Elucidating the role and regulation of heterochromatin during maize reproduction, and its potential for developing novel plant breeding strategies.

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Sequence information (the genome) determines phenotypic outcome, but depends on a proper chromatin environment (the epigenome) for both the transcriptional competence of genes, and the organization of the genome. The epigenome is thus of great interest for fundamental as well as translational research. Arabidopsis has thus far provided most of our understanding of epigenetic regulation in plants. It is, however, an unusual plant with a small genome and few repetitive elements, in sharp contrast to most crops, whose epigenomes differ from the Arabidopsis paradigm in both structural and mechanistic terms. Importantly, altering the epigenome in crops, particularly in maize, has strong developmental consequences, while Arabidopsis is highly resilient to epigenomic instability. Reproductive development is central to plant breeding, yield, and hence food security. Yet, the mechanisms controlling epigenome function and dynamics during plant reproduction remain understudied in food crops. Many laboratories have shown that chromatin-level regulations are important for reproductive success. We, and others, have hinted that heterochromatin in particular, which encompasses most of the repeated fraction of the genome, plays an important role in plant reproduction. This is especially clear in species with complex genomes, where the disruption of enzymes that control heterochromatin results in altered reproductive development, including abnormal meiosis, and tendencies toward apomixis, a widely recognized but unrealized goal in plant breeding that would greatly benefit farmers and breeders. In this proposal, we posit that heterochromatin acts as a stabilizer of reproductive development, and that altering heterochromatin results in more flexible reproductive outcomes, of potential value for breeding. We thus propose to elucidate the role and regulation of heterochromatin during reproduction, using maize as our model, and focusing on two aspects of reproduction: meiosis and early embryogenesis. We will then assess the consequences of altered heterochromatin on two traits: recombination rates, and the potential for clonal reproduction. Maize is a key crop worldwide, and an exceptional model to address the interplay between genetics and epigenetics, owing to a long history of epigenetic research, many mutants affecting epigenetic determinants, and an exceptional cytology. This project relies on a collection of maize mutants affecting heterochromatin, the strong experience of the participants in epigenomic and plant reproduction, novel methods to analyze epigenomic information in living cells, and a strong body of preliminary data showing that heterochromatin can be genetically and epigenetically manipulated through mutation and recombination. We will combine these elements to assess the functional importance of heterochromatic pathways in shaping maize reproductive outcomes, and derive novel tools for plant breeding.