The Spatiotemporal Dynamics of Nutrient Exchange at the Arbuscule

Plants are the major primary producers, source of biomass, and defining feature of ecosystems on Earth. But their ability to fix carbon is only half the story: plant growth also requires a suite of mineral elements that usually exist at limiting-levels in the soil. Most land plant species rely on a symbiotic partnership with arbuscular mycorrhizal (AM) fungi to meet this nutrient demand. AM symbiosis involves the fungus-to-plant transfer of phosphorus and nitrogen, and the reciprocal plant-to-fungus transfer of carbon at specialised structures within plant root cells, the arbuscules. While many studies have evidenced the AM-mediated transfer of these nutrients, the spatial and temporal elements remain largely unknown. This is significant because AM symbiosis is highly dynamic and heterogenous, from the scale of a single arbuscule up to the level of a colonised root system. This PhD work therefore aimed to uncover the spatiotemporal dynamics of nutrient exchange at the arbuscule during AM symbiosis. Fluorescent reporter lines in rice and novel microscopy techniques were developed to follow the localisations of AM-specific nutrient transporter proteins throughout arbuscule lifetime. Reporters for OsPT11, responsible for fungus-to-plant phosphate transport, revealed highly specific expression-timing and localisation, largely coinciding with arbuscule branching, which are essential for functional AM symbiosis. Surprisingly, OsAMT3;1, responsible for ammonium transport in the same direction, showed a longer window of expression and broader spatial distribution, suggesting the absence of a universal time or domain of nutrient exchange. This was augmented by a further set of unique dynamics shown by the lipid transporters OsSTR1 and OsSTR2, responsible for the opposite direction of transport. OsSTR1/OsSTR2 localised to the arbuscule earlier than OsPT11, but lipid export was not essential for OsPT11 or OsAMT3;1 expression. Variation in relative abundance of each nutrient transporter at the arbuscule was consistently observed, and was found to be responsive to plant nutrient status. Together, these results paint a picture of distinct co-ordination of symbiotic phosphorus, nitrogen, and carbon transporters, with arbuscules representing functionally unique structures as opposed to identical units of nutrient exchange. Additional to answering biological questions, the micrographs produced during this work were re-purposed to engage the public with AM symbiosis. The final chapter of this thesis discusses the potential of scientific visual data to increase awareness, appreciation, and knowledge of ‘overlooked organisms’, combining examples from the literature with outreach work carried out during this PhD. The resulting benefits are highlighted, providing inspiration and motivation for researchers to share their images beyond academia.

Cambridge Commonwealth, European & International Trust; St John's College, University of Cambridge; Department of Plant Sciences, University of Cambridge