Genetic evidence for nonrandom sorting of mitochondria in the basidiomycete Agrocybe aegerita

Abstract

We studied mitochondrial transmission in the homobasidiomycete Agrocybe aegerita during plasmogamy, vegetative growth, and basidiocarp differentiation. Plasmogamy between homokaryons from progeny of three wild-type strains resulted in bidirectional nuclear migration, and the dikaryotization speed was dependent on the nuclear genotype of the recipient homokaryon. Little mitochondrial migration accompanied the nuclear migration. A total of 75% of the dikaryons from the fusion lines had both parental mitochondrial haplotypes (mixed dikaryons), and 25% had only a single haplotype (homoplasmic dikaryons); with some matings, there was a strong bias in favor of one parental haplotype. We demonstrated the heteroplasmic nature of mixed dikaryons by (i) isolating and subculturing apical cells in micromanipulation experiments and (ii) identifying recombinant mitochondrial genomes. This heteroplasmy is consistent with the previously reported suggestion that there is recombination between mitochondrial alleles in A. aegerita. Conversion of heteroplasmons into homoplasmons occurred (i) during long-term storage, (ii) in mycelia regenerated from isolated apical cells, and (iii) during basidiocarp differentiation. Homokaryons that readily accepted foreign nuclei were the most efficient homokaryons in maintaining their mitochondrial haplotype during plasmogamy, long-term storage, and basidiocarp differentiation. This suggests that the mechanism responsible for the nonrandom retention or elimination of a given haplotype may be related to the nuclear genotype or the mitochondrial haplotype or both.

Deletion of the sex-determining gene SXI1α enhances the spread of mitochondrial introns in Cryptococcus neoformans

“…These two processes have been observed in other species. For example, homologous mitochondrial genome recombination has been reported in the basidiomycete mushrooms Coprinus cinereus [ 30 ], Agrocybe aegerita [ 31 ] and Pleurotus ostreatus [ 32 ]. Similarly, independent transfers of HEG-associated introns have also been reported in other species including the baker’s yeast Saccharomyces cerevisiae [ 7 ], the plant fungal pathogen U. maydis [ 20 , 21 ] and the unicellular algae Chlamydomonas species [ 9 ].…”

Promiscuous mitochondria inCryptococcus gattii

“…In addition, recombination between the two types of mitochondria that were present may have resulted in mitochondrial genomes with both AFLP4/VGI and AFLP6/VGII sequences. It is important to note that recombination between mitochondria has been observed in other fungi under laboratory conditions, for example Agaricus bisporus (De la Bastide & Horgen, 2003), Agrocybe aegerita (Barroso & Labarère, 1997), Neurospora intermedia (Yang & Griffiths, 1992), Saccharomyces cerevisiae (Nakagawa et al , 1992), as well as in natural populations, for example A. aegerita (Barroso et al , 1995), Armillaria gallica (Saville et al , 1998), Candida albicans (Anderson et al , 2001; Jacobsen et al , 2008) and Neurospora crassa (Taylor et al , 1986). In addition, mitochondrial recombination has been observed in laboratory crossings of C. neoformans isolates (Toffaletti et al , 2004; Yan et al , 2007b).…”

Geographically specific heteroplasmy of mitochondrial DNA in the seaweed, Fucus serratus (Heterokontophyta: Phaeophyceae, Fucales)

“…Mitochondrial heteroplasmy has been reported in vertebrates, invertebrates, basidiomycetes and some angiosperms (Hale & Singh 1986; Barroso & LaBarere 1997; Lunt et al . 1998; Yamato & Newton 1999; Steel et al .…”