A resourceful genome: updating the functional repertoire and evolutionary role of animal mitochondrial DNAs

Breton, Sophie; Milani, Liliana; Ghiselli, Fabrizio; Guerra, Davide; Stewart, Donald T.; Passamonti, Marco

doi:10.1016/j.tig.2014.09.002

Cited by 102 publications

(119 citation statements)

References 91 publications

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“…Their functions are still unknown, although the presence of gene products in the nucleus indicates that they are not involved in ATP production, like other typical mtDNAencoded proteins (Breton et al 2011(Breton et al , 2014Milani et al 2014). An initial hypothesis proposed that these genes may play a role in sex determination because of the observation that gonochorism (i.e., separate male and female sexes) in freshwater bivalves is absolutely correlated with the presence of DUI and these novel sex-specific proteins whereas closely related hermaphroditic species lack the M mtDNA (i.e., possess SMI) and have macromutations in the F-orf in their F mtDNAs (Breton et al 2011).…”

Section: Doubly Uniparental Inheritancementioning

confidence: 99%

Atypical mitochondrial inheritance patterns in eukaryotes

Breton

Stewart

2015

Genome

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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.Key words: mitochondrial DNA, mitochondrial inheritance, sex determination, paternal leakage, heteroplasmy.Résumé : L'ADN mitochondrial (l'ADNmt) est principalement hérité de la meÌre chez les eucaryotes. Divers mé-canismes moléculaires sous-jacents au phénomeÌne ont été décrits, mais les forces évolutives responsables de sa prédominance chez les eucaryotes restent encore aÌ etre élucidées. Des exceptions aÌ la transmission strictement maternelle de l'ADNmt (« strict maternal inheritance » ou SMI) ont été signalées chez divers taxons eucaryotes, laissant penser que plusieurs nouveaux mécanismes moléculaires de transmission de l'ADNmt existent chez les eucaryotes. Nous proposons que ces mécanismes seront mieux compris en étudiant les exceptions au type prédominant de transmission mitochondrial SMI. Cette mini-revue résume les études sur les espeÌces eucaryotes avec des systeÌmes de transmission mitochondriale inhabituels ou rares, c'est-aÌ-dire autres que la SMI, tels que la transmission maternelle stable d'une hétéroplasmie, la transmission occasionnelle de l'ADNmt paternel (« paternal leakage »), la transmission biparentale ou encore strictement paternelle de l'ADNmt et la transmission doublement uniparentale de l'ADNmt. Les geÌnes et les mécanismes impliqués dans le contrôle de la transmission mitochondriale chez ces organismes « déviants » sont discutés. Le lien étroit entre la t...

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Section: Doubly Uniparental Inheritancementioning

confidence: 99%

Atypical mitochondrial inheritance patterns in eukaryotes

Breton

Stewart

2015

Genome

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“…[9][10][11] ). Several reasons can explain this extensive variation: increase can be due to changes in the genetic code or a consequence of tRNA gene duplication, while decrease is generally due to the loss of mt tRNA genes during evolution, compensated by the import of nucleus-encoded tRNAs, a classical phenomenon in mitochondria.…”

Section: Introductionmentioning

confidence: 99%

Large gene overlaps and tRNA processing in the compact mitochondrial genome of the crustaceanArmadillidium vulgare

et al. 2015

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“…nucleotide P-distance: 22-39%; amino-acid P-distances in Ruditapes philippinarum and unionoids freshwater mussels: 34% and up to~51%, respectively; reviewed in Zouros, 2013), co-exist in the same species and are inherited through separate routes. The F is transmitted by females through eggs to both sons and daughters, whereas the M is transmitted by males through spermatozoa to sons only (Breton et al, 2007;Passamonti and Ghiselli, 2009;Zouros, 2013;Breton et al, 2014). Females are essentially homoplasmic for the F mtDNA, whereas males are always heteroplasmic carrying both F and M mtDNAs.…”

Section: Introductionmentioning

confidence: 99%

“…Evidence indicates that DUI relies on the same molecular machine of strictly maternal inheritance typical of animals, with some modifications that let paternal inheritance of M mtDNA happen (Breton et al, 2014). The preferential segregation of M mtDNA in male germ line seems more linked to active processes than to replication rate only (Venetis et al, 2006;Ghiselli et al, 2011;Milani et al, 2011;Guerra et al, 2014), while the driving forces behind F and M distribution in somatic tissues are still unknown.…”

Section: Introductionmentioning

confidence: 99%

Early replication dynamics of sex-linked mitochondrial DNAs in the doubly uniparental inheritance species Ruditapes philippinarum (Bivalvia Veneridae)

et al. 2015

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Mitochondrial homoplasmy, which is maintained by strictly maternal inheritance and a series of bottlenecks, is thought to be an adaptive condition for metazoans. Doubly uniparental inheritance (DUI) is a unique mode of mitochondrial transmission found in bivalve species, in which two distinct mitochondrial genome (mtDNA) lines are present, one inherited through eggs (F) and one through sperm (M). During development, the two lines segregate in a sex-and tissue-specific manner: females lose M during embryogenesis, whereas males actively segregate it in the germ line. These two pivotal events are still poorly characterized. Here we investigated mtDNA replication dynamics during embryogenesis and pre-adulthood of the venerid Ruditapes philippinarum using real-time quantitative PCR. We found that both mtDNAs do not detectably replicate during early embryogenesis, and that the M line might be lost from females around 24 h of age. A rise in mtDNA copy number was observed before the first reproductive season in both sexes, with the M mitochondrial genome replicating more than the F in males, and we associate these boosts to the early phase of gonad production. As evidence indicates that DUI relies on the same molecular machine of mitochondrial maternal inheritance that is common in most animals, our data are relevant not only to DUI but also to shed light on how differential segregations of mtDNA variants, in the same nuclear background, may be controlled during development.

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A resourceful genome: updating the functional repertoire and evolutionary role of animal mitochondrial DNAs

Cited by 102 publications

References 91 publications

Atypical mitochondrial inheritance patterns in eukaryotes

Atypical mitochondrial inheritance patterns in eukaryotes

Large gene overlaps and tRNA processing in the compact mitochondrial genome of the crustaceanArmadillidium vulgare

Early replication dynamics of sex-linked mitochondrial DNAs in the doubly uniparental inheritance species Ruditapes philippinarum (Bivalvia Veneridae)

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