We are interested in mechanisms that generate and maintain heritable phenotypic variation. Our current emphasis is aimed at understanding epigenetic systems that cause mitotically, and meiotically, heritable changes in gene activity. We are focusing on one particular mechanism, called paramutation, in which the regulation of one allele is heritably altered through interactions with the homologous allele. We are asking several key questions: what is the molecular nature of this meiotically heritable change, how does this change affect gene expression, how do two alleles communicate with each other, and how general is this mechanism in plant growth and development? We use the superb genetic, molecular genetic, cytogenetic, and cytological tools available in Zea mays to address these questions.

Our general strategy is to identify molecular and cellular components required for paramutation and then use these as tools to further understand the genomic and chromosome dynamics involved. We use the well-defined anthocyanin pigment pathway as our simple model system. Plant color in maize is quantitatively controlled by action of the purple plant1 (pl1) gene. One particular pl1 allele (Pl) can exist in distinct transcription states. In the figure to the right, note tassels of sibling maize plants displaying two distinct epigenetic expression states of the pl1 gene. Darkly colored anthers reflect high levels of pl1 transcription and lightly colored anthers indicate a repressed transcription state.

Highly transcribed Pl alleles are invariably repressed when exposed to a repressed Pl allele (Pl’) in a heterozygote. Genetic and molecular observations suggest that paramutation reflects alterations in chromatin structure that are sensitive to chromosome pairing interactions.

We’ve begun to identify important components of the paramutation system using genetic analyses. Seedling-based screens have identified mutations in critical cis-acting sequences and a novel class of trans-acting rmr (required to maintain repression) loci that allow heritable restoration of high levels of pl1 gene action. Several rmr genes also play crucial roles in growth and development. Cloning of these rmr loci by positional approaches has begun to highlight novel features of a presumed small RNA-directed DNA methylation pathway that affect meiotically heritable changes in epigenomic control. In addition to cloning the remaining rmr genes, we are currently taking both biochemical and genomic approaches to understand the operation of this novel regulatory system in plant development and homeostasis.