Maternal inheritance of mitochondria: multipolarity, multiallelism and hierarchical transmission of mitochondrial DNA in the true slime mold Physarum polycephalum

Abstract

Direct evidence of digestion of paternal mitochondrial DNA (mtDNA) has been found in the true slime mold Physarum polycephalum. This is the first report on the selective digestion of mtDNA inside the zygote, and is striking evidence for the mechanism of maternal inheritance of mitochondria. Moreover, two mitochondrial nuclease activities were detected in this organism as-candidates for the nucleases responsible for selective digestion of mtDNA. In the true slime mold, there is an additional-feature of the uniparental inheritance of mitochondria.Although mitochondria are believed to be inherited from the maternal lineage in nearly all eukaryotes, the mating types of the true slime mold P. polycephalum is not restricted to two: there are three mating loci--matA, matB,and matC--and these loci have 16, 15, and 3 alleles,-respectively. Interestingly, the transmission patterns of mtDNA are determined by the matA locus, in a hierarchical-fashion (matA hierarchy) as follows: matA7[matA2[matA11[matA12[matA15/matA16[matA1[matA6.The strain possessing the higher status of matA would be the mtDNA donor in crosses. Furthermore, we have found that some crosses showed biparental inheritance of mitochondria.This review describes the phenomenon of hierarchical transmission of mtDNA in true slime molds, and discusses the presumed molecular mechanism of maternal and biparental inheritance.

Origins of Eukaryotic Sexual Reproduction

“…Although there is as yet no information on the molecules that exert mating-type UP control in most systems, the selective destruction of one set of organelle genomes has been shown in several disparate radiations, including the chlorophytes Gonium (Setohigashi et al 2011) and Bryopsis (Kuroiwa and Hori 1986), the ulvophyte Ulva (Kagami et al 2008), brown algae (Motomura et al 2010), the slime mold Physarum (Moriyama and Kawano 2010), Drosophila (DeLuca and O'Farrell 2012), the fish Orizias (Nishimura et al 2006), and the mouse (Kaneda et al 1995;Kuroiwa 2010;Sato and Sato 2013). Notably, in the vertebrate examples, the sperm organelles enter the egg but are quickly and selectively eliminated in the zygote in a species-specific fashion (Kaneda et al 1995).…”

Evolution of uni- and bifactorial sexual compatibility systems in fungi

“…Bifactorial incompatibility systems are not restricted to fungi; instead, they have also been found in different plant species of the Poaceae family (Klaas et al, 2011), in different tristylous plants (Barrett and Shore, 2008), in tunicates (Harada et al, 2008) and in the social amoeba of the genus Physarum (Moriyama and Kawano, 2010). Of these bifactorial systems, only that of the social amoeba is similar to that of the Basidiomycetes in that compatibility occurs only when both loci carry different alleles.…”

Mitochondrial fusion and inheritance of the mitochondrial genome

“…Mitochondria are inherited strictly maternally in many species, as described above. Uniparental inheritance of mitochondria has also been reported in P. polycephalum Meland et al 1991;Moriyama and Kawano 2003; reviewed by Moriyama and Kawano (2010) in this issue). Because more than two mating types exist in P. polycephalum, the pattern of mitochondrial inheritance is complex.…”

“…Because more than two mating types exist in P. polycephalum, the pattern of mitochondrial inheritance is complex. The mitochondria are transmitted uniparentally, in general, according to their relative sexualities, as determined by the mating-type locus matA, which has at least 13 alleles (see Moriyama and Kawano (2010) in this issue). The matA alleles can be ranked in a linear hierarchy to determine which parent loses its mitochondrial genome.…”