Female and male gamete mitochondria are distinct and complementary in transcription, structure, and genome function.

Respiratory electron transport in mitochondria is coupled to ATP synthesis while generating mutagenic oxygen free radicals. Mitochondrial DNA mutation then accumulates with age, and may set a limit to the lifespan of individual, multicellular organisms. Why is this mutation not inherited? Here we demonstrate that female gametes-oocytes-have unusually small and simple mitochondria that are suppressed for DNA transcription, electron transport, and free radical production. By contrast, male gametes-sperm-and somatic cells of both sexes transcribe mitochondrial genes for respiratory electron carriers and produce oxygen free radicals. This germ-line division between mitochondria of sperm and egg is observed in both the vinegar fruitfly and the zebrafish-species spanning a major evolutionary divide within the animal kingdom. We interpret these findings as an evidence that oocyte mitochondria serve primarily as genetic templates, giving rise, irreversibly and in each new generation, to the familiar energy-transducing mitochondria of somatic cells and male gametes. Suppressed mitochondrial metabolism in the female germ line may therefore constitute a mechanism for increasing the fidelity of mitochondrial DNA inheritance.

Mitochondrial genome function and maternal inheritance.

The persistence of mtDNA to encode a small subset of mitochondrial proteins reflects the selective advantage of co-location of key respiratory chain subunit genes with their gene products. The disadvantage of this co-location is exposure of mtDNA to mutagenic ROS (reactive oxygen species), which are by-products of aerobic respiration. The resulting 'vicious circle' of mitochondrial mutation has been proposed to underlie aging and its associated degenerative diseases. Recent evidence is consistent with the hypothesis that oocyte mitochondria escape the aging process by acting as quiescent genetic templates, transcriptionally and bioenergetically repressed. Transmission of unexpressed mtDNA in the female germline is considered as a reason for the existence of separate sexes, i.e. male and female. Maternal inheritance then circumvents incremental accumulation of age-related disease in each new generation.

Energy, ageing, fidelity and sex: oocyte mitochondrial DNA as a protected genetic template.

Oxidative phosphorylation couples ATP synthesis to respiratory electron transport. In eukaryotes, this coupling occurs in mitochondria, which carry DNA. Respiratory electron transport in the presence of molecular oxygen generates free radicals, reactive oxygen species (ROS), which are mutagenic. In animals, mutational damage to mitochondrial DNA therefore accumulates within the lifespan of the individual. Fertilization generally requires motility of one gamete, and motility requires ATP. It has been proposed that oxidative phosphorylation is nevertheless absent in the special case of quiescent, template mitochondria, that these remain sequestered in oocytes and female germ lines and that oocyte mitochondrial DNA is thus protected from damage, but evidence to support that view has hitherto been lacking. Here we show that female gametes of Aurelia aurita, the common jellyfish, do not transcribe mitochondrial DNA, lack electron transport, and produce no free radicals. In contrast, male gametes actively transcribe mitochondrial genes for respiratory chain components and produce ROS. Electron microscopy shows that this functional division of labour between sperm and egg is accompanied by contrasting mitochondrial morphology. We suggest that mitochondrial anisogamy underlies division of any animal species into two sexes with complementary roles in sexual reproduction. We predict that quiescent oocyte mitochondria contain DNA as an unexpressed template that avoids mutational accumulation by being transmitted through the female germ line. The active descendants of oocyte mitochondria perform oxidative phosphorylation in somatic cells and in male gametes of each new generation, and the mutations that they accumulated are not inherited. We propose that the avoidance of ROS-dependent mutation is the evolutionary pressure underlying maternal mitochondrial inheritance and the developmental origin of the female germ line.

Chloroplast-mitochondria cross-talk in diatoms.

Diatoms are unicellular, mainly photosynthetic, eukaryotes living within elaborate silicified cell walls and believed to be responsible for around 40% of global primary productivity in the oceans. Their abundance in aquatic ecosystems is such that they have on different occasions been described as the insects, the weeds, or the cancer cells of the ocean. In contrast to higher plants and green algae which derive from a primary endosymbiosis, diatoms are now believed to originate from a serial secondary endosymbiosis involving both green and red algae and a heterotrophic exosymbiont host. As a consequence of their dynamic evolutionary history, they appear to have red algal-derived chloroplasts empowered largely by green algal proteins, working alongside mitochondria derived from the non-photosynthetic exosymbiont. This review will discuss the evidence for such an unusual assemblage of organelles in diatoms, and will present the evidence implying that it has enabled them with unorthodox metabolisms that may have contributed to their profound ecological success.

A structural phylogenetic map for chloroplast photosynthesis.

Chloroplasts are cytoplasmic organelles and the sites of photosynthesis in eukaryotic cells. Advances in structural biology and comparative genomics allow us to identify individual components of the photosynthetic apparatus precisely with respect to the subcellular location of their genes. Here we present outline maps of four energy-transducing thylakoid membranes. The maps for land plants and red and green algae distinguish protein subunits encoded in the nucleus from those encoded in the chloroplast. We find no defining structural feature that is common to all chloroplast gene products. Instead, conserved patterns of gene location are consistent with photosynthetic redox chemistry exerting gene regulatory control over its own rate-limiting steps. Chloroplast DNA carries genes whose expression is placed under this control.

MutS HOMOLOG1 is a nucleoid protein that alters mitochondrial and plastid properties and plant response to high light.

Mitochondrial-plastid interdependence within the plant cell is presumed to be essential, but measurable demonstration of this intimate interaction is difficult. At the level of cellular metabolism, several biosynthetic pathways involve both mitochondrial- and plastid-localized steps. However, at an environmental response level, it is not clear how the two organelles intersect in programmed cellular responses. Here, we provide evidence, using genetic perturbation of the MutS Homolog1 (MSH1) nuclear gene in five plant species, that MSH1 functions within the mitochondrion and plastid to influence organellar genome behavior and plant growth patterns. The mitochondrial form of the protein participates in DNA recombination surveillance, with disruption of the gene resulting in enhanced mitochondrial genome recombination at numerous repeated sequences. The plastid-localized form of the protein interacts with the plastid genome and influences genome stability and plastid development, with its disruption leading to variegation of the plant. These developmental changes include altered patterns of nuclear gene expression. Consistency of plastid and mitochondrial response across both monocot and dicot species indicate that the dual-functioning nature of MSH1 is well conserved. Variegated tissues show changes in redox status together with enhanced plant survival and reproduction under photooxidative light conditions, evidence that the plastid changes triggered in this study comprise an adaptive response to naturally occurring light stress.

Participation of leaky ribosome scanning in protein dual targeting by alternative translation initiation in higher plants.

Postendosymbiotic evolution has given rise to proteins that are multiply targeted within the cell. Various mechanisms have been identified to permit the expression of proteins encoding distinct N termini from a single gene. One mechanism involves alternative translation initiation (aTI). We previously showed evidence of aTI activity within the Arabidopsis thaliana organellar DNA polymerase gene POLgamma2. Translation initiates at four distinct sites within this gene, two non-AUG, to produce distinct plastid and mitochondrially targeted forms of the protein. To understand the regulation of aTI in higher plants, we used Polgamma2 as a model to investigate both cis- and trans-acting features of the process. Here, we show that aTI in Polgamma2 and other plant genes involves ribosome scanning dependent on sequence context at the multiple initiation sites to condition specific binding of at least one trans-acting factor essential for site recognition. Multiple active translation initiation sites appear to operate in several plant genes, often to expand protein targeting. In plants, where the mitochondrion and plastid must share a considerable portion of their proteomes and coordinate their functions, leaky ribosome scanning behavior provides adaptive advantage in the evolution of protein dual targeting and translational regulation.