Atypical mitochondrial inheritance patterns in eukaryotes

Breton, Sophie; Stewart, Donald T.

doi:10.1139/gen-2015-0090

Cited by 82 publications

(84 citation statements)

References 76 publications

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“…One possibility is occasional inheritance of mitochondria and symbionts through the paternal germline (paternal leakage). Paternal leakage is a common phenomenon that occurs in a variety of different taxa at low frequency (reviewed in Breton & Stewart, ), which would agree with our observation that introgressed symbionts are rare. The second possibility is doubly uniparental inheritance (DUI) of mitochondria, which would involve a regulated system of paternal cotransmission as suggested previously for Vesicomya sp.…”

Section: Discussionsupporting

confidence: 92%

Host hybridization as a potential mechanism of lateral symbiont transfer in deep‐sea vesicomyid clams

et al. 2019

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Deep‐sea vesicomyid clams live in mutualistic symbiosis with chemosynthetic bacteria that are inherited through the maternal germ line. On evolutionary timescales, strictly vertical transmission should lead to cospeciation of host mitochondrial and symbiont lineages; nonetheless, examples of incongruent phylogenies have been reported, suggesting that symbionts are occasionally horizontally transmitted between host species. The current paradigm for vesicomyid clams holds that direct transfers cause host shifts or mixtures of symbionts. An alternative hypothesis suggests that hybridization between host species might explain symbiont transfers. Two clam species, Archivesica gigas and Phreagena soyoae, frequently co‐occur at deep‐sea hydrocarbon seeps in the eastern Pacific Ocean. Although the two species typically host gammaproteobacterial symbiont lineages marked by divergent 16S rRNA phylotypes, we identified a number of clams with the A. gigas mitotype that hosted symbionts with the P. soyoae phylotype. Demographic inference models based on genome‐wide SNP data and three Sanger sequenced gene markers provided evidence that A. gigas and P. soyoae hybridized in the past, supporting the hypothesis that hybridization might be a viable mechanism of interspecific symbiont transfer. These findings provide new perspectives on the evolution of vertically transmitted symbionts and their hosts in deep‐sea chemosynthetic environments.

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Section: Discussionsupporting

confidence: 92%

Host hybridization as a potential mechanism of lateral symbiont transfer in deep‐sea vesicomyid clams

et al. 2019

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“…It is the first reported species with DUI from the family Semelidae, raising the total number of veneroid families in which DUI has been discovered to six (Theologidis et al, 2008; Plazzi, 2015; Dégletagne, Abele & Held, 2016; present study). Apart from providing new insights into the taxonomic distribution of DUI, S. plana may play a key role for better understanding the hypothesized role of DUI in sex determination (e.g., Breton et al, 2007; Breton et al, 2011a; Breton et al, 2014; Breton & Stewart, 2015; Mitchell et al, 2016). Indeed, an “intersex” condition, i.e., the appearance of oocytes in male gonads following endocrine disruption, has been reported in S. plana and is associated with differentially expressed mitochondrial transcripts in males exhibiting intersex compared to “normal” males (Chesman & Langston, 2006).…”

Section: Discussionmentioning

confidence: 99%

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

Gusman

Lecomte

Stewart

et al. 2016

PeerJ

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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 nuculanoid Yoldia hyperborea(Gould, 1841)and the veneroid Scrobicularia 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.

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“…Besides Metazoa, evidence also supports the existence of biparental inheritance of mitochondria in various plant and fungal taxa (see Barr et al. and Breton and Stewart for reviews). The discovery of DUI in bivalves dates back to 1990, when Fisher and Skibinski () observed that mitochondrial DNA (mtDNA) heteroplasmy was common in Mytilus Linnaeus, 1758 populations in Britain.…”

Section: Introductionmentioning

confidence: 89%

Evidence for extreme sequence divergence between the male- and female-transmitted mitochondrial genomes in the bivalve mollusc,Modiolus modiolus(Mytilidae)

Robicheau

Powell

Bel

et al. 2016

J Zool Syst Evol Res

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Marine mussels of the family Mytilidae, as well as a number of other bivalves, have a unique system of mitochondrial DNA inheritance called doubly uniparental inheritance (DUI). DUI is characterized by the presence of an ‘F’ mitochondrial genome that is transmitted through mothers to daughters and sons, and an ‘M’ mitochondrial genome that is transmitted only from fathers to sons. In this paper, we demonstrate that DUI exists in the horse mussel, Modiolus modiolus (Linnaeus, 1758) and compare the pattern of molecular evolution of the M and F types in this species. Total DNA was isolated from M. modiolus male and female gonad tissues, as well as from spawned sperm cells. From these DNA samples, partial mitochondrial DNA fragments were amplified from both cytochrome c oxidase subunit I (cox1), and 16S ribosomal RNA (rrnL) genes. Based on cox1 and rrnL sequences, heteroplasmy was observed in M. modiolus and characterized by the resolution of two mitotypes: an F mitotype present in tissues of both males and females, and an M mitotype present in spawned sperm. Using standardized p‐distance and Tamura‐Nei values, M. modiolus is found to display the highest M/F conspecific sequence divergence for any member of the family Mytilidae (i.e. 38% M/F sequence divergence, which is 9% higher than any other intraspecific M/F comparison for the family Mytilidae when standardized using p‐distances across all taxa observed). Sequence analysis also indicated that the M. modiolus M mitotype evolves significantly faster than its conspecific F type. The findings discussed herein broaden the range of mytilid species known to exhibit DUI and they also establish a new threshold for the genetic divergence of male mytilid mitochondrial genomes.

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Atypical mitochondrial inheritance patterns in eukaryotes

Cited by 82 publications

References 76 publications

Host hybridization as a potential mechanism of lateral symbiont transfer in deep‐sea vesicomyid clams

Host hybridization as a potential mechanism of lateral symbiont transfer in deep‐sea vesicomyid clams

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

Evidence for extreme sequence divergence between the male- and female-transmitted mitochondrial genomes in the bivalve mollusc,Modiolus modiolus(Mytilidae)

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