Horizontal Gene Transfer in Multicellular Eukaryotes

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DESCRIPTION (provided by applicant): Horizontal gene transfer (HGT) is now recognized as a major evolutionary genetic force driving genomic and phenotypic change in the microbial world -- throughout prokaryotes and in many unicellular eukaryotes (all phagotrophic protists). We and others recently discovered the first evidence for widespread HGT within any group of multicellular eukaryotes, finding that horizontal transfer of mitochondrial genes in plants is both frequent and recent. Many of these transfers yield mitochondrial gene duplications (of vertically and horizontally transmitted homologs), whereas others lead to strikingly chimeric genes (part horizontal/part vertical) or repopulate the genome with genes previously transferred to the nucleus. Some of the transferred genes are intact, expressed, and probably functional. One mitochondrial genome has already been identified with multiple, perhaps many horizontally acquired genes. The goal of this study is to build on these exciting findings and conduct the first comprehensive and rigorous study of HGT in multicellular eukaryotes. Because HGT is a fundamental but poorly understood process in genome evolution, these studies will provide an important new perspective on genome structure and function. The maintenance of an intact, functioning genome is critical for human health, and understanding mechanisms of gene exchange is important to the development of gene therapy. This project focuses on plant mitochondrial genomes because their exceptional propensity for HGT and several other attributes make them a model system for investigating HGT in eukaryotes. Studies include targeted macroarray screens of 4000 plants, all-gene sequencing in 200 diverse plants, whole-genome sequencing in 15 plants with exceptionally extensive HGT, and various follow-up studies on specific cases of high interest from the above. Results will address numerous questions concerning rates, patterns, extents, chimeric consequences, donor/recipient relationships, functionality, and mechanisms of HGT across many lineages of plant mitochondrial genomes. Certain of the mechanistic studies follow from emerging evidence suggesting that certain plants and genes are unusually prone to HGT and that a common mechanism of transfer is physical penetration between parasitic plants and their host plants.