When and why are mitochondria paternally inherited?

Munasinghe, Manisha; Ågren, J. Arvid

doi:10.1016/j.gde.2023.102053

Cited by 11 publications

(10 citation statements)

References 105 publications

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“…For this purpose it is useful that many rare conifers already grow and reproduce in nearby botanical gardens and pinetums. Knowing the “hows and whys” (Mogensen 1996 ) of uniparental cytoplasmic inheritance is an interesting evolutionary question in its own right (Munasinghe and Ågren ( 2023 ) and conifers seem an excellent study system. Many conifers are vulnerable, threatened in their natural populations or are relicts from families that dominated the world millions of years ago.…”

Section: Discussionmentioning

confidence: 99%

Paternal Inheritance of Mitochondrial DNA May Lead to Dioecy in Conifers

de Jong,

Shmida

2024

Acta Biotheor

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In angiosperms cytoplasmic DNA is typically passed on maternally through ovules. Genes in the mtDNA may cause male sterility. When male-sterile (female) cytotypes produce more seeds than cosexuals, they pass on more copies of their mtDNA and will co-occur with cosexuals with a neutral cytotype. Cytoplasmic gynodioecy is a well-known phenomenon in angiosperms, both in wild and crop plants. In some conifer families (e.g. Pinaceae) mitochondria are also maternally inherited. However in some other families (e.g. Taxaceae and Cupressaceae) mtDNA is paternally inherited through the pollen. With paternal mtDNA inheritance, male cytotypes that produce more pollen than cosexuals are expected to co-occur with cosexuals. This is uncharted territory. An ESS model shows that the presence of male cytotypes selects for more female allocation in the cosexual, i.e. for sexual specialisation. An allele that switches sex from male to female can then invade. This leads to rapid loss of the neutral cytotype of the cosexual, fixation of the male cytotype and dioecy with 50% males and 50% females. The models suggest that paternal inheritance of mtDNA facilitates the evolution dioecy. Consistent with this hypothesis the Pinaceae are 100% monoecious, while dioecy is common in the Taxaceae family and in the genus Juniperus (Cupressaceae). However, no reliable data are yet available on both mode of inheritance of mtDNA and gender variation of the same species. When cosexuals benefit from reproductive assurance (high selfing rate, low inbreeding depression, low fertilisation) they maintain themselves next to males and females. This predicted pattern with three sex types present in the same population is observed in conifers in nature.

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Section: Discussionmentioning

confidence: 99%

Paternal Inheritance of Mitochondrial DNA May Lead to Dioecy in Conifers

de Jong,

Shmida

2024

Acta Biotheor

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“…In cases where mtDNA is inherited maternally, the "mother's curse" effect can lead to the accumulation of mutations which are damaging to males but are neutral or beneficial for females (Gemmell et al, 2004). Alternative inheritance patterns can give rise to a similar "father's curse" (Munasinghe & Ågren, 2023). Mitonuclear interactions are a mechanism by which the curse can be resolved (Connallon et al, 2018).…”

Section: How Do Organisms Maintain the Function Of The Genes They Ret...mentioning

confidence: 99%

“…The inheritance patterns of mtDNA in a given species contribute to its ability to maintain function and reduce genomic conflicts (Cosmides & Tooby, 1981;Greiner et al, 2015;Munasinghe & Ågren, 2023). Strictly maternal inheritance avoids generating heteroplasmy by mixing parental mtDNA contributions, and hence limits the negative consequences of mixed mtDNA (Lane, 2012;Latorre-Pellicer et al, 2019;Sharpley et al, 2012).…”

Section: Inheritance and Exchangementioning

confidence: 99%

“…If some paternal contribution is allowed, and recombination supported (Birky, 1995;Camus et al, 2022;Greiner et al, 2015), heterozygosity can be maintained in a population and more rapid adaptation to changing environments may be supported (Radzvilavicius & Johnston, 2020). Purely paternal inheritance, rarely observed, has been suggested to support strong selection through a severe bottleneck (Havey, 2017;Munasinghe & Ågren, 2023) Some species may support horizontal gene transfer of mtDNA on various scales, from the transfer of individual mitochondria (and hence mtDNA) between cells, to large-scale exchange of mtDNA content between individuals. Introgression -where mitochondrial content from another organism not involved in the nuclear reproductive process -has been naturally observed in algae (Neiva et al, 2010), and is a key component of human therapies targeting the inheritance of mtDNA disease (Burgstaller et al, 2015;Craven et al, 2010;Wolf et al, 2015).…”

Section: Inheritance and Exchangementioning

confidence: 99%

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Evolution and maintenance of mtDNA gene content across eukaryotes

Veeraragavan,

Johansen,

Johnston

2024

Preprint

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Across eukaryotes, most genes required for mitochondrial function have been transferred to, or otherwise acquired by, the nucleus. Encoding genes in the nucleus has many advantages. So why do mitochondria retain any genes at all? Why does the set of mtDNA genes vary so much across different species? And how do species maintain functionality in the mtDNA genes they do retain? In this review we will discuss some possible answers to these questions, attempting a broad perspective across eukaryotes. We hope to cover some interesting features which may be less familiar from the perspective of particular species, including the ubiquity of recombination outside bilaterian animals, encrypted chainmail-like mtDNA, single genes split over multiple mtDNA chromosomes, triparental inheritance, gene transfer by grafting, gain of mtDNA recombination factors, social networks of mitochondria, and the role of mtDNA disease in feeding the world. We will discuss a unifying picture where organismal ecology and gene-specific features together influence whether organism X retains mtDNA gene Y, and where ecology and development together determine which strategies, importantly including recombination, are used to maintain the mtDNA genes that are retained.

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“…One key contributor to this divergence is genetic conflict (Werren & Beukeboom, 1998; Schenkel et al, under review). Different genetic elements within an individual segregate to and from males and females in different ways (Haig et al ., 2014); autosomes move freely from parents to offspring of both sexes, whereas Y-chromosomes segregate exclusively from fathers to sons, and cytoplasmic material inherits almost exclusively through the maternal route (but see Munasinghe & Ågren, 2023). Genetic elements that are transmitted at unequal rates to and from individuals will prefer to bias sex determination towards that sex through which they are transmitted more often (Cosmides & Tooby, 1981; Werren & Beukeboom, 1998).…”

Section: Introductionmentioning

confidence: 99%

Quantifying internal conflicts and their threats to organismal form and fitness

Schenkel,

Patten,

Ågren

2024

Preprint

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Evolutionary biologists often treat organisms as both fitness-maximizing agents and as the primary level at which adaptation manifests. Yet, genes and cells may also seek to optimize their fitness by distorting the Mendelian rules of transmission or by influencing organismal traits for their own benefit. Organismal form and fitness are therefore threatened from within by selfish genes and cells. However, to what extent such internal conflicts actually harm individual organisms and threaten our concept of the organism as the sole bearer of adaptation remains unclear. We introduce a mathematical framework to capture the threat posed by internal conflicts and develop two metrics to measure their various forms of harm. We name these metrics fitness unity and trait unity, and use them to refer to the threats posed by internal conflicts to an organism's role as the optimizing agent and the strategy wielded to achieve that optimization, respectively. We apply our framework to two examples of internal conflicts, genomic imprinting and sex ratio distortion, to illustrate how such harms from internal conflict may be quantified. We conclude by discussing the conditions under which internal conflict becomes sufficiently disruptive to organisms that it no longer makes sense to think of them as unified fitness-maximizing agents, but instead as adaptive compromises of multiple competing sub-agents.

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When and why are mitochondria paternally inherited?

Cited by 11 publications

References 105 publications

Paternal Inheritance of Mitochondrial DNA May Lead to Dioecy in Conifers

Paternal Inheritance of Mitochondrial DNA May Lead to Dioecy in Conifers

Evolution and maintenance of mtDNA gene content across eukaryotes

Quantifying internal conflicts and their threats to organismal form and fitness

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