Paternal inheritance of mitochondrial DNA in the sheep ( Ovine aries )

Paternal inheritance of mitochondria DNA in sheep was discovered by examination of 152 sheep from 38 hybrid families for mtDNA D-loop polymorphisms using PCR-RFLP, amplification of repeated sequence somain, and PCR-SSCP of the D-loop 5′ end region of a 253 bp fragment. Our findings have provided the first evidence of paternal inheritance of mtDNA in sheep and possible mechanisms of paternal inheritance were discussed.     

Paternal transmission of mitochondrial DNA as an integral part of mitochondrial inheritance in metapopulations of Drosophila simulans

Maternal inheritance is one of the hallmarks of animal mitochondrial DNA (mtDNA) and central to its success as a molecular marker. This mode of inheritance and subsequent lack of heterologous recombination allows us to retrace evolutionary relationships unambiguously down the matriline and without the confounding effects of recombinant genetic information. Accumulating evidence of biparental inheritance of mtDNA (paternal leakage), however, challenges our current understanding of how this molecule is inherited. Here, using Drosophila simulans collected from an East African metapopulation exhibiting recurring mitochondrial heteroplasmy, we conducted single fly matings and screened F1 offspring for the presence of paternal mtDNA using allele-specific PCR assays (AS–PCR). In all, 27 out of 4092 offspring were identified as harboring paternal mtDNA, suggesting a frequency of 0.66% paternal leakage in this species. Our findings strongly suggest that recurring mtDNA heteroplasmy as observed in natural populations of Drosophila simulans is most likely caused by repeated paternal leakage. Our findings further suggest that this phenomenon to potentially be an integral part of mtDNA inheritance in these populations and consequently of significance for mtDNA as a molecular marker.     

Paternal inheritance of chloroplast DNA in interspecific hybrids in the genus Larrea (Zygophyllaceae)

The mode of chloroplast DNA (cpDNA) inheritance was investigated in the genus Larrea (Zygophyllaceae) by polymerase chain reaction (PCR) amplification of cpDNA fragments using three pairs of chloroplast universal primers. A total of 20 F(1)s from interspecific crosses among five different taxa in the section Bifolium was examined. Twelve F(1)s were from six crosses between L. cuneifolia (4x) and L. divaricata (2x) (Peru or Argentina) or L. tridentata (2x or 4x). Eight F(1)s were from two sets of reciprocal crosses between L. divaricata (2x) (Argentina) and L. tridentata (2x). Length polymorphism was observed in all three regions of cpDNA that separated L. cuneifolia parents from L. divaricata and L. tridentata parents and in one of the three cpDNA regions that differentiated L. divaricata (Argentina) parents from L. tridentata (2x) parents. In each case, it was the paternal cpDNA marker that appeared in the F(1) individuals. This was further confirmed by restriction fragment length polymorphism (RFLP) analysis of the amplified cpDNA fragments. Larrea may be the fifth genus reported in angiosperms with a paternal bias in cpDNA transmission. Possible mechanisms that may result in paternal cpDNA inheritance were briefly reviewed. Based on the observed uniparental paternal inheritance of cpDNA, restriction analysis of the three cpDNA regions and previous cytogenetic studies, L. divaricata was probably the maternal progenitor of L. cuneifolia.     

Paternal inheritance of chloroplast DNA and maternal inheritance of mitochondrial DNA in loblolly pine

Summary The inheritance of organelle DNAs in loblolly pine was studied by using restriction fragment length polymorphisms. Chloroplast DNA from loblolly pine is paternally inherited in pitch pine x loblolly pine hybrids. Mitochondrial DNA is maternally inherited in loblolly pine crosses. The uniparental inheritance of organelle genomes from opposite sexes within the same plant appears to be unique among those higher plants that have been tested and indicates that loblolly pine, and possibly other conifers, must have special mechanisms for organelle exclusion or degradation or both. This genetic system creates an exceptional opportunity for the study of maternal and paternal genetic lineages within a single species.     

Paternal inheritance of mitochondrial DNA in the sheep (Ovine aries)

Paternal inheritance of mitochondria DNA in sheep was discovered by examination of 152 sheep from 38 hybrid families for mtDNA D-loop polymorphisms using PCR-RFLP, amplification of repeated sequence somain, and PCR-SSCP of the D-loop 5′ end region of a 253 bp fragment. Our findings have provided the first evidence of paternal inheritance of mtDNA in sheep and possible mechanisms of paternal inheritance were discussed.     

Maternal inheritance of mitochondrial DNA

Maternal inheritance of mitochondrial DNA (mtDNA) is generally observed in many eukaryotes. Sperm-derived paternal mitochondria and their mtDNA enter the oocyte cytoplasm upon fertilization and then normally disappear during early embryogenesis. However, the mechanism underlying this clearance of paternal mitochondria has remained largely unknown. Recently, we showed that autophagy is required for the elimination of paternal mitochondria in Caenorhabditis elegans embryos. Shortly after fertilization, autophagosomes are induced locally around the penetrated sperm components. These autophagosomes engulf paternal mitochondria, resulting in their lysosomal degradation during early embryogenesis. In autophagy-defective zygotes, paternal mitochondria and their genomes remain even in the larval stage. Therefore, maternal inheritance of mtDNA is accomplished by autophagic degradation of paternal mitochondria. We also found that another kind of sperm-derived structure, called the membranous organelle, is degraded by zygotic autophagy as well. We thus propose to term this allogeneic (nonself) organelle autophagy as allophagy.     

Further evidence for paternal inheritance of mitochondrial DNA in the sheep (Ovis aries)

The mitochondrial DNA of 172 sheep from 48 families were typed by using PCR-RFLP, direct amplification of the repeated sequence domain and sequencing analysis. The mitochondrial DNA from three lambs in two half-sib families were found to show paternal inheritance. Our findings provide direct evidence of paternal inheritance of mitochondria DNA in sheep. A total of 12 highly polymorphic microsatellite markers, which mapped on different chromosomes, were employed to type the sheep population to confirm family relationships. Possible mechanisms of paternal inheritance are discussed.     

Paternal inheritance of chloroplast DNA in Larix

Restriction enzyme analysis was used to determine the inheritance of chloroplast DNA in conifers. The plant material studied included five individual trees of European larch (Larix decidua Mill.) and Japanese larch (Larix leptolepis Sieb. & Zucc.) and six hybrids from controlled crosses between these species. The chloroplast DNA fragment patterns generated by Bam-HI and Bcl-I were species-specific. Paternal inheritance of chloroplast DNA patterns was found in most Larix crosses. One hybrid showed maternal chloroplast DNA patterns. In addition, two other hybrids had mixed Bam-HI patterns suggesting recombination between maternal and paternal chloroplast DNA. The mechanisms favoring paternal inheritance in conifers are not known. Paternal inheritance of chloroplast DNA is suggested it to be a general phenomenon in conifers.     

Non-mendelian inheritance of mitochondrial DNA and ribosomal DNA in the myxomycete, Didymium iridis

Summary The inheritance of both the mitochondrial DNA (mtDNA) and the nuclear-encoded extrachromosomal ribosomal DNA (rDNA) has been studied in the myxomycete, Didymium iridis, by DNA-DNA hybridization of labeled probes to total DNA at various stage of the life cycle. Both the mtDNA and rDNA populations rapidly become homogeneous in individuals, but there is a qualitative difference in the patterns of inheritance of these two molecules. One parental rDNA type was preferentially inherited in all crosses; selective replication of this molecule is tentatively proposed as the mechanism of inheritance. In contrast, either parental mtDNA type could be inherited. Since the inherited population of parental mtDNA molecules are not partitioned into cells in this coenocytic organism, no known mechanism of inheritance can explain the rapid and apparently random loss of one parental mtDNA type in individuals.     

Paternal, maternal, and biparental inheritance of the chloroplast genome in Passiflora (Passifloraceae): implications for phylogenetic studies

Patterns of inheritance of the chloroplast genome in Passiflora were analyzed by examining the progeny from both interspecific and intraspecific crosses. Artificial crosses of field-collected material were performed in greenhouses at The University of Texas at Austin. DNA from fresh leaf material was analyzed by Southern blot techniques to identify the donor of the chloroplast genome. Initially, single progeny were analyzed for 11 crosses; two intraspecific crosses demonstrated maternal inheritance, whereas the nine interspecific crosses had paternal inheritance. Subsequently, the donor of the chloroplast genome was determined for multiple progeny in seven crosses. Passiflora oerstedii × P. retipetala showed strict paternal inheritance in all of 17 progeny. A series of five crosses and backcrosses between P. oerstedii and P. menispermifolia demonstrated strictly paternal inheritance. Finally, when 15 progeny were analyzed for the P. costaricensis × P. costaricensis cross, 12 of the 15 showed maternal inheritance, whereas the remaining three were biparental. Interestingly, all interspecific crosses had primarily paternal inheritance, whereas all intraspecific crosses had primarily maternal inheritance. The implications of heteroplasmy on phylogenetic analyses of chloroplast DNA are discussed.     

A novel maternal lineage revealed in sheep (Ovis aries)

It is generally believed that domestic sheep have two maternal lineages (haplotypes A and B), based on mitochondrial DNA analysis. In the present study, we provide evidence that a novel maternal lineage (haplotype C) is exhibited in Chinese native sheep. To verify this finding, 231 samples were collected from six Chinese local breeds, which cover the vast geographical region of sheep inhabitation in China. For comparison, 50 samples were collected from two Western breeds collected in China. Mitochondrial DNA was screened by PCR single-strand conformational polymorphism (SSCP), leading to the identification of novel band patterns in ND2 and ND4 genes in the Chinese breeds. Interestingly, mutations at the two loci were in strong linkage disequilibrium. Direct sequencing of the DNA fragments revealed a non-synonymous substitution in ND2. Furthermore, two synonymous mutations were identified by comparisons of the novel type (haplotype C) and the established types (haplotypes A and B). The entire mitochondrial control region for 55 samples was then sequenced to construct a phylogenetic tree and median joining network. Both the tree and network demonstrated a topology of three groups, which is in consistent with the SSCP analysis. Unlike Western breeds, Chinese breeds are composed mainly of haplotypes A and B, but with a small fraction of haplotype C. According to Fu's test and mismatch distribution, haplotype C has not been subject to a recent population expansion. Based on these results, we propose a novel origin for Chinese sheep.     

Mitochondrial DNA variation of domestic sheep (Ovis aries) in Kenya

The history of domestic sheep (Ovis aries) in Africa remains largely unknown. After being first introduced from the Near East, sheep gradually spread through the African continent with pastoral societies. The eastern part of Africa was important either for the first diffusion of sheep southward or for putative secondary introductions from the Arabian Peninsula or southern Asia. We analysed mitochondrial DNA control region sequences of 91 domestic sheep from Kenya and found a high diversity of matrilines from the widespread haplogroup B, whereas only a single individual from haplogroup A was detected. Our phylogeography analyses of more than 500 available mitochondrial DNA sequences also identified ancestral haplotypes that were probably first introduced in Africa and are now widely distributed. Moreover, we found no evidence of an admixture between East and West African sheep. The presence of shared haplotypes in eastern and ancient southern African sheep suggests the possible southward movement of sheep along the eastern part of Africa. Finally, we found no evidence of an extensive introduction of sheep from southern Asia into Africa via the Indian Ocean trade. The overall findings on the phylogeography of East African domestic sheep set the grounds for understanding the origin and subsequent movements of sheep in Africa. The richness of maternal lineages in Kenyan breeds is of prime importance for future conservation and breeding programmes.     

Paternal leakage of mitochondrial DNA inPinus

Summary We studied mitochondrial DNA restriction fragment length polymorphism in 11 parents and 125 seedlings of 23 controlled matings within and between jack pine (Pinus banksiana Lamb.) and lodgepole pine (P. contorta Dougl.). A potential mitochondrial distinction between these two conifers was evident in the parental samples. Only maternal mitochondrial restriction fragments were observed in a majority of the seedlings, which is consistent with results from angiosperms and other members of the genusPinus L. However, we detected exclusively paternal mitochondrial DNA in six of the seedlings. These unusual seedlings were not attributable to heteroplasmy or contamination of the experimental material, indicating that mitochondrial inheritance was not strictly maternal. Paternal mitochondrial leakage inPinus may permit novel insights into the transmission genetics and evolution of organellar polymorphisms.     

Population subdivision among desert bighorn sheep (Oviscanadensis) ewes revealed by mitochondrial DNA analysis

We used behavioural observations and mitochondrial DNA (mtDNA) sequence analysis to examine demographic and genetic structure within and among home-range groups of desert bighorn sheep (Oviscanadensis) ewes in the Peninsular Ranges of southern California, USA. We identified substantial genetic variation in the first 515 bp of the mtDNA control region and determined that seven haplotypes were distributed in a nonrandom fashion among these ewe subpopulations. Although a significant (P < 0.01) amount of mtDNA variation (33%) was partitioned among home-range groups, we did not find strong evidence for matrilineal substructuring within these groups. Based on analyses of molecular variance, and comparisons of behavioural associations and distances between centres of activity, we concluded that within a given home-range group, bighorn sheep ewes generally associate with other ewes based on their availability rather than their matrilineal relationships. Our results also supported the conclusion that multiple ewe subpopulations exist within the Peninsular Ranges, and that these subpopulations are the most basic demographic and genetic units.     

Autophagy is not involved in the degradation of sperm mitochondria after fertilization in mice

In almost all animals, mitochondrial DNA (mtDNA) is transmitted only from the female, while the paternal mitochondria and mtDNA are thought to be eliminated during early embryogenesis. Autophagy is involved in the elimination of sperm mitochondria and mtDNA in early embryos in Caenorhabditis elegans; however, solid evidence is still lacking in mammals. Recently, we found that despite the fact that some autophagy-related proteins, such as SQSTM1 and LC3 could localize nearby sperm mitochondria before the 2-cell stage, autophagy did not participate in the elimination of sperm mitochondria and mtDNA. Instead, the pre-elimination of sperm mtDNA before fertilization and the restriction of sperm mitochondria in one blastomere before 4-cell stage embryos are the most important mechanisms of maternal mitochondrial inheritance in mice.     

Selective sweeps of mitochondrial DNA can drive the evolution of uniparental inheritance

Although the uniparental (or maternal) inheritance of mitochondrial DNA (mtDNA) is widespread, the reasons for its evolution remain unclear. Two main hypotheses have been proposed: selection against individuals containing different mtDNAs (heteroplasmy) and selection against “selfish” mtDNA mutations. Recently, uniparental inheritance was shown to promote adaptive evolution in mtDNA, potentially providing a third hypothesis for its evolution. Here, we explore this hypothesis theoretically and ask if the accumulation of beneficial mutations provides a sufficient fitness advantage for uniparental inheritance to invade a population in which mtDNA is inherited biparentally. In a deterministic model, uniparental inheritance increases in frequency but cannot replace biparental inheritance if only a single beneficial mtDNA mutation sweeps through the population. When we allow successive selective sweeps of mtDNA, however, uniparental inheritance can replace biparental inheritance. Using a stochastic model, we show that a combination of selection and drift facilitates the fixation of uniparental inheritance (compared to a neutral trait) when there is only a single selective mtDNA sweep. When we consider multiple mtDNA sweeps in a stochastic model, uniparental inheritance becomes even more likely to replace biparental inheritance. Our findings thus suggest that selective sweeps of beneficial mtDNA haplotypes can drive the evolution of uniparental inheritance.     

Paternal inheritance of chloroplast DNA and maternal inheritance of mitochondrial DNA in the genus Actinidia

PCR amplification of four chloroplast DNA (cpDNA) and two mitochondrial DNA (mtDNA) regions followed by restriction of the amplified products was used to identify restriction fragment length polymorphisms in 21 Actinidia taxa. Subsequently, the mode of organelle inheritance was investigated in both interspecific and intraspecific controlled crosses made between genotypes showing different cpDNA and/or mtDNA haplotypes. Fifty-six seedlings produced from three interspecific crosses, including in one case the pseudo reciprocal (different genotypes of the same species used as opposite parents), were checked for cpDNA inheritance, and 102 seedlings from the same interspecific crosses and 32 seedlings from two intraspecific crosses within the species A. deliciosa were checked for mtDNA inheritance. In all cases, cpDNA was inherited from the father and mtDNA was inherited from the mother. Maternal inheritance of mtDNA was expected, being the rule in plants, but A. deliciosa is the first genus in angiosperms for which a widespread and strictly paternal inheritance of cpDNA has been reported. Transmission of chloroplastic and mitochondrial genomes through opposite parents provides an exceptional opportunity for studying the paternal and maternal genetic lineages of species in the genus Actinidia.     

Phylogenetic position of a copper age sheep (Ovis aries) mitochondrial DNA

Background

Sheep (Ovis aries) were domesticated in the Fertile Crescent region about 9,000-8,000 years ago. Currently, few mitochondrial (mt) DNA studies are available on archaeological sheep. In particular, no data on archaeological European sheep are available.

Methodology/Principal Findings

Here we describe the first portion of mtDNA sequence of a Copper Age European sheep. DNA was extracted from hair shafts which were part of the clothes of the so-called Tyrolean Iceman or Ötzi (5,350 - 5,100 years before present). Mitochondrial DNA (a total of 2,429 base pairs, encompassing a portion of the control region, tRNA^Phe, a portion of the 12S rRNA gene, and the whole cytochrome B gene) was sequenced using a mixed sequencing procedure based on PCR amplification and 454 sequencing of pooled amplification products. We have compared the sequence with the corresponding sequence of 334 extant lineages.

Conclusions/Significance

A phylogenetic network based on a new cladistic notation for the mitochondrial diversity of domestic sheep shows that the Ötzi''s sheep falls within haplogroup B, thus demonstrating that sheep belonging to this haplogroup were already present in the Alps more than 5,000 years ago. On the other hand, the lineage of the Ötzi''s sheep is defined by two transitions (16147, and 16440) which, assembled together, define a motif that has not yet been identified in modern sheep populations.     

Exceptional inheritance of plastids via pollen in Nicotiana sylvestris with no detectable paternal mitochondrial DNA in the progeny

Plastids and mitochondria, the DNA‐containing cytoplasmic organelles, are maternally inherited in the majority of angiosperm species. Even in plants with strict maternal inheritance, exceptional paternal transmission of plastids has been observed. Our objective was to detect rare leakage of plastids via pollen in Nicotiana sylvestris and to determine if pollen transmission of plastids results in co‐transmission of paternal mitochondria. As father plants, we used N. sylvestris plants with transgenic, selectable plastids and wild‐type mitochondria. As mother plants, we used N. sylvestris plants with Nicotiana undulata cytoplasm, including the CMS‐92 mitochondria that cause cytoplasmic male sterility (CMS) by homeotic transformation of the stamens. We report here exceptional paternal plastid DNA in approximately 0.002% of N. sylvestris seedlings. However, we did not detect paternal mitochondrial DNA in any of the six plastid‐transmission lines, suggesting independent transmission of the cytoplasmic organelles via pollen. When we used fertile N. sylvestris as mothers, we obtained eight fertile plastid transmission lines, which did not transmit their plastids via pollen at higher frequencies than their fathers. We discuss the implications for transgene containment and plant evolutionary histories inferred from cytoplasmic phylogenies.