This research project will expand our understanding of the causes and consequences of an unusual form of inheritance in plants, the transmission of organelles through pollen. A defining feature of cells with nuclei is the existence of organelles that have separate genomes. The nuclear genome is generally inherited from two parents. By contrast, the genomes of organelles, such as those in mitochondria, are nearly always inherited from the mother only. However, we know little about the frequency and cause of deviations from this general rule. Understanding the inheritance of organelle genomes is therefore important for understanding evolutionary processes. Using the plant Silene vulgaris as a model system, this project will explore the relationship between the geographic origins of the nuclear genome and paternal mitochondrial transmission, and the relationship between the physical structure of the mitochondrial genome and the propensity for mitochondrial genes to recombine, will be studied. This requires 1) sequencing several S. vulgaris mitochondrial genomes to document genome structure and identify genetic markers used to study recombination, 2) genotyping individuals from natural populations in order to estimate recombination, 3) conducting experimental crosses between individuals of varying nuclear and mitochondrial genotypes, and 4) genotyping their offspring to identify incidences of mitochondrial paternal inheritance.
In addition to furthering fundamental knowledge of plant mitochondrial genome biology, the results should be of applied significance. Plant breeders are concerned with developing CMS (cytoplasmic male sterility) resources because utilization of male-sterile individuals in breeding programs increases efficiency, and CMS genes usually reside in the mitochondrial genome. Studies of the inheritance of organellar genomes are also valuable because of concerns about gene escape from genetically modified organisms.
The primary defining feature of higher animals, plants and fungi, the so-called eukaryotes, is that their cells contain membrane-bound structures that perform various cellular functions (organelles). Organelles can have their own genetic information (or genomes) that can be passed on to their offspring using very different modes of inheritance. The nucleus, for example, carries a large, complex genome that in many organisms is transmitted to the offspring from both parents. This process generally involves sexual reproduction, where the genomes of the two parents recombine to produce genetically unique and highly variable offspring. By contrast, most mitochondrial genomes are transmitted directly from the mother to her offspring, without sexual reproduction. These fundamental differences are thought to have profound effects on the size, structure and hence the remarkable diversity of eukaryotic genomes. Recent research in a variety of organisms, including humans, suggests that mitochondrial genomes can be transmitted from both parents and undergo genetic recombination. Even if such sexual reproduction is very rare, it can have profound effects on the genetics and evolution of mitochondrial genomes. This project addressed two fundamental questions, is the mitochondrial genome truly asexual, and if not, what are the genetic and evolutionary consequences? This research was a collaboration with David McCauley at Vanderbilt University, using the plant, Silene vulgaris, as a model system. The McCauley and Taylor laboratories have worked together on previous projects involving the population genetics of invasive species as well as the genetic diversity of mitochondrial genomes. The McCauley laboratory discovered instances of paternal transmission of the mitochondrial genome and recruited the Taylor laboratory to apply the tools of genomics to study the process in greater detail. Specifically, we discovered that paternal transmission occurred at high frequencies in regions of North America where distinct European lineages were coming together and hybridizing. We therefore set out to test the hypothesis that the molecular mechanisms that enforce maternal transmission break down when divergent lineages hybridize. We used high throughput sequencing technologies to sequence the mitochondrial genomes of several families within the species, Silene vulgaris. We showed that the mitochondrial genome is rapidly changing through time, with extreme diversity in gene content and gene order among individual families. We used the sequence information to develop high throughput assays that detect single nucleotide polymorphisms (or SNPs) throughout the mitochondrial genome. We detected significant recombination in the mitochondrial genome, evidenced by a breakdown in the statistical associations among SNPs in different mitochondrial genes. The data provided evidence for infrequent, but genetically significant, recombination within the mitochondrial genome. Our findings demonstrate that rare genetic recombination can render the mitochondrial genome effectively sexual. This predicts, for example, that the mitochondrial genome in Silene vulgaris will not be vulnerable to the mutational meltdown that is thought to afflict the genomes of asexual species. Also, the reshuffling of genes in the mitochondrial genome may create new genetic variants, thus facilitating adaptation to novel environments. Future research will explore what mechanisms cause certain mitochondrial genomes to recombine, and how widespread infrequent but genetically significant mitochondrial recombination is in nature.
