On the nature and regulation of the plant-fungal biotrophic interface

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During plant infection, many pathogenic fungi, including the devastating rice and wheat blast fungus Magnaporthe oryzae, can grow in intimate contact with living host cells for extended periods of time. This parasitic (biotrophic) growth stage involves the accretion of host plant membranes around fungal invasive hyphae, forming interfacial zones across which effectors are deployed and nutrients are acquired. Despite the intrinsic nature of the biotrophic interface and associated compartments to host infection, the biological underpinnings of interfacial membrane maintenance and construction are largely unknown. This severely undermines efforts to understand the host-pathogen interaction and likely obscures novel sources of host resistance and the identification of new targets for limiting a broad range of plant diseases as well as improving crop health. This project seeks to address these knowledge gaps by characterizing mutant strains of M. oryzae that fail to properly maintain biotrophic interfacial function or membrane integrity during growth in host plant cells. This is expected to uncover novel cellular, biochemical, and genetic mechanisms governing rice infection. Results may shed light on fundamental concepts of plant host-microbe interactions that could be leveraged to understand how beneficial plant-fungal interactions might be promoted while those detrimental to crop health are diminished. We also expect that this work will provide an invigorating environment for student learning that will inspire underrepresented students to consider a STEM career and become the next generation of scientists.Based on our recent discoveries, our central hypothesis is that, despite comprising both plant and fungal membranes, biotrophic interfaces are fungal constructs with properties and dynamics dictated by the metabolic demands of the invading fungus. Here, we seek to test our hypothesis by leveraging novel mutant strains to provide important new information on biotrophic interfacial regulation, dynamics, and function. By focusing on fungal processes required for maintaining biotrophic interfacial integrity, and by examining some important aspects of the function of the biotrophic interface, the stated objectives will use forward and reverse genetics, multiomic approaches, and live-cell imaging to understand how fungal metabolic processes dominate the plant-fungal interaction in living host cells. This could lead to the development of novel crop protection strategies targeting molecular pathways that are critical for the biotrophic growth of the fungus but are not required for the normal function of the host cell, and could shed new light on both the basic principles of cell growth, and on the nature and regulation of host-microbe interfaces. The educational objective will inspire undergraduates to excel in research, will allow graduate students to develop as mentors and teachers, and will provide all students with the tools to excel in STEM careers.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.