RESEARCH-PGR: The Cytonuclear Dimension of Allopolyploidy

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One of the key realizations of the genomics era is that all plants, including our major crop plants, have histories of genome duplication in which the DNA content inside cells is doubled (polyploidy). Although much has been learned about the consequences of genome doubling in recent years, many fundamental questions remain regarding how genome duplication contributes to plant biology and crop productivity. An important dimension of genome duplication is how the now-doubled nuclear genome interacts with other genomic compartments found within the plant cell, such as the mitochondria and plastids. The planned research will investigate this underexplored aspect of genome duplications, with implications for how cellular energetics, which play a key role in growth, reproduction, and yield, are altered in the wake of genome doubling events. The research will use a diverse panel of important crop systems and state-of-the-art genomics techniques. Project resources, data, and personnel will be used to expand outreach and education programs, including an international workshop series on genomics and a long-term effort to provide high school teachers with an immersive experience in hands-on research and curricular development. The project will create training opportunities for participants across the full range of educational and career stages in both research and service-learning. In sum, this research aims to provide fundamental insights into genome interactions and crop biology and broaden participation in plant biological research.Allopolyploidy events entail the simultaneous merger of genomes from two divergent lineages combined with the doubling of nuclear genome content. Because cytoplasmic genomes are typically inherited from only a single (maternal) parent, allopolyploidization is expected to have complex effects on the relative copy number (i.e., stoichiometry) of nuclear and cytoplasmic genomes, and also create novel, "untested" pairings of nuclear and cytoplasmic genotypes. The planned research will reveal the spectrum of genomic responses that alleviate the disruptive effects of allopolyploidy on cytonuclear interactions and facilitate the successful establishment of hybrid/polyploid lineages. Bioinformatic analyses will test for predicted compensatory responses in organelle-targeted nuclear genes that resolve maladapted interactions between the paternally derived nuclear subgenome and maternally derived cytoplasmic genomes, including: (1) maternally biased gene conversion; (2) altered selection pressures on sequence evolution in the paternal subgenome; (3) paternally biased pseudogenization and gene loss; and (4) preferential down-regulation of paternal homoeologs. By taking advantage of 600 re-sequenced genomes from cotton allopolyploids, the proposed research will be extended to the population-genomic level to detect these effects "in action". Finally, the relative copy number of nuclear vs. cytoplasmic genomes and the relative expression levels in the nucleus, mitochondria, and plastids will be precisely quantified to differentiate among multiple hypothesized responses to stoichiometric imbalance. Together, these analyses will provide a powerful test of whether and how cytonuclear interactions contribute to the formation and evolution of polyploid crops.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.