Mitonuclear interactions and coevolution in the dynamic plant mitochondrial tRNA pool

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Basic biological functions depend on direct molecular interactions between gene products. Although the intimacy of such interactions has led to highly coevolved and integrated sets of genes, some systems demonstrate remarkable lability, essentially swapping gene products as “interchangeable parts” or rewiring entire networks of molecular interactions. This project will use the diverse pool of plant mitochondrial transfer RNAs (tRNAs) and the associated network of tRNA-processing enzymes as a model to understand how molecular systems respond when one gene is lost and functionally replaced by another. The research will provide training at the undergraduate, graduate, and postdoctoral levels in bioinformatics, molecular genetics, and evolutionary biology. It will also be coupled with outreach efforts and programs for first-year undergraduates to broaden access to career opportunities in computational biology.In some plant lineages, including the angiosperm genus Silene, there is an ongoing process of tRNA gene loss from the mitochondrial genome and functional replacement by import of nuclear-encoded tRNAs from the cytosol. These replacements amount to exchanging bacterial-like (mitochondrial) genes for archaeal-like (nuclear) genes that are separated by billions of years of evolution. It is not clear how these changes occur without disrupting the essential functions of mitochondrial translation systems because the maturation and charging of tRNAs depends on specific interactions with a number of nuclear-encoded enzymes (e.g., aminoacyl-tRNA synthetases). This project will use genomic, transcriptomic, and experimental approaches to investigate how tRNA-processing enzymes change in amino acid sequence and subcellular targeting in Silene species with different histories of recent tRNA gene loss/replacement. The work will distinguish between two alternative hypotheses: 1) that existing mitochondrial enzymes have evolved to act on cytosolic tRNAs as new substrates, or 2) that cytosolic enzyme networks have been retargeted to the mitochondria, maintaining their functional relationship with the newly imported cytosolic tRNAs.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.