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From Surface Sensing to Biotrophic Growth: Unraveling the Metabolic Strategies of the Rice Blast Fungus Magnaporthe Oryzae during Infection
Magnaporthe oryzae is a global food security threat that causes blast, the most devastating disease of cultivated rice and an emerging threat to wheat. Here, we identify new components of central importance to the development of rice blast infection. At the start of foliar infection, the fungus breaches the plant cuticle by using a specialized infection structure called an appressorium. As the appressorium matures, deposition of melanin and chitin plays a role in strengthening the appressoria cell wall to prevent the leakage of solutes. Together, the impermeable layer and the accumulation of solutes generate an internal turgor pressure that drives the emergence of a penetration peg from the pore located at the base of the melanized appressorium and penetrates the plant cuticle. Equally important, but still poorly understood, mucilage production by the appressorium is another element that enables fungal penetration. By using gene functional analysis, we demonstrate for the first time in a fungal system, that spermine synthesis is fundamental to appressorial adhesion via mucilage production, and thus, to fungal penetration of the plant cell wall. Deletion of the Magnaporthe spermine synthase-encoding gene SPS1 abolished infection and generated a Δsps1 mutant strain impaired in turgor accumulation, exhibiting misshapen appressoria with thinner cell walls. Once inside the host cell, M. oryzae programs its metabolic machinery to utilize glucose through the pentose phosphate pathway (PPP) in order to fuel the NADPH production, needed for redox balance. As part of regulatory processes maintaining carbon flux distribution, the nucleoside diphosphate kinase, Ndk1 is a key checkpoint for the correct generation of signaling molecules. Perturbing the system by deleting NDK1 caused a flux redistribution of the fungal central metabolism, favoring salvage reactions in the purine metabolism and, consequently, the generation of ROS. Changes to the fungal redox status and reallocation of metabolic resources led to impaired fungal growth, disturbances of the biotrophic interfacial complex, and ultimately recognition by the rice immune system. Overall, the research presented here expands our understanding of the molecular and biochemical mechanisms underpinning host access and colonization by the rice blast fungus and might yield novel management strategies of the blast disease.
de Olivera Rocha, Raquel, "From Surface Sensing to Biotrophic Growth: Unraveling the Metabolic Strategies of the Rice Blast Fungus Magnaporthe Oryzae during Infection" (2019). ETD collection for University of Nebraska - Lincoln. AAI27667308.