How complex multicellular organisms develop from a single cell into a fully-fledged living being is a fundamental and fascinating question in biology. For many years we exploited pollen as a developmental model system to address this key question, helping uncover the molecular basis for sperm development in flowering plants and the nature of epigenetic reprogramming that drives plant life cycle transitions. We are now applying our expertise in red algae, where the relevance and function of molecular processes underlying development and reproduction is poorly understood.
Sperm specification in flowering plants
Each pollen grain in flowering plants will deliver two embedded sperm cells to initiate seed development, a process that is essential for plant fertility and crop production. We helped uncover a module of sperm-specific transcription factors - DUO1 [link] and DAZ1/DAZ2 [link] - that act in concert to coordinate a genetic framework that is essential for sperm formation and seed development in Arabidopsis.
Resetting epigenetic memory in sperm chromatin
Precisely how the paternal epigenome is reprogrammed in flowering plants was for a long time unclear since, unlike most animals, DNA is not demethylated and histones are retained in sperm. We revealed how the epigenetic memory mediated by H3K27me3 is reset in Arabidopsis sperm to license sperm specification and prime early seed development. This occurs through a multi-layered mechanism involving the silencing of H3K27me3 ‘writers’, the activity of H3K27me3 ‘erasers’ and deposition of the sperm-specific histone H3.10.
Epigenetic reprogramming drives plant life cycle transitions
The life cycle of most plants and algae alternates between two distinct life forms - a haploid form with a single copy of the genome and a diploid form with two. Pollen represents the haploid form in flowering plants and is subject to extensive epigenetic reprogramming, resulting in two cell types with a different chromatin configuration and vastly differing fate.
We showed how the reprogramming of histone H3K9 and DNA methylation in the companion cell of the pollen grain rewires haploid gene expression and thus licenses the diploid-to-haploid transition. This acts in parallel with H3K27me3 reprogramming in sperm, which in contrast prepares for diploid gene expression in the next generation, thus licensing the haploid-to-diploid transition.
Reproduction and development in red algae
Red algae are the ancient cousins of modern-day plants that play an essential role in aquatic ecosystems around the planet. They have played a key role in the evolution of life by being the ancient donor of plastids to other major groups of algae like dinoflagellates, diatoms and brown algae. Red algae have some of the most complex and fascinating life cycles known in living organisms, which involves specialised structures that mediate a highly sophisticated mode of sexual reproduction that rivals that seen in land plants.
We are actively developing a burgeoning model organism for red algae to address these over-arching questions. We aim to shed light on the molecular biology of red algal development through genetic and epigenetic investigations using cutting-edge cell biology, biochemistry, epigenetic and evolutionary biology approaches.