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Uniparental inheritance of chloroplast DNA is strict in the isogamous volvocalean Gonium.

ABSTRACT: A problem has remained unresolved regarding the exceptions to the unilateral inheritance of chloroplast DNA (cpDNA) from MT+/female in Chlamydomonas and other volvocaleans demonstrated by the previous genetic analyses. For identification of the parental types of cpDNA, these studies used parents that have differences in restriction fragment length polymorphisms and exhibit partial sexual incompatibility.In the present study, we used sexually compatible parents of the isogamous colonial volvocalean Gonium maiaprilis that seemed an ideal species to identify the pattern of cpDNA inheritance based on the length difference in the putative group I intron interrupted in the Rubisco large subunit gene and objective identification of mating types by the presence or absence of the minus-dominance (MID) gene. We examined patterns of inheritance of cpDNA and presence/absence of a MID ortholog (GmMID) in 107 F(1) progeny of G. maiaprilis that were obtained by inducing germination of separated single zygotes. The results demonstrated no exception of the uniparental inheritance of cpDNA from the MT+ parent (lacking GmMID) in sexually compatible or genetically less divergent strains of G. maiaprilis.The present data suggest that the uniparental inheritance of cpDNA is likely more strict in crossings of less diverged strains or sexually compatible parental volvocaleans, and some genetic inconsistency between the parents may cause exceptional uniparental inheritance of cpDNA.

SUBMITTER: Setohigashi Y

PROVIDER: S-EPMC3085477 | biostudies-literature | 2011 Apr

REPOSITORIES: biostudies-literature

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Uniparental inheritance of chloroplast DNA is strict in the isogamous volvocalean Gonium.

Setohigashi Yuka Y Hamaji Takashi T Hayama Mahoko M Matsuzaki Ryo R Nozaki Hisayoshi H

PloS one 20110429 4

<h4>Background</h4>A problem has remained unresolved regarding the exceptions to the unilateral inheritance of chloroplast DNA (cpDNA) from MT+/female in Chlamydomonas and other volvocaleans demonstrated by the previous genetic analyses. For identification of the parental types of cpDNA, these studies used parents that have differences in restriction fragment length polymorphisms and exhibit partial sexual incompatibility.<h4>Methodology/principal findings</h4>In the present study, we used sexua ...[more]

PMID: 21559302

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Project description:UNLABELLED:Uniparental inheritance of mitochondrial DNA is pervasive in nonisogamic higher eukaryotes during sexual reproduction, and postzygotic and/or prezygotic factors are shown to be important in ensuring such an inheritance pattern. Although the fungus Cryptococcus neoformans undergoes sexual production with isogamic partners of opposite mating types a and ?, most progeny derived from such mating events inherit the mitochondrial DNA (mtDNA) from the a parent. The homeodomain protein complex Sxi1?/Sxi2a, formed in the zygote after a-? cell fusion, was previously shown to play a role in this uniparental mtDNA inheritance. Here, we defined the timing of the establishment of the mtDNA inheritance pattern during the mating process and demonstrated a critical role in determining the mtDNA inheritance pattern by a prezygotic factor, Mat2. Mat2 is the key transcription factor that governs the pheromone sensing and response pathway, and it is critical for the early mating events that lead to cell fusion and zygote formation. We show that Mat2 governs mtDNA inheritance independently of the postzygotic factors Sxi1?/Sxi2a, and the cooperation between these prezygotic and postzygotic factors helps to achieve stricter uniparental mitochondrial inheritance in this eukaryotic microbe. IMPORTANCE:Mitochondrial DNA is inherited uniparentally from the maternal parent in the majority of eukaryotes. Studies done on higher eukaryotes such as mammals have shown that the transmission of parental mitochondrial DNA is controlled at both the prefertilization and postfertilization stages to achieve strict uniparental inheritance. However, the molecular mechanisms underlying such uniparental mitochondrial inheritance have been investigated in detail mostly in anisogamic multicellular eukaryotes. Here, we show that in a simple isogamic microbe, Cryptococcus neoformans, the mitochondrial inheritance is controlled at the prezygotic level as well as the postzygotic level by regulators that are critical for sexual development. Furthermore, the cooperation between these two levels of control ensures stricter uniparental mitochondrial inheritance, echoing what has been observed in higher eukaryotes. Thus, the investigation of uniparental mitochondrial inheritance in this eukaryotic microbe could help advance our understanding of the convergent evolution of this widespread phenomenon in the eukaryotic domain.

Dataset Information

Uniparental inheritance of chloroplast DNA is strict in the isogamous volvocalean Gonium.

Publications

Uniparental inheritance of chloroplast DNA is strict in the isogamous volvocalean Gonium.

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