MagicSpore · Mechanisms and biological functions of H3K27me3 reprogramming in plant microspores

How totipotency is established in germ cells is an essential question in reproductive biology. In the plant male germline, the haploid meiotic products microspores are totipotent, which permits crop breeding via microspore embryogenesis. However, the molecular basis and biological significance of microspore totipotency are unknown. More generally, our understanding of plant cell totipotency is in its infancy. My lab established the Arabidopsis male germline as a model to study germline epigenetic reprogramming. We recently discovered that H3K27me3, a histone modification essential for developmental regulation, is globally erased in microspores. We also identified a new family of histone H2A deubiquitinases (GDUs), and our results suggest that the GDUs and a histone H3 variant (H3.15) gradually remove H3K27me3 during microspore development. I hypothesize that global H3K27me3 erasure facilitates the diploid to haploid transcriptional shift, establishes cellular totipotency, and allows the two identical sperm cells within a pollen grain to initiate the development of distinct seed structures (embryo and endosperm). We will leverage our recent discoveries, as well as state-of-the-art technologies, to study in-depth the epigenetic basis of microspore totipotency and its biological functions, via these aims: 1) determine the timing, scope and functions of H3K27me3 reprogramming in microspores; 2) understand the role of histone H3.15 and GDUs in H3K27me3 reprogramming; 3) alter microspore regeneration ability by manipulating H3K27me3 reprogramming; 4) elucidate the contribution of global H3K27me3 erasure to double fertilization. Our outputs will revolutionize our understanding of plant cellular totipotency and sexual reproduction, and elucidate novel strategies to enhance microspore embryogenesis in recalcitrant crops. These insights will in turn reveal core principles governing epigenetic regulation of sexual reproduction in eukaryotes.