Epigenetic regulation of sexual lineage development in plants

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A key characteristic of life is the ability to reproduce. Reproductive strategies are major contributors to evolutionary fitness and can vary substantially between species. Like humans, most flowering plants reproduce sexually by mating with another individual; however, unlike humans, plants typically possess both male and female organs, and many plant species, including major crops, are capable of self-fertilization. Sexual reproduction in flowering plants is important to mankind as it produces the seeds that comprise most of our staple food. With decreasing arable land, an exploding population and global climate change, feeding the world in the 21st century will require a step-change in the efficiency of seed production, and this can only come from a deeper understanding of plant reproductive development. Sexual reproduction in plants is carried out by two highly specialized families of cells, here called the male and female sexual lineages (SLs). A fundamental but still unresolved question that has always fascinated me is how SL function and fate are installed and maintained precisely in these cell lineages. My DPhil and postdoctoral studies focused on how genetic and 'epigenetic' pathways contribute to SL function and fertility. 'Epigenetic' regulation - such as DNA methylation - is named after its ability to alter gene expression by modifying the state of DNA without changing its genetic sequence. Recently, I discovered that the RNA-directed DNA methylation (RdDM) pathway regulates SL development in Arabidopsis plants by controlling the expression of several hundred genes. Consistent with the importance of the RdDM pathway in SL development, its mutations cause defects in SL development in both Arabidopsis and maize. My proposed research integrates plant developmental, molecular, genetics and epigenetics biology to investigate how RdDM installs reproductive function and fate in the male SL of the model plant Arabidopsis thaliana. To detect changes in the DNA methylation and gene expression, I have developed state-of-the-art techniques such as fluorescence-activated cell sorting and micromanipulation to isolate all types of male SL cells to high purity. I will use whole-genome sequencing of these SL cells from RdDM mutants to pinpoint the function of the SL-specific RdDM pathway, and a combination of genetics and developmental biology to determine how the genes controlled by the SL-specific RdDM regulate SL development. Finally, through a combination of genomics, developmental biology and mutant screens, I will decipher the mechanism by which RdDM is directed to genes in the SL.This multi-disciplinary program of work will deepen our understanding of male SL development and function by identifying a number of key genetic and epigenetic regulators. Due to the significant parallels between male and female SL development, and because discoveries in the model plant Arabidopsis have been routinely translated into major crops such as rice and maize, these insights will be widely applicable and may be used to improve crop fertility and yield. At a more generic level, my work will demonstrate, for the first time, how epigenetic pathways can be tailored in a specific lineage of cells to convey precise biological functions. This kind of developmental regulation likely affects many biological processes in a wide range of cell types and tissues. I therefore believe that my work will lay a foundation for the study of epigenetic regulation of plant development. Many DNA methylation mechanisms are highly conserved between Arabidopsis and mammals, and recent evidence points to a role for DNA methylation in directing the differentiation of human cell lines. Insights from this work thus have the potential to shed light on the regulation of lineage development by DNA methylation in mammals, which is important to combat DNA methylation-related human diseases such as cancer.