Mutational meltdown of organelle genomes is overcome by episodes of recombination between organelle genomes. Importantly, such elements cannot be disarmed by recombination. Finally, we propose experimental strategies to test the assumptions underlying our model. Although not universal, maternal inheritance is the predominant mode of organelle transmission in all eukaryotic kingdoms.
This raises the question as to which evolutionary forces favor its prevalence. Below, we briefly discuss the main models in the light of existing experimental evidence. We point out unsettled questions and assumptions that remain to be scrutinized. It should be emphasized that these models are not necessarily mutually exclusive. As originally proposed by Grun 26 and based on genetic observations in evening primroses genus Oenothera , the most frequently expressed explanation for the evolution of uniparental organelle inheritance is the avoidance of cytonuclear conflicts 21 , From a modeling perspective, the two schemes cannot be fully discerned from each other 27 - However, with few exceptions e.
Wolbachia and related infectious bacteria in arthropods and nematodes , the frequent presence and vertical transmission of cytoplasmic parasites is not documented for many eukaryotes. In addition, the assumption that mixing of such parasites generally reduces host fitness is doubtable Moreover, uniparental transmission may exclude organelles from vertical transmission, but not necessarily parasites at the same time. For example, paternal transmission of a virus was observed in barley 34 , a species that inherits its organelles maternally Table 1.
Mutations in one of the genomes, for example in a locus determining the replication speed of the organelle, would allow one of the lineages to outgrow the other. Also, mutations in oDNA might arise that mar the competing organelles by their attempts to gain a competitive advantage 24 , Alternatively, there is the possibility that different organelles harbor different alleles of one locus, and their heteroplasmic combination is maladaptive to the cell Obviously, a strict uniparental inheritance of organelles largely avoids these problems. Indeed, modeling of such scenarios frequently leads to the fixation of a nuclear inheritance modifier that causes switching from an ancestral biparental to a derived uniparental mode of inheritance.
Another starting point toward explaining uniparental inheritance is the assumption that sexual recombination of oDNA is not the only force that counteracts Muller's ratchet see below. Hence, strict uniparental organelle transmission may be less harmful than widely assumed. Most relevant in this context is that organelles pass a genetic bottleneck when entering the germline Box 1. Subsequently, deleterious mutations can be eliminated effectively by selection 12 , Modeling work showed that paternal leakage or biparental transmission would interfere with this process Another model that deserves consideration was postulated recently In particular, the different types of genomic conflict hypotheses have been modeled extensively.
From this work, several theoretical problems arose. A general argument against these hypotheses is that a mutation leading to uniparental transmission can only be advantageous if a selfish cytoplasmic element is present, but not yet fixed in the population 6 , 16 , Uniparental inheritance can, therefore, only evolve within rather strict boundary conditions.
It seems that these problems can be solved by a recently proposed model 5. It makes the assumption that the gametes control organelle inheritance. It further takes the dynamics of the fitness costs of biparental inheritance into account in that cells do not suffer from a fixed cost of biparental inheritance, but the actual costs depend on the number of selfish or maladaptive mutations. This appears to be the case under very broad parameters. However, in agreement with previous modeling, it was found that an inheritance modifier that kills its own organelles cannot spread.
Paternal exclusion should, therefore, be evolutionarily unstable This is mainly due to the mechanistic problem that such an allele cannot be genetically linked with the fittest cytotype 5 , 6 , It is, however, obviously associated with fitness costs.
Different Organelles and their Functions
However, in contrast to mammalian mitochondrial DNA, the nucleotide substitution frequencies in plastid and plant mitochondrial genomes are very low 51 , In these organisms, maternal transmission implies a costly mechanism for the organism to eliminate its own paternal cytoplasm.
The second argument that can be raised against all models for uniparental inheritance is the implicit assumption that the cytotype transmitted into the hybrid typically the maternal cytotype is generally fitter than the excluded paternal cytotype e. Hence, the current theoretical problem connected with organelle inheritance is not its sex linkage per se, but rather the dominance of the maternal over the paternal mode and in many cases its control by the paternal gamete.
Arguing that gamete size simply determines organelle inheritance in a largely quantitative manner in that female gametes are larger and, therefore, harbor more organelles , is not satisfactory either. Especially in plants, many examples exist for i contrasting modes of plastid DNA ptDNA and mitochondrial DNA mtDNA inheritance, and ii biparental or predominantly paternal transmission, implying a high organelle load in the paternal gamete 46 , 49 , 53 , 54 ; Table 1 ; Box 3. In view of the problems outlined above, some authors assume that the current models do not provide a fully satisfactory explanation for the prevalence of uniparental transmission of plastids and mitochondria in the entire eukaryotic domain 16 , 42 , 44 , Organelle genomes of plants and animals as well as those of unicellular and multicellular eukaryotes differ greatly in genome organization, coding capacity, copy number per cell and mutation rate, as do cell and gamete sizes and ecological niches.
On the other hand, the predominance of maternal organelle transmission, along with the virtual absence of sexual recombination between organelles in most lineages of eukaryotic evolution, is striking. It thus appears likely that there is a general explanation for the observed pattern but also see The exclusion of organelles from the germline is an active process and should be costly 46 - Also, it has likely evolved repeatedly 16 , 46 , 49 ; Fig.
Hence, there must be a strong, general selection pressure maintaining this trait. By arguing from a physiological point of view, a possible explanation was offered by Allen It posits that only the maternal organelle DNA is maintained because it is protected from oxidative damage as caused by the electron transfer reactions in photosynthesis and respiration. Since the sessile egg cell has a lower energy demand than the mobile sperm, the paternal oDNA may suffer from higher oxidative damage and, therefore, is excluded from inheritance.
By contrast, the maternal germline cells are protected in specialized tissues, where organelles would display low metabolic rates. This assumption seems to be true for a wide range of animal systems 57 , and likely also for proplastids in plant meristems. However, since the meristem confers plant growth and cellular differentiation, it has a high energy demand. Therefore, its mitochondria should not be protected from reactive oxygen species.
Also, the hypothesis cannot apply to unicellular organisms. Thus, like most of the genetic models described above, the theory falls short of explaining organelle inheritance patterns for all eukaryotes.
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Even though it provides an elegant explanation for why paternal exclusion of cytoplasms could be frequent, the theory cannot explain the widespread occurrence of biparental transmission of chloroplast, paternal leakage, and cases of paternal oDNA inheritance 46 , 49 , 53 ; Table 1. Taking a number of theoretical considerations into account, we propose here a unifying model for organelle inheritance Fig. However, uniparental inheritance is evolutionarily unstable, because organelles are subject to Muller's ratchet.
This drives a relaxation of strict maternal inheritance by paternal leakage or regular biparental transmission. Biparental inheritance is again susceptible to the evolution of selfish genomes and, therefore, is repeatedly lost and restored over evolutionary timeframes. In other words, the mutational meltdown by Muller's ratchet is escaped from by episodes or longer periods of sexual recombination between organelle genomes. Importantly, sexual oDNA recombination is not sufficient to stop the spread of selfish cytoplasmic elements.
What is the actual evidence for these assumptions? If uniparental inheritance is evolutionarily unstable, three major patterns in organelle inheritance should be observable. First, biparental transmission should evolve repeatedly and independently. Second, paternal leakage should be relatively frequent.
Strikingly, these patterns are indeed observed, throughout the eukaryotic domain Box 3 ; Fig. In all sexually reproducing eukaryotes, the zygote develops through fusion of an egg cell with a usually motile sperm cell. It subsequently undergoes rapid divisions that incur a high energy demand.
This should be the case for both mtDNA and ptDNA, because in many seed plant taxa, embryos are green at least in the early stages of seed development the embryo is exposed to light and perform photosynthesis If selection in the zygote is the driving force for paternal exclusion, one must, however, assume higher mutation rates for paternally inherited organelle genotypes.
This can be tested in paternally inherited cytotypes as found in gymnosperms. Strikingly, oDNA mutation rates are indeed higher in these taxa, suggesting that, compared to the egg cell, organelles in the pollen carry a higher mutational load 52 , 59 , However, since oxidative damage fails to explain relaxed maternal organelle inheritance patterns see above , it cannot be the sole and universal driving force for the observed patterns of oDNA inheritance.
However, paternal oDNA copy numbers in the sperm cell are typically substantially smaller than maternal copy numbers in the larger egg cell. Hence, genetic drift of oDNAs due to stronger genetic bottlenecking at the level of the gamete might represent an additional relevant factor. This view is in line with theoretical considerations, arguing that the higher mutational load of organelle genomes in general is not due to asexuality per se, but is the result of the small effective population size of organellar genomes Taken together, maternal dominance in organelle inheritance could be due to a lower mutational load, since in most organisms, more oDNA copies are inherited by the mother.
However, in organisms where bottlenecking is less severe for the male gamete, paternal oDNA inheritance can evolve, thus potentially explaining why contrasting modes of organelle inheritance exist. This especially applies to isogamous organisms, carrying two organelles such as green algae Box 2. Finally, uniparental maternal inheritance must be seen as a consequence of, rather than the underlying reason for, anisogamy Box 2. Maternal dominance of uniparental inheritance could be explained by a higher mutational load of the paternal gamete.
Examining plant cells under the microscope
However, why does uniparental inheritance exist at all, and what are the selection forces, leading to uniparental maternal inheritance? In the case of mitochondria, a possible mechanistic scenario could, for example, involve the unscheduled onset of apoptosis. At least for plastids of seed plants, such interactions are difficult to image, since plastids usually do not undergo fusion 16 , 46 , Negative interactions between mitochondria in plants and animals seem to be possible, and were reported in some cell fusions 65 , Recently, it was demonstrated that heteroplasmic mice display reduced respiratory activity and behavioral phenotypes, whereas mice homoplasmic for either of the two mitochondrial genotypes had no phenotype However, analyses on sexual oDNA recombination in yeast and Chlamydomonas somewhat argue against the widespread occurrence of deleterious epistasis between oDNA alleles, since the expected segregation distortion is not normally observed Box 4.
Given the few documented examples, the general significance of deleterious epistatic interactions between organelles is currently questionable. Recombination between biparentally inherited organelle genomes has been reported for some taxa, but is controversial in others 15 , 16 , 18 , 20 for references. It is important to note that, upon strict uniparental inheritance and lack of sexual recombination , selective sweeps should be frequent in organellar genomes, but are barely observed Detailed genetic linkage analyses based on sexual oDNA recombination were conducted in yeast e. Both organisms display biparental inheritance or paternal leakage of their organelles Table 1.
Linkage analyses in yeast and Chlamydomonas uncovered remarkable differences of oDNA recombination compared to recombination mapping in the nuclear genome. Furthermore, random pairing of oDNA molecules, multiple rounds of paring and recombination, and random segregation of oDNA copies is assumed In spite of these uncertainties, genetic distances obtained from segregation analyses usually correlate well with the physical distances of the genetic markers , , Also, recombination hotspots can exist in oDNAs This is likely due to gene conversion, but other factors may be involved as well The general features of sexual oDNA recombination as worked out for unicellular organisms may be transferable to many multicellular eukaryotes.
However, there are some limitations concerning the frequency of organelle mixing and fusion. For example, plastids of seed plants do not seem to regularly undergo recombination in crosses, not even in organisms with biparental plastid inheritance However, especially in cell fusion experiments ptDNA recombination was occasionally seen e. It appears likely that recombination between plastomes in sexual crosses of seed plants is largely prevented by the absence of plastid fusion in the zygote 46 , 47 , This is in contrast to Chlamydomonas , where plastid fusion occurs after syngamy.
Organelle recombination of plant mitochondrial genomes was repeatedly demonstrated in protoplast fusion 3 , 65 , and preliminary evidence for recombination in sexual crosses has also been obtained If biparental transmission occurs, sexual recombination of plant mtDNA is expected, because plant mitochondria regularly undergo fusion and fission , and homologous recombination events seem to occur frequently in mitochondrial genomes , In contrast to plants and fungi reviewed in 20 , occurrence and evolutionary relevance of mitochondrial genome recombination in animals are still controversial.
Mixed evidence is available in that recombination was detected in some animal species, but not in others 2 , 15 , , The general presence of sexual oDNA recombination has gained some support from investigations of natural populations. Circumstantial phylogenetic evidence points to sexual recombination in both plant and animal systems, but the currently available data are still sparse and a bit controversial 1 , 3 , 15 , 18 , While genetic studies in natural populations of campion genus Silene suggest presence of recombination 19 , somewhat contradicting evidence has been obtained for fruit flies and fungi 91 , More rigorous and systematic investigations of oDNA recombination in natural populations and hybrid zones are needed that, for example, also take into account the possibility of selection against recombinant genotypes.
In summary, it seems possible that sexual recombination of oDNA is widespread and perhaps even a general phenomenon.
As paternal leakage of plastids occurs at least occasionally in many, if not all, species, sexual recombination of plastids in seed plants may be limited by the rarity of plastid fusion events. In contrast, the limiting factor in sexual recombination of mtDNA may be paternal leakage and reduced recombination ability, at least in some animal taxa, most notably in mammals cf. It is noteworthy in this respect that mammalian mitochondrial genomes have considerably higher nucleotide substitution rates than plastid genomes and plant mitochondrial genomes.
Interestingly, plant mitochondria, which are likely subject to paternal leakage and regularly undergo fusion and mtDNA recombination, display one of the lowest nucleotide substitution rates known in nature 51 , However, whether or not oDNA recombination frequencies in all organisms, and especially in mammalian mitochondria and seed plant plastids, are high enough to overcome Muller's ratchet, remains to be determined see main text. Another common posit is that uniparental inheritance has evolved to avoid the spread of selfish cytoplasmic elements.
Some solid datasets are available for competition between organelle genomes in both plant and animal systems. Examples have come from cell fusion events, oDNA mutants and sexual crosses 6 , 12 , 18 , 67 , For example, in evening primroses, plastids display different multiplication speeds in sexual crosses depending on the plastid genotype If the avoidance of competition between organelles was the major driving force for the evolution of uniparental inheritance, a replication race between oDNAs must be harmful to the nucleus.
Although some human diseases are associated with altered mtDNA copy numbers 69 , in most eukaryotic systems studied so far, the amounts of oDNA versus nuclear DNA remain constant within a rather narrow range and are likely under nuclear control 1 , 12 , 69 - Hence, it appears unlikely that solely differences in oDNA replication speeds provide sufficient driving force for the evolution of uniparental inheritance. Tools Request permission Export citation Add to favorites Track citation.
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Institutional Login. Log in to Wiley Online Library. Purchase Instant Access. View Preview. Learn more Check out. Abstract The work of mitochondria and chloroplasts is energy transduction in respiration and photosynthesis. Citing Literature. Volume 27 , Issue 4 April Pages Related Information.
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The Cytoplasm and Cellular Organelles – Anatomy and Physiology
The eukaryotic mitochondrion is derived from a proteobacterial endosymbiotic ancestor but most of the genes that were originally present in this ancestor's genome have been transferred to the nucleus thick black arrow , with only a small number being retained in the organelle blue circle. Similarly, most of the genes from the cyanobacterial endosymbiont ancestor of the chloroplast were also transferred to the nucleus thick black arrow. The dotted arrows indicate how DNA of mitochondrial blue and chloroplast green origin is still being transferred to the nucleus.
Chloroplast and nuclear sequences are also found in the mitochondrial genome but little or no promiscuous DNA is located in the chloroplast. Comments Close.