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Novel protein genes in animal mtDNA: a new sex determination system in freshwater mussels (Bivalvia: Unionoida)?

ABSTRACT: Mitochondrial (mt) function depends critically on optimal interactions between components encoded by mt and nuclear DNAs. mitochondrial DNA (mtDNA) inheritance (SMI) is thought to have evolved in animal species to maintain mito-nuclear complementarity by preventing the spread of selfish mt elements thus typically rendering mtDNA heteroplasmy evolutionarily ephemeral. Here, we show that mtDNA intraorganismal heteroplasmy can have deterministic underpinnings and persist for hundreds of millions of years. We demonstrate that the only exception to SMI in the animal kingdom, that is, the doubly uniparental mtDNA inheritance system in bivalves, with its three-way interactions among egg mt-, sperm mt- and nucleus-encoded gene products, is tightly associated with the maintenance of separate male and female sexes (dioecy) in freshwater mussels. Specifically, this mother-through-daughter and father-through-son mtDNA inheritance system, containing highly differentiated mt genomes, is found in all dioecious freshwater mussel species. Conversely, all hermaphroditic species lack the paternally transmitted mtDNA (=possess SMI) and have heterogeneous macromutations in the recently discovered, novel protein-coding gene (F-orf) in their maternally transmitted mt genomes. Using immunoelectron microscopy, we have localized the F-open reading frame (ORF) protein, likely involved in specifying separate sexes, in mitochondria and in the nucleus. Our results support the hypothesis that proteins coded by the highly divergent maternally and paternally transmitted mt genomes could be directly involved in sex determination in freshwater mussels. Concomitantly, our study demonstrates novel features for animal mt genomes: the existence of additional, lineage-specific, mtDNA-encoded proteins with functional significance and the involvement of mtDNA-encoded proteins in extra-mt functions. Our results open new avenues for the identification, characterization, and functional analyses of ORFs in the intergenic regions, previously defined as "noncoding," found in a large proportion of animal mt genomes.

SUBMITTER: Breton S

PROVIDER: S-EPMC3107663 | biostudies-literature | 2011 May

REPOSITORIES: biostudies-literature

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Novel protein genes in animal mtDNA: a new sex determination system in freshwater mussels (Bivalvia: Unionoida)?

Breton Sophie S Stewart Donald T DT Shepardson Sally S Trdan Richard J RJ Bogan Arthur E AE Chapman Eric G EG Ruminas Andrew J AJ Piontkivska Helen H Hoeh Walter R WR

Molecular biology and evolution 20101220 5

Mitochondrial (mt) function depends critically on optimal interactions between components encoded by mt and nuclear DNAs. mitochondrial DNA (mtDNA) inheritance (SMI) is thought to have evolved in animal species to maintain mito-nuclear complementarity by preventing the spread of selfish mt elements thus typically rendering mtDNA heteroplasmy evolutionarily ephemeral. Here, we show that mtDNA intraorganismal heteroplasmy can have deterministic underpinnings and persist for hundreds of millions of ...[more]

PMID: 21172831

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Project description:BackgroundMany species of bivalves exhibit a unique system of mtDNA transmission named Doubly Uniparental Inheritance (DUI). Under this system, species have two distinct, sex-linked mitochondrial genomes: the M-type mtDNA, which is transmitted by males to male offspring and found in spermatozoa, and the F-type mtDNA, which is transmitted by females to all offspring, and found in all tissues of females and in somatic tissues of males. Bivalves with DUI also have sex-specific mitochondrial ORFan genes, (M-orf in the M mtDNA, F-orf in the F mtDNA), which are open reading frames having no detectable homology and no known function. DUI ORFan proteins have previously been characterized in silico in a taxonomically broad array of bivalves including four mytiloid, one veneroid and one unionoid species. However, the large evolutionary distance among these taxa prevented a meaningful comparison of ORFan properties among these divergent lineages. The present in silico study focuses on a suite of more closely-related Unionoid freshwater mussel species to provide more reliably interpretable information on patterns of conservation and properties of DUI ORFans. Unionoid species typically have separate sexes, but hermaphroditism also occurs, and hermaphroditic species lack the M-type mtDNA and possess a highly mutated version of the F-orf in their maternally transmitted mtDNA (named H-orf in these taxa). In this study, H-orfs and their respective proteins are analysed for the first time.ResultsDespite a rapid rate of evolution, strong structural and functional similarities were found for M-ORF proteins compared among species, and among the F-ORF and H-ORF proteins across the studied species. In silico analyses suggest that M-ORFs have a role in transport and cellular processes such as signalling, cell cycle and division, and cytoskeleton organisation, and that F-ORFs may be involved in cellular traffic and transport, and in immune response. H-ORFs appear to be structural glycoproteins, which may be involved in signalling, transport and transcription. Our results also support either a viral or a mitochondrial origin for the ORFans.ConclusionsOur findings reveal striking structural and functional similarities among proteins encoded by mitochondrial ORFans in freshwater mussels, and strongly support a role for these genes in the DUI mechanism. Our analyses also support the possibility of DUI systems with elements of different sources/origins and different mechanisms of action in the distantly-related DUI taxa. Parallel situations to the novel mitochondrially-encoded functions of freshwater mussel ORFans present in some other eukaryotes are also discussed.

Project description:BackgroundA novel feature for animal mitochondrial genomes has been recently established: i.e., the presence of additional, lineage-specific, mtDNA-encoded proteins with functional significance. This feature has been observed in freshwater mussels with doubly uniparental inheritance of mtDNA (DUI). The latter unique system of mtDNA transmission, which also exists in some marine mussels and marine clams, is characterized by one mt genome inherited from the female parent (F mtDNA) and one mt genome inherited from the male parent (M mtDNA). In freshwater mussels, the novel mtDNA-encoded proteins have been shown to be mt genome-specific (i.e., one novel protein for F genomes and one novel protein for M genomes). It has been hypothesized that these novel, F- and M-specific, mtDNA-encoded proteins (and/or other F- and/or M-specific mtDNA sequences) could be responsible for the different modes of mtDNA transmission in bivalves but this remains to be demonstrated.Methodology/principal findingsWe investigated all complete (or nearly complete) female- and male-transmitted marine mussel mtDNAs previously sequenced for the presence of ORFs that could have functional importance in these bivalves. Our results confirm the presence of a novel F genome-specific mt ORF, of significant length (>100aa) and located in the control region, that most likely has functional significance in marine mussels. The identification of this ORF in five Mytilus species suggests that it has been maintained in the mytilid lineage (subfamily Mytilinae) for ∼13 million years. Furthermore, this ORF likely has a homologue in the F mt genome of Musculista senhousia, a DUI-containing mytilid species in the subfamily Crenellinae. We present evidence supporting the functionality of this F-specific ORF at the transcriptional, amino acid and nucleotide levels.Conclusions/significanceOur results offer support for the hypothesis that "novel F genome-specific mitochondrial genes" are involved in key biological functions in bivalve species with DUI.

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Novel protein genes in animal mtDNA: a new sex determination system in freshwater mussels (Bivalvia: Unionoida)?

Publications

Novel protein genes in animal mtDNA: a new sex determination system in freshwater mussels (Bivalvia: Unionoida)?

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