scholarly journals Atypical mitochondrial inheritance patterns in eukaryotes

Genome ◽  
2015 ◽  
Vol 58 (10) ◽  
pp. 423-431 ◽  
Author(s):  
Sophie Breton ◽  
Donald T. Stewart
Keyword(s):  
Sex Determination ◽  
Molecular Mechanisms ◽  
Maternal Inheritance ◽  
Uniparental Inheritance ◽  
Mitochondrial Inheritance ◽  
Doubly Uniparental Inheritance ◽  
Inheritance Patterns ◽  
Sexual Systems ◽  
Evolutionary Forces ◽  
Mtdna Inheritance

Mitochondrial DNA (mtDNA) is predominantly maternally inherited in eukaryotes. Diverse molecular mechanisms underlying the phenomenon of strict maternal inheritance (SMI) of mtDNA have been described, but the evolutionary forces responsible for its predominance in eukaryotes remain to be elucidated. Exceptions to SMI have been reported in diverse eukaryotic taxa, leading to the prediction that several distinct molecular mechanisms controlling mtDNA transmission are present among the eukaryotes. We propose that these mechanisms will be better understood by studying the deviations from the predominating pattern of SMI. This minireview summarizes studies on eukaryote species with unusual or rare mitochondrial inheritance patterns, i.e., other than the predominant SMI pattern, such as maternal inheritance of stable heteroplasmy, paternal leakage of mtDNA, biparental and strictly paternal inheritance, and doubly uniparental inheritance of mtDNA. The potential genes and mechanisms involved in controlling mitochondrial inheritance in these organisms are discussed. The linkage between mitochondrial inheritance and sex determination is also discussed, given that the atypical systems of mtDNA inheritance examined in this minireview are frequently found in organisms with uncommon sexual systems such as gynodioecy, monoecy, or andromonoecy. The potential of deviations from SMI for facilitating a better understanding of a number of fundamental questions in biology, such as the evolution of mtDNA inheritance, the coevolution of nuclear and mitochondrial genomes, and, perhaps, the role of mitochondria in sex determination, is considerable.

scholarly journals Chloroplast competition is controlled by lipid biosynthesis in evening primroses

2019 ◽  
Vol 116 (12) ◽  
pp. 5665-5674 ◽  
Author(s):  
Johanna Sobanski ◽  
Patrick Giavalisco ◽  
Axel Fischer ◽  
Julia M. Kreiner ◽  
Dirk Walther ◽  
...  
Keyword(s):  
Molecular Mechanisms ◽  
Regulatory Region ◽  
Nuclear Genome ◽  
Lipid Biosynthesis ◽  
Metabolic Phenotype ◽  
Uniparental Inheritance ◽  
Biparental Inheritance ◽  
Turnover Rates ◽  
Evening Primrose ◽  
Evolutionary Forces

In most eukaryotes, organellar genomes are transmitted preferentially by the mother, but molecular mechanisms and evolutionary forces underlying this fundamental biological principle are far from understood. It is believed that biparental inheritance promotes competition between the cytoplasmic organelles and allows the spread of so-called selfish cytoplasmic elements. Those can be, for example, fast-replicating or aggressive chloroplasts (plastids) that are incompatible with the hybrid nuclear genome and therefore maladaptive. Here we show that the ability of plastids to compete against each other is a metabolic phenotype determined by extremely rapidly evolving genes in the plastid genome of the evening primroseOenothera. Repeats in the regulatory region ofaccD(the plastid-encoded subunit of the acetyl-CoA carboxylase, which catalyzes the first and rate-limiting step of lipid biosynthesis), as well as inycf2(a giant reading frame of still unknown function), are responsible for the differences in competitive behavior of plastid genotypes. Polymorphisms in these genes influence lipid synthesis and most likely profiles of the plastid envelope membrane. These in turn determine plastid division and/or turnover rates and hence competitiveness. This work uncovers cytoplasmic drive loci controlling the outcome of biparental chloroplast transmission. Here, they define the mode of chloroplast inheritance, as plastid competitiveness can result in uniparental inheritance (through elimination of the “weak” plastid) or biparental inheritance (when two similarly “strong” plastids are transmitted).

scholarly journals Variability of mitochondrial ORFans hints at possible differences in the system of doubly uniparental inheritance of mitochondria among families of freshwater mussels (Bivalvia: Unionida)

2019 ◽  
Vol 19 (1) ◽  
Author(s):  
Davide Guerra ◽  
Manuel Lopes-Lima ◽  
Elsa Froufe ◽  
Han Ming Gan ◽  
Paz Ondina ◽  
...  
Keyword(s):  
Freshwater Mussels ◽  
Complete Mitochondrial Genome ◽  
Physiological Role ◽  
Freshwater Mussel ◽  
Single Species ◽  
Open Reading Frames ◽  
Uniparental Inheritance ◽  
Doubly Uniparental Inheritance ◽  
Sexual Systems ◽  
Mitogenome Sequence

Abstract Background Supernumerary ORFan genes (i.e., open reading frames without obvious homology to other genes) are present in the mitochondrial genomes of gonochoric freshwater mussels (Bivalvia: Unionida) showing doubly uniparental inheritance (DUI) of mitochondria. DUI is a system in which distinct female-transmitted and male-transmitted mitotypes coexist in a single species. In families Unionidae and Margaritiferidae, the transition from dioecy to hermaphroditism and the loss of DUI appear to be linked, and this event seems to affect the integrity of the ORFan genes. These observations led to the hypothesis that the ORFans have a role in DUI and/or sex determination. Complete mitochondrial genome sequences are however scarce for most families of freshwater mussels, therefore hindering a clear localization of DUI in the various lineages and a comprehensive understanding of the influence of the ORFans on DUI and sexual systems. Therefore, we sequenced and characterized eleven new mitogenomes from poorly sampled freshwater mussel families to gather information on the evolution and variability of the ORFan genes and their protein products. Results We obtained ten complete plus one almost complete mitogenome sequence from ten representative species (gonochoric and hermaphroditic) of families Margaritiferidae, Hyriidae, Mulleriidae, and Iridinidae. ORFan genes are present only in DUI species from Margaritiferidae and Hyriidae, while non-DUI species from Hyriidae, Iridinidae, and Mulleriidae lack them completely, independently of their sexual system. Comparisons among the proteins translated from the newly characterized ORFans and already known ones provide evidence of conserved structures, as well as family-specific features. Conclusions The ORFan proteins show a comparable organization of secondary structures among different families of freshwater mussels, which supports a conserved physiological role, but also have distinctive family-specific features. Given this latter observation and the fact that the ORFans can be either highly mutated or completely absent in species that secondarily lost DUI depending on their respective family, we hypothesize that some aspects of the connection among ORFans, sexual systems, and DUI may differ in the various lineages of unionids.

scholarly journals Mitochondrial RNA and its eccentricities

2015 ◽  
Vol 37 (2) ◽  
pp. 28-32
Author(s):  
Zofia M. ChrzanowskaLightowlers
Keyword(s):  
Gene Expression ◽  
Molecular Mechanisms ◽  
Maternal Inheritance ◽  
Mitochondrial Gene ◽  
Mitochondrial Rna ◽  
Mitochondrial Gene Expression ◽  
Mitochondrial Evolution ◽  
Inheritance Patterns ◽  
Rna Elements

For those who do not work on mitochondria, their knowledge is often restricted to eubacterial origins, production of ATP and perhaps an appreciation of the non-Mendelian maternal inheritance patterns. These features are true enough, but things then start to get more complicated. Although the origins of mitochondria are accepted as a eubacterial endosymbiont of evolving eukaryotic cells1, there were organisms that were described as having jettisoned these ‘organelles’, referred to as amitochondriate eukaryotes. This concept has been challenged, and rudimentary mitochondria, or mitosomes, have now been found in those eukaryotes, which are apparently reluctant to lose this organelle2. The consequences of mitochondrial evolution can be seen in the divergence from the standard repertoire of RNA elements. These eccentricities pose challenges to our understanding of molecular mechanisms underlying mitochondrial gene expression.

scholarly journals Chloroplast competition is controlled by lipid biosynthesis in evening primroses

2018 ◽  
Author(s):  
Johanna Sobanski ◽  
Patrick Giavalisco ◽  
Axel Fischer ◽  
Julia Kreiner ◽  
Dirk Walther ◽  
...  
Keyword(s):  
Molecular Mechanisms ◽  
Regulatory Region ◽  
Lipid Synthesis ◽  
Nuclear Genome ◽  
Lipid Biosynthesis ◽  
Metabolic Phenotype ◽  
Uniparental Inheritance ◽  
Biparental Inheritance ◽  
Evening Primrose ◽  
Evolutionary Forces

AbstractIn most eukaryotes, organellar genomes are transmitted preferentially by the mother, but molecular mechanisms and evolutionary forces underlying this fundamental biological principle are far from understood. It is believed that biparental inheritance promotes competition between the cytoplasmic organelles and allows the spread of so-called selfish cytoplasmic elements. Those can be, for example, fast replicating or aggressive chloroplasts (plastids) that are incompatible with the hybrid nuclear genome and therefore maladaptive. Here we show that the ability of plastids to compete against each other is a metabolic phenotype determined by extremely rapidly evolving genes in the plastid genome of the evening primroseOenothera. Repeats in the regulatory region ofaccD(the plastid-encoded subunit of the acetyl-CoA carboxylase, which catalyzes the first and rate limiting step of lipid biosynthesis), as well as inycf2(a giant reading frame of still unknown function), are responsible for the differences in competitive behavior of plastid genotypes. Polymorphisms in these genes influence lipid synthesis and most likely profiles of the plastid envelope membrane. These in turn determine plastid division and/or turn-over rates and hence competitiveness. This work uncovers cytoplasmic drive loci controlling the outcome of biparental chloroplast transmission. Here, they define the mode of chloroplast inheritance, since plastid competitiveness can result in uniparental inheritance (through elimination of the “weak” plastid) or biparental inheritance (when two similarly “strong” plastids are transmitted).Significance statementPlastids and mitochondria are usually uniparentally inherited, typically maternally. When the DNA-containing organelles are transmitted to the progeny by both parents, evolutionary theory predicts that the maternal and paternal organelles will compete in the hybrid. As their genomes do not undergo sexual recombination, one organelle will “try” to outcompete the other, thus favoring the evolution and spread of aggressive cytoplasms. The investigations described here in the evening primrose, a model species for biparental plastid transmission, have discovered that chloroplast competition is a metabolic phenotype. It is conferred by rapidly evolving genes that are encoded on the chloroplast genome and control lipid biosynthesis. Due to their high mutation rate these loci can evolve and become fixed in a population very quickly.

scholarly journals Sex Determining Mechanisms in Bivalves

2017 ◽  
Author(s):  
Sophie Breton ◽  
Charlotte Capt ◽  
Davide Guerra ◽  
Donald Stewart
Keyword(s):  
Final Section ◽  
Genetic Factors ◽  
Current Knowledge ◽  
Mitochondrial Genes ◽  
Uniparental Inheritance ◽  
Developmental Pathway ◽  
Doubly Uniparental Inheritance ◽  
Sexual Systems ◽  
Determination System ◽  
Sex Determination System

In this review, we provide an overview of the current knowledge on the different sexual systems and sex determining mechanisms in bivalves, with a focus on the various epigenetic and genetic factors that may be involved. The final section of the review provides recent discoveries on sex-specific mitochondrial genes in bivalves possessing the unconventional system of doubly uniparental inheritance of mitochondria (which is found in several members of the orders Mytiloida, Unionoida, Veneroida and Nuculanoida). The genes involved in this developmental pathway could represent the first sex determination system in animals in which mitochondrially-encoded genes are directly involved.

scholarly journals A naturally heteroplasmic clam provides clues about the effects of genetic bottleneck on paternal mtDNA

2021 ◽  
Author(s):  
Mariangela Iannello ◽  
Stefano Bettinazzi ◽  
Sophie Breton ◽  
Fabrizio Ghiselli ◽  
Liliana Milani
Keyword(s):  
Maternal Inheritance ◽  
Ruditapes Philippinarum ◽  
Uniparental Inheritance ◽  
Single Individual ◽  
Doubly Uniparental Inheritance ◽  
Large Variability ◽  
Unique System ◽  
Multiple Copies ◽  
First Time ◽  
Different Tissues

Abstract Mitochondrial DNA (mtDNA) is present in multiple copies within an organism. Since these copies are not identical, a single individual carries a heterogeneous population of mtDNAs, a condition known as heteroplasmy. Several factors play a role in the dynamics of the within-organism mtDNA population: among them genetic bottlenecks, selection, and strictly maternal inheritance are known to shape the levels of heteroplasmy across mtDNAs. In Metazoa, the only evolutionarily stable exception to the strictly maternal inheritance of mitochondria is the doubly uniparental inheritance (DUI), reported in 100+ bivalve species. In DUI species there are two highly divergent mtDNA lineages, one inherited through oocyte mitochondria (F-type) and the other through sperm mitochondria (M-type). Having both parents contributing to the mtDNA pool of the progeny makes DUI a unique system to study the dynamics of mtDNA populations. Since in bivalves the spermatozoon has few mitochondria (4-5), M-type mtDNA faces a tight bottleneck during embryo segregation, one of the narrowest mitochondrial bottlenecks investigated so far. Here, we analyzed the F- and M-type mtDNA variability within individuals of the DUI species Ruditapes philippinarum, and we investigated for the first time the effects of such a narrow bottleneck affecting mtDNA populations. As a potential consequence of this narrow bottleneck, the M-type mtDNA shows a large variability in different tissues, a condition so pronounced that it leads to genotypes from different tissues of the same individual not to cluster together. We believe such results may help understanding the effect of low population size on mtDNA bottleneck.

scholarly journals Pursuing the quest for better understanding the taxonomic distribution of the system of doubly uniparental inheritance of mtDNA

PeerJ ◽  
2016 ◽  
Vol 4 ◽  
pp. e2760 ◽  
Author(s):  
Arthur Gusman ◽  
Sophia Lecomte ◽  
Donald T. Stewart ◽  
Marco Passamonti ◽  
Sophie Breton
Keyword(s):  
Maternal Inheritance ◽  
Uniparental Inheritance ◽  
Bivalve Species ◽  
Animal Kingdom ◽  
Doubly Uniparental Inheritance ◽  
Taxonomic Distribution ◽  
Scrobicularia Plana ◽  
Mitochondrial Transmission ◽  
And Function ◽  
Yoldia Hyperborea

There is only one exception to strict maternal inheritance of mitochondrial DNA (mtDNA) in the animal kingdom: a system named doubly uniparental inheritance (DUI), which is found in several bivalve species. Why and how such a radically different system of mitochondrial transmission evolved in bivalve remains obscure. Obtaining a more complete taxonomic distribution of DUI in the Bivalvia may help to better understand its origin and function. In this study we provide evidence for the presence of sex-linked heteroplasmy (thus the possible presence of DUI) in two bivalve species, i.e., the nuculanoidYoldia hyperborea(Gould, 1841)and the veneroidScrobicularia plana(Da Costa,1778), increasing the number of families in which DUI has been found by two. An update on the taxonomic distribution of DUI in the Bivalvia is also presented.

scholarly journals Bioenergetic consequences of sex-specific mitochondrial DNA evolution

2021 ◽  
Vol 288 (1957) ◽  
pp. 20211585
Author(s):  
Stefano Bettinazzi ◽  
Liliana Milani ◽  
Pierre U. Blier ◽  
Sophie Breton
Keyword(s):  
Mitochondrial Genome ◽  
Acid Metabolism ◽  
Maternal Inheritance ◽  
Tricarboxylic Acid Cycle ◽  
General Rule ◽  
High Energy ◽  
Uniparental Inheritance ◽  
Doubly Uniparental Inheritance ◽  
Antioxidant Metabolism ◽  
The Impact

Doubly uniparental inheritance (DUI) represents a notable exception to the general rule of strict maternal inheritance (SMI) of mitochondria in metazoans. This system entails the coexistence of two mitochondrial lineages (F- and M-type) transmitted separately through oocytes and sperm, thence providing an unprecedented opportunity for the mitochondrial genome to evolve adaptively for male functions. In this study, we explored the impact of a sex-specific mitochondrial evolution upon gamete bioenergetics of DUI and SMI bivalve species, comparing the activity of key enzymes of glycolysis, fermentation, fatty acid metabolism, tricarboxylic acid cycle, oxidative phosphorylation and antioxidant metabolism. Our findings suggest reorganized bioenergetic pathways in DUI gametes compared to SMI gametes. This generally results in a decreased enzymatic capacity in DUI sperm with respect to DUI oocytes, a limitation especially prominent at the terminus of the electron transport system. This bioenergetic remodelling fits a reproductive strategy that does not require high energy input and could potentially link with the preservation of the paternally transmitted mitochondrial genome in DUI species. Whether this phenotype may derive from positive or relaxed selection acting on DUI sperm is still uncertain.

scholarly journals Uniparental inheritance and replacement of mitochondrial DNA in Neurospora tetrasperma.

Genetics ◽  
1993 ◽  
Vol 134 (4) ◽  
pp. 1063-1075
Author(s):  
S B Lee ◽  
J W Taylor
Keyword(s):  
Mitochondrial Dna ◽  
Uniparental Inheritance ◽  
Mitochondrial Inheritance ◽  
Reproductive Structure ◽  
Hyphal Fusion ◽  
Heterokaryon Incompatibility ◽  
Reciprocal Interactions ◽  
Mtdna Inheritance ◽  
Length Polymorphisms ◽  
Neurospora Tetrasperma

Abstract This study tested mechanisms proposed for maternal uniparental mitochondrial inheritance in Neurospora: (1) exclusion of conidial mitochondria by the specialized female reproductive structure, trichogyne, due to mating locus heterokaryon incompatibility and (2) mitochondrial input bias favoring the larger trichogyne over the smaller conidium. These mechanisms were tested by determining the modes of mitochondrial DNA (mtDNA) inheritance and transmission in the absence of mating locus heterokaryon incompatibility following crosses of uninucleate strains of Neurospora tetrasperma with trichogyne (trichogyne inoculated by conidia) and without trichogyne (hyphal fusion). Maternal uniparental mitochondrial inheritance was observed in 136 single ascospore progeny following both mating with and without trichogyne using mtDNA restriction fragment length polymorphisms to distinguish parental types. This suggests that maternal mitochondrial inheritance following hyphal fusions is due to some mechanism other than those that implicate the trichogyne. Following hyphal fusion, mutually exclusive nuclear migration permitted investigation of reciprocal interactions. Regardless of which strain accepted nuclei following seven replicate hyphal fusion matings, acceptor mtDNA was the only type detected in 34 hyphal plug and tip samples taken from the contact and acceptor zones. No intracellular mtDNA mixtures were detected. Surprisingly, 3 days following hyphal fusion, acceptor mtDNA replaced donor mtDNA throughout the entire colony. To our knowledge, this is the first report of complete mitochondrial replacement during mating in a filamentous fungus.

scholarly journals The Effects of Natural Hybridization on the Regulation of Doubly Uniparental mtDNA Inheritance in Blue Mussels (Mytilus spp.)

Genetics ◽  
1996 ◽  
Vol 144 (1) ◽  
pp. 241-248 ◽  
Author(s):  
Paul D Ramon ◽  
Carol L Secor ◽  
Thomas J Hilbish
Keyword(s):  
High Frequency ◽  
Blue Mussel ◽  
Natural Hybridization ◽  
F1 Hybrids ◽  
Uniparental Inheritance ◽  
Male Gonad ◽  
Doubly Uniparental Inheritance ◽  
High Frequencies ◽  
Blue Mussels ◽  
Mtdna Inheritance

Abstract Blue mussels in the Mythilus edulis species complex have a doubly uniparental mode of mtDNA inheritance with separate maternal and paternal mtDNA lineages. Female mussels inherit their mtDNA solely from their mother, while males inherit mtDNA from both parents. In the male gonad the paternal mtDNA is preferentially replicated so that only paternal mtDNA is transmitted from fathers to sons. Hybridization is common among differentiated blue mussel taxa; whenever it involves M. trossulus, doubly uniparental mtDNA inheritance is disrupted. We have found high frequencies of males without and females with paternal mtDNA among hybrid mussels produced by interspecific matings between M. galloprovincialis and M. trossulus. In contrast, hybridization between M. galloprovincialis and M. edulis does not affect doubly uniparental inheritance, indicating a difference in the divergence of the mechanisms regulating mtDNA inheritance among the three blue mussel taxa. Our data indicate a high frequency of disrupted mtDNA transmission in F1 hybrids and suggest that two separate mechanisms, one regulating the transmission of paternal mtDNA to males and another inhibiting the establishment of paternal mtDNAin females, act to regulate doubly uniparental inheritance. We propose a model for the regulation of doubly uniparental inheritance that is consistent with these observations.

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