%

Sex Determination Directs Uniparental Mitochondrial Inheritance in Phycomyces

Shakya

Idnurm

2014

Eukaryot Cell

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Uniparental inheritance (UPI) of mitochondria is common among eukaryotes. The underlying molecular basis by which the sexes of the parents control this non-Mendelian pattern of inheritance is yet to be fully understood. Two major factors have complicated the understanding of the role of sex-specific genes in the UPI phenomenon: in many cases (i) fusion occurs between cells of unequal size or (ii) mating requires a large region of the genome or chromosome that includes genes unrelated to sex determination. The fungus Phycomyces blakesleeanus is a member of the Mucoromycotina and has a simple mating type locus encoding only one high-mobility group (HMG) domain protein, and mating occurs by fusion of isogamous cells, thus providing a model system without the limitations mentioned above. Analysis of more than 250 progeny from a series of genetic crosses between wild-type strains of Phycomyces revealed a correlation between the individual genes in the mating type locus and UPI of mitochondria. Inheritance is from the plus (؉) sex type and is associated with degradation of the mtDNA from the minus (؊) parent. These findings suggest that UPI can be directly controlled by genes that determine sex identity, independent of cell size or the complexity of the genetic composition of a sex chromosome.

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“…In the case of mtDNA, uniparental inheritance is not surprising, as even in fungi that have biparental mitochondrial inheritance, mitochondria quickly become homoplasmic (Basse 2010). However, it is more challenging to explain the single-parent nature of the multicopy, chromosomally encoded rDNA.…”

Section: Discussionmentioning

confidence: 99%

Epichloë hybrida, sp. nov., an emerging model system for investigating fungal allopolyploidy

et al. 2017

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Endophytes of the genus Epichloë (Clavicipitaceae, Ascomycota) frequently occur within coolseason grasses and form interactions with their hosts that range from mutualistic to antagonistic. Many Epichloë species have arisen via interspecific hybridization, resulting in species with two or three subgenomes that retain all or nearly all of their original parental genomes, a process termed allopolyploidization. Here, we characterize Epichloë hybrida, sp. nov., a mutualistic species that has increasingly become a model system for investigating allopolyploidy in fungi. The Epichloë species so far identified as the closest known relatives of the two progenitors of E. hybrida are E. festucae var. lolii and E. typhina. We confirm that the nuclear genome of E. hybrida contains two homeologs of most protein-coding genes from E. festucae and E. typhina, with genome-wide gene expression analysis indicating a slight bias in overall gene expression from the E. typhina subgenome. Mitochondrial DNA is detectable only from E. festucae, whereas ribosomal DNA is detectable only from E. typhina. Inheriting ribosomal DNA from just one parent might be expected to preferentially favor interactions with ribosomal proteins from the same parent, but we find that ribosomal protein genes from both parental subgenomes are nearly all expressed equally in E. hybrida. Finally, we provide a comprehensive set of resources for this model system that are intended to facilitate further study of fungal hybridization by other researchers. ARTICLE HISTORY

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Mitochondrial inheritance in fungi

Cited by 114 publications

References 58 publications

The Mitochondrial Dnm1-Like Fission Component Is Required for lga2 -Induced Mitophagy but Dispensable for Starvation-Induced Mitophagy in Ustilago maydis

The Mitochondrial Dnm1-Like Fission Component Is Required for lga2 -Induced Mitophagy but Dispensable for Starvation-Induced Mitophagy in Ustilago maydis

Sex Determination Directs Uniparental Mitochondrial Inheritance in Phycomyces

Epichloë hybrida, sp. nov., an emerging model system for investigating fungal allopolyploidy

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