Prezygotic and Postzygotic Control of Uniparental Mitochondrial DNA Inheritance in <named-content content-type="genus-species">Cryptococcus neoformans</named-content>

ABSTRACT 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 pr...

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Autores principales:	Rachana Gyawali, Xiaorong Lin
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2013
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/d672f9e91947491ab768b2ed101d931f
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spelling	oai:doaj.org-article:d672f9e91947491ab768b2ed101d931f2021-11-15T15:40:27ZPrezygotic and Postzygotic Control of Uniparental Mitochondrial DNA Inheritance in <named-content content-type="genus-species">Cryptococcus neoformans</named-content>10.1128/mBio.00112-132150-7511https://doaj.org/article/d672f9e91947491ab768b2ed101d931f2013-05-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00112-13https://doaj.org/toc/2150-7511ABSTRACT 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 α, most progeny derived from such mating events inherit the mitochondrial DNA (mtDNA) from the a parent. The homeodomain protein complex Sxi1α/Sxi2a, formed in the zygote after a-α 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 Sxi1α/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.Rachana GyawaliXiaorong LinAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 4, Iss 2 (2013)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Rachana Gyawali Xiaorong Lin Prezygotic and Postzygotic Control of Uniparental Mitochondrial DNA Inheritance in <named-content content-type="genus-species">Cryptococcus neoformans</named-content>
description	ABSTRACT 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 α, most progeny derived from such mating events inherit the mitochondrial DNA (mtDNA) from the a parent. The homeodomain protein complex Sxi1α/Sxi2a, formed in the zygote after a-α 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 Sxi1α/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.
format	article
author	Rachana Gyawali Xiaorong Lin
author_facet	Rachana Gyawali Xiaorong Lin
author_sort	Rachana Gyawali
title	Prezygotic and Postzygotic Control of Uniparental Mitochondrial DNA Inheritance in <named-content content-type="genus-species">Cryptococcus neoformans</named-content>
title_short	Prezygotic and Postzygotic Control of Uniparental Mitochondrial DNA Inheritance in <named-content content-type="genus-species">Cryptococcus neoformans</named-content>
title_full	Prezygotic and Postzygotic Control of Uniparental Mitochondrial DNA Inheritance in <named-content content-type="genus-species">Cryptococcus neoformans</named-content>
title_fullStr	Prezygotic and Postzygotic Control of Uniparental Mitochondrial DNA Inheritance in <named-content content-type="genus-species">Cryptococcus neoformans</named-content>
title_full_unstemmed	Prezygotic and Postzygotic Control of Uniparental Mitochondrial DNA Inheritance in <named-content content-type="genus-species">Cryptococcus neoformans</named-content>
title_sort	prezygotic and postzygotic control of uniparental mitochondrial dna inheritance in <named-content content-type="genus-species">cryptococcus neoformans</named-content>
publisher	American Society for Microbiology
publishDate	2013
url	https://doaj.org/article/d672f9e91947491ab768b2ed101d931f
work_keys_str_mv	AT rachanagyawali prezygoticandpostzygoticcontrolofuniparentalmitochondrialdnainheritanceinnamedcontentcontenttypegenusspeciescryptococcusneoformansnamedcontent AT xiaoronglin prezygoticandpostzygoticcontrolofuniparentalmitochondrialdnainheritanceinnamedcontentcontenttypegenusspeciescryptococcusneoformansnamedcontent
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Prezygotic and Postzygotic Control of Uniparental Mitochondrial DNA Inheritance in <named-content content-type="genus-species">Cryptococcus neoformans</named-content>

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