Intimate Relationship between mtDNA, Plasmids, and the Fusion of Mitochondria

Physarum polycephalum. The conformation of Physarum mtDNA is currently thought to be circular. The inheritance of its mtDNA depends on the multiallelic mating type loci, matA. In a cross with ordinary matA combinations, the strain that has the higher matA status transmits its mtDNA to the progeny (uniparental inheritance). The mF plasmid promotes the fusion of mitochondria in the zygote and during sporulation. When it exists in a strain with a lower status matA, the mF plasmid overcomes the force of uniparental inheritance and is preferentially transmitted to the progeny via mitochondrial fusion. Moreover, the conformation of mtDNA is changed from circular to linear by recombination with the mF plasmid. Since biparental inheritance usually occurs in a cross involving a combination of matA1 and matA15, two types of inheritance of Physarum mtDNA exist. Considering the existence of the mF plasmid, there are four patterns of cytoplasmic inheritance in P. polycephalum: 1) uniparental inheritance of mtDNA, 2) uniparental inheritance of mtDNA and preferential transmission of the mF plasmid, 3) biparental inheritance of mtDNA, and 4) biparental inheritance of mtDNA and the mF plasmid. This article describes the events involved in each pattern. Finally, we discuss a hypothetical mechanism for mitochondrial fusion. The essential protein may be the ORF640 protein encoded in the mF plasmid. Received 8 March 2000/ Accepted in revised form 23 March 2000     

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.     

RFLP marker analysis supports tetrasonic inheritance in Lotus corniculatus L.

Lotus corniculatus is a tetraploid (2n=4x=24) perennial forage legume and has been reported to have tetrasomic inheritance for several traits, although it has also been reported to show disomic inheritance. Molecular markers were used to clarify whether tetrasomic inheritance, disomic inheritance, or a combination of both, was found within an F₂ population arising from a cross between two diverse L. corniculatus accessions. The inheritance of ”tetra-allelic” RFLP markers (markers with four segregating bands) indicated that disomic inheritance could not account for the phenotypic F₂ classes observed, and that only tetrasomic inheritance would explain the observed results. Goodness of fit tests for ”tetra-allelic” and ”tri-allelic” (three segregating bands) RFLP marker data suggested support for chromosomal-type tetrasomic inheritance. RFLP genotypes interpreted from autoradiographic signal intensity provided additional support for tetrasomic inheritance and the occurrence of preferential pairing between parental chromosomes. Bivalent pairing was predominant in the two parental lines and their F₁ hybrid in cytological analyses. L. corniculatus has been classified as both an autotetraploid and an allotetraploid species. RFLP evidence of tetrasomic inheritance gives support for L. corniculatus being classified as an autotetraploid species. Even though bivalent pairing occurs, as seen in other autotetraploid species, pairing between any of the four homologous chromosomes is possible. Preferential pairing in the F₁ hybrid suggests that genome differentiation appears to be minimal between homologs within an accession, while genome differentiation is greater between homologs from different accessions of this genetically diverse species. Received: 16 November 1999 / Accepted: 14 July 2000     

Strict paternal inheritance of chloroplast DNA and maternal inheritance of mitochondrial DNA in intraspecific crosses of kiwifruit

 Previous studies have established that chloroplasts are inherited paternally in Actinidia interspecific crosses. However, fertilisation problems in interspecific crosses may affect the transmission of organelles. Six female clones, i.e. ‘Abbott’, ‘Bruno’, ‘Greensill’, ‘Hayward’, ‘Jones’, ‘Monty’, and four male clones were used to identify cpDNA polymorphisms within the cultivated kiwifruit species A. deliciosa. The restriction patterns by HpaII of a chloroplast fragment amplified by PCR with a pair of universal primers revealed a polymorphism at the intraspecific level. The inheritance of cpDNA in 143 seedlings from three intraspecific crosses in kiwifruit (Actinidia deliciosa) was studied. All offspring displayed the restriction pattern of the paternal parent, indicating that maternal inheritance of cpDNA in kiwifruit is rare at best. Strict maternal inheritance of mtDNA was confirmed in the same crosses used to investigate cpDNA transmission. Studies of cytoplasmic inheritance in the Actinidia genus represent to date the best documented report of differential organelle inheritance of cpDNA and mtDNA in angiosperms. Received: 10 November 1998 / Accepted: 14 December 1998     

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.     

Mapping Fusarium wilt race 1 resistance genes in cotton by inheritance,QTL and sequencing composition

Knowledge of the inheritance of disease resistance and genomic regions housing resistance (R) genes is essential to prevent expanding pathogen threats such as Fusarium wilt [Fusarium oxysporum f.sp. vasinfectum (FOV) Atk. Sny & Hans] in cotton (Gossypium spp.). We conducted a comprehensive study combining conventional inheritance, genetic and quantitative trait loci (QTL) mapping, QTL marker-sequence composition, and genome sequencing to examine the distribution, structure and organization of disease R genes to race 1 of FOV in the cotton genome. Molecular markers were applied to F₂ and recombinant inbred line (RIL) interspecific mapping populations from the crosses Pima-S7 (G. barbadense L.) × ‘Acala NemX’ (G. hirsutum L.) and Upland TM-1 (G. hirsutum) × Pima 3-79 (G. barbadense), respectively. Three greenhouse tests and one field test were used to obtain sequential estimates of severity index (DSI) of leaves, and vascular stem and root staining (VRS). A single resistance gene model was observed for the F₂ population based on inheritance of phenotypes. However, additional inheritance analyses and QTL mapping indicated gene interactions and inheritance from nine cotton chromosomes, with major QTLs detected on five chromosomes [Fov1-C06, Fov1-C08, (Fov1-C11 ₁ and Fov1-C11 ₂₎ , Fov1-C16 and Fov1-C19 loci], explaining 8–31% of the DSI or VRS variation. The Fov1-C16 QTL locus identified in the F₂ and in the RIL populations had a significant role in conferring FOV race 1 resistance in different cotton backgrounds. Identified molecular markers may have important potential for breeding effective FOV race 1 resistance into elite cultivars by marker-assisted selection. Reconciliation between genetic and physical mapping of gene annotations from marker-DNA and new DNA sequences of BAC clones tagged with the resistance-associated QTLs revealed defenses genes induced upon pathogen infection and gene regions rich in disease-response elements, respectively. These offer candidate gene targets for Fusarium wilt resistance response in cotton and other host plants.     

Inheritance in tetraploid yeast revisited: segregation patterns and statistical power under different inheritance models

In their recent article, Albertin et al. (2009) suggest an autotetraploid origin of 10 tetraploid strains of baker’s yeast (Saccharomyces cerevisiae), supported by the frequent observation of double reduction meiospores. However, the presented inheritance results were puzzling and seemed to contradict the authors’ interpretation that segregation ratios support a tetrasomic model of inheritance. Here, we provide an overview of the expected segregation ratios at the tetrad and meiospore level given scenarios of strict disomic and tetrasomic inheritance, for cases with and without recombination between locus and centromere. We also use a power analysis to derive adequate sample sizes to distinguish alternative models. Closer inspection of the Albertin et al. data reveals that strict disomy can be rejected in most cases. However, disomic inheritance with strong but imperfect preferential pairing could not be excluded with the sample sizes used. The possibility of tetrad analysis in tetraploid yeast offers a valuable opportunity to improve our understanding of meiosis and inheritance of tetraploids.     

The cytoplasmic structure hypothesis for ribosome assembly,vertical inheritance,and phylogeny

Fundamental questions in evolution concern deep divisions in the living world and vertical versus horizontal information transfer. Two contrasting views are: (i) three superkingdoms Archaea, Eubacteria, and Eukarya based on vertical inheritance of genes encoding ribosomes; versus (ii) a prokaryotic/eukaryotic dichotomy with unconstrained horizontal gene transfer (HGT) among prokaryotes. Vertical inheritance implies continuity of cytoplasmic and structural information whereas HGT transfers only DNA. By hypothesis, HGT of the translation machinery is constrained by interaction between new ribosomal gene products and vertically inherited cytoplasmic structure made largely of preexisting ribosomes. Ribosomes differentially enhance the assembly of new ribosomes made from closely related genes and inhibit the assembly of products from more distal genes. This hypothesis suggests experiments for synthetic biology: the ability of synthetic genomes to “boot,” i.e., establish hereditary continuity, will be constrained by the phylogenetic closeness of the cell “body” into which genomes are placed.     

Paternal inheritance of mitochondria in Chlamydomonas

To analyze mitochondrial DNA (mtDNA) inheritance, differences in mtDNA between Chlamydomonas reinhardtii and Chlamydomonas smithii, respiration deficiency and antibiotic resistance were used to distinguish mtDNA origins. The analyses indicated paternal inheritance. However, these experiments raised questions regarding whether paternal inheritance occurred normally. Mitochondrial nucleoids were observed in living zygotes from mating until 3 days after mating and then until progeny formation. However, selective disappearance of nucleoids was not observed. Subsequently, experimental serial backcrosses between the two strains demonstrated strict paternal inheritance. The fate of mt+ and mt− mtDNA was followed using the differences in mtDNA between the two strains. The slow elimination of mt+ mtDNA through zygote maturation in darkness was observed, and later the disappearance of mt+ mtDNA was observed at the beginning of meiosis. To explain the different fates of mtDNA, methylation status was investigated; however, no methylation was detected. Variously constructed diploid cells showed biparental inheritance. Thus, when the mating process occurs normally, paternal inheritance occurs. Mutations disrupting mtDNA inheritance have not yet been isolated. Mutations that disrupt maternal inheritance of chloroplast DNA (cpDNA) do not disrupt inheritance of mtDNA. The genes responsible for mtDNA inheritance are different from those of chloroplasts.     

An AFLP marker that differentiates biotypes of the Asian rice gall midge (Orseolia oryzae, Wood-Mason) is sex-linked and also linked to avirulence

In an attempt to identify a specific marker for biotype 2 of the Asian rice gall midge (Orseolia oryzae, Wood-Mason), we used AFLP (amplified fragment length polymorphism) fingerprinting. We identified an AFLP marker that is specifically amplified in biotypes 1, 2 and 5 of the rice gall midge, but not in biotype 4. Biotypes 1, 2 and 5 are avirulent to hosts bearing the Gm2 resistance gene (found in rice variety Phalguna), whereas biotype 4 is virulent to Gm2. Based on the sequence of this AFLP marker, SCAR (sequence characterized amplified region) primers were designed and used in combination with previously developed SCAR primers to distinguish effectively all five biotypes in a multiplex PCR-based assay. The inheritance pattern of this marker in the progenies of inter-biotype crosses between biotypes 1, 2 and 4 shows that the marker can be amplified by PCR from all F₁ females, irrespective of the biotype status of their parents. However, the marker is present only in those male progenies whose mother was of a Gm2 avirulent biotype. The specific amplification of this marker in the avirulent biotypes and its pattern of inheritance show that avirulence with respect to carriers of the Gm2 gene in rice gall midge is sex-linked. Received: 16 August 1999 / Accepted: 27 December 1999     

The foundation of extranuclear inheritance: plastid and mitochondrial genetics

In 1909 two papers by Correns and by Baur published in volume 1 of Zeitschrift für induktive Abstammungs- und Vererbungslehre (now Molecular Genetics and Genomics) reported on the non-Mendelian inheritance of chlorophyll deficiencies. These papers, reporting the very first cases of extranuclear inheritance, laid the foundation for a new field: non-Mendelian or extranuclear genetics. Correns observed a purely maternal inheritance (in Mirabilis), whereas Baur found a biparental inheritance (in Pelargonium). Correns suspected the non-Mendelian factors in the cytoplasm, while Baur believed that the plastids carry these extranuclear factors. In the following years, Baur’s hypothesis was proved to be correct. Baur subsequently developed the theory of plastid inheritance. In many genera the plastids are transmitted only uniparentally by the mother, while in a few genera there is a biparental plastid inheritance. Commonly there is random sorting of plastids during ontogenetic development. Renner and Schwemmle as well as geneticists in other countries added additional details to this theory. Pioneering studies on mitochondrial inheritance in yeast started in 1949 in the group of Ephrussi and Slonimski; respiration-deficient cells (petites in yeast, poky in Neurospora) were demonstrated to be due to mitochondrial mutations. Electron microscopical and biochemical studies (1962–1964) showed that plastids and mitochondria contain organelle-specific DNA molecules. These findings laid the molecular basis for the two branches of extranuclear inheritance: plastid and mitochondrial genetics.     

Matroclinal inheritance of cuticular waxes in reciprocal hybrids of Rosa species, sect. Caninae (Rosaceae)

Chemical surface characters play a decisive role in the interaction between plants and their environment. Maternal or paternal inheritance of wax characters in Rosa, section Caninae may allow for ecological niche differentiation according to the parental evolutionary constraints. If so, the radiation of hybrid offspring may reflect the parentally determined framework of interaction and selection against pathogens and abiotic stresses. We tested the inheritance of cuticular chemical wax parameters of reciprocal hybrids within Rosa, section Caninae, the dogroses. We not only found an extremely rich spectrum of chemical compounds on abaxial and adaxial leaf surfaces of dogroses, but also a maternally skewed inheritance of some of these wax characters. The possible role of these findings for the evolution of the allopolyploid dogrose complex is discussed.     

Isolation and variability of polymorphic microsatellite loci in Aedes aegypti,the vector of dengue viruses

We isolated five microsatellite sequences from an enriched‐(CAA)_n library of 5000 recombinant clones in Aedes aegypti. Two polymorphic microsatellites from our library and four from other sequence databases were tested: we investigated their polymorphism and Mendelian inheritance in mosquito populations. Our results indicate that trinucleotide repeat markers could be used to differentiate Ae. aegypti populations, making them valuable tools for the study of population genetic structure.     

Chloroplast DNA inheritance in theStellaria longipes complex (Caryophyllaceae)

Inheritance of chloroplast DNA (cpDNA) was examined in F₁ progenies derived from three crosses and three corresponding reciprocal crosses betweenStellaria porsildii andS. longifolia. Chloroplast DNA restriction fragments were analyzed using methods of nonradioactive digoxigenin-11-dUTP labeling and chemiluminescent detection with Lumi-Phos 530. Distinct interspecific restriction fragment polymorphisms were identified and used to demonstrate the mode of cpDNA inheritance. Mode of cpDNA inheritance differed among crosses. Two crosses in whichS. porsildii, SP2920-21, was the maternal parent exhibited three different types of plastids, maternal, paternal and biparental, among the F₁ hybrids, suggesting a biparental cpDNA inheritance and plastid sorting-out inStellaria.     

Inheritance patterns of ITS1, chloroplasts and mitochondria in artificial hybrids of the seaweeds Fucus serratus and F. evanescens (Phaeophyceae)

Patterns of nuclear and organelle inheritance among artificial hybrids of the seaweeds Fucus serratus and F. evanescens were detected using single-strand conformation polymorphism (SSCP). Three alleles were identified in the 231?bp rDNA-ITS1 gene (nuclear): two in F. serratus and one in F. evanescens. Alleles differed by 1–2?bp and all hybrids possessed one allele from each parent. Two haplotypes were present in the 288?bp Rubisco spacer (chloroplast), differentiated by a 33?bp indel. Two haplotypes differing by a single nucleotide were found in a 135?bp region of nad11 gene (mitochondrion). Both organelles are maternally inherited, as all hybrids contained the haplotypes of the parent contributing the egg. Although laboratory hybrids among Fucus spp. have been produced previously, this is the first time that both nuclear and cytoplasmic genetic markers have been used to document inheritance patterns. SSCPs analysed on an automated sequencer offer a rapid and powerful approach for identifying suspected hybrids from field samples, as well as a screen for intraspecific and intra-individual variation in DNA regions prior to confirmation of variations by sequencing.     

Variation in generative cell plastid nucleoids and male fertility in Medicago sativa

Biparental inheritance of plastids has been documented in numerous angiosperm species. The adaptive significance of the mode of plastid inheritance (unior biparental) is poorly understood. In plants exhibiting paternal inheritance of plastids, DNA-containing plastids in the microgametophyte may affect survival or growth of the gametophyte or the embryo. In this study the number of plastids containing DNA (nucleoids) in generative cells and generative cell and pollen volumes were evaluated in a range of genotypes of Medicago sativa (alfalfa). M. sativa exhibits biparental inheritance of plastids with strong paternal bias. The M. sativa genotypes used were crossed as male parents to a common genotype and the relationships between the gametophytic traits measured and male reproductive success were assessed. Generative cell plastid number and pollen grain size exhibited opposing associations with male fertility. Path analysis showed that generative cell plastid number was negatively associated with male fertility. This study provides evidence that there may be a competitive advantage at fertilization afforded sperm that have minimized their organelle content. The apparent lack of strong selection for reduced plastid number in generative cells of M. sativa may be a reflection of the diminished importance of reproductive success due to its perenniality or its long use in cultivation.     

Inheritance of chloroplast and mitochondrial genomes in pedunculate oak investigated with an efficient PCR method

The restriction patterns of two chloroplast fragments and one mitochondrial DNA fragment, amplified by PCR with universal primers, were studied to determine the mode of inheritance of these organelles in 143 progeny of five intraspecific crosses in pedunculate oak (Quercus robur L.). The results indicate that both genomes are maternally inherited, an observation which agrees with the commonly observed pattern of inheritance in angiosperms. They confirm that both chloroplast DNA and mitochondrial DNA can be used as a source of seed-specific markers for the study of the geographic structure of oaks. This is the first report of organelle inheritance within the Fagaceae, an important and widespread tree family.     

Inheritance of plastid DNA in the Turnera ulmifolia complex (Turneraceae)

We used PCR to amplify most of the rbcL gene and identified restriction fragment length polymorphisms to study the inheritance of chloroplast DNA (cpDNA) in the cross between two taxonomic varieties of the Turnera ulmifolia L. complex, vars. angustifolia and velutina. We identified an Alu I restriction site polymorphism that distinguished the parental plants. All 23 progeny from the cross var. angustifolia × var. velutina, where var. angustifolia was the maternal parent, possessed the paternal cpDNA. Results for the reciprocal cross were more varied, and the 16 progeny showed maternal, paternal, or biparental inheritance. We believe this represents the first study of plastid inheritance for any species in the Tumeraceae. The results are unusual and warrant further investigation using other species in this family.     

Localization of growth arrest-specific genes on mouse Chromosomes 1, 7, 8, 11, 13, and 16

Growth arrest in NIH3T3 cells is associated with increased expression of a variety of mRNAs, several of which have been isolated as cDNA clones. Six of these growth arrest-specific (Gas) genes were mapped by following the inheritance of DNA restriction fragment length variants (RFLVs) associated with them in panels of recombinant inbred (RI) strains of mice and in the progeny of backcrosses both between laboratory mouse strains and between a laboratory strain and Mus spretus. The six genes are unlinked. Gas-1 maps to Chromosome (Chr) 13, Gas-2 to Chr 7, Gas-3 to Chr 11, Gas-4 to Chr 16, Gas-6 to Chr 8, and Gas-10 to Chr 1.     

Plastid DNA inheritance and plastome-genome incompatibility in interspecific hybrids of Zantedeschia (Araceae)

Plastid DNA (ptDNA) probes were used in RFLP analysis to determine ptDNA inheritance in interspecific hybrids in Zantedeschia. Biparental and maternal ptDNA inheritance was found in albino hybrids between the evergreen species Z. aethiopica and several winter-dormant species. From two albino hybrids, different types of ptDNA were detected in shoots derived from different parts of an embryo. This result indicates that plastids were sorted out during embryo development. Only maternal ptDNA was detected in the hybrids of Z. aethiopica × Z. odorata (a summer-dormant species) but paternal, biparental, and maternal ptDNA were found in the hybrids of the reciprocal cross. Z. odorata × Z. aethiopica. By correlating these ptDNA inheritance patterns with the leaf colour (albino, pale-green, and green) of the hybrids, it is suggested that the Z. odorata plastome is incompatible with the Z. aethiopica genome. The Z. aethiopica plastome is partially compatible with the Z. odorata genome but the development of Z. aethiopica plastids appears to be blocked by the presence of the Z. odorata plastids.