Determining how Magnaporthe oryzae senses turgor pressure to trigger rice blast disease

Lauren S. Ryder 1 Yasin F. Dagdas 1,4 Michael J. Kershaw 1 Chandrasekhar Venkataraman 2,3 Anotida Madzvamuse 3 Darren M. Soanes 1 Miriam Oses-Ruiz 1 Vanessa Styles 3 Jan Sklenar 4 Frank L.H. Menke 4 Nicholas Talbot 1
1Biosciences, University of Exeter, Exeter, UK
2School of Mathematics and Statistics, University of St. Andrews, North Haugh, UK
3School of Mathematics and Physical Sciences, University of Sussex, Brighton, UK
4Norwich Research Park, The Sainsbury Laboratory, Norwich, UK

Plant pathogenic fungi cause many of the world’s most devastating crop diseases, and pose a significant threat to global food security. With up to 30% of the global harvest lost each year to plant disease, it is paramount to identify affordable and durable solutions to increase plant productivity in a sustainable way. Rice blast disease caused by the fungus Magnaporthe oryzae is found in all rice-growing regions of the world, and is responsible for 10-30% loss of the global rice harvest annually. M. oryzae develops a specialised infection cell called an appressorium, which is a unicellular dome-shaped cell that forms soon after spore germination on the leaf surface, and is characteristic of many cereal pathogens. This together with the genetic tractability makes M. oryzae a model organism for studying host-pathogen interactions. To cause plant disease, the appressorium develops enormous turgor of up to 8.0MPa, by accumulating high concentrations of glycerol. The appressorium has a differentiated cell wall rich in melanin, which is essential for turgor generation. This is rapidly translated into mechanical force allowing a narrow penetration hypha to emerge from the base of the appressorium, rupturing the rice leaf cuticle and cause disease. Development and re-polarisation of the appressorium requires four septin GTPases, Sep3, Sep4, Sep5 and Sep6 which form a toroidal, heterooligomeric complex at the base of the appressorium that re-models and re-organises the F-actin cytoskeleton to the precise point at which plant infection occurs. Septin-mediated plant infection is controlled by NADPH oxidase activity. A specialised Nox2-NoxR NADPH oxidase is necessary for septin-mediated control of actin dynamics. Here, we present a model that shows how the fungus is able to monitor the turgor pressure within the appressorium and determine the optimal point which triggers its puncturing of the rice leaf cuticle to cause rice blast disease.