Uncovering Principles of Metabolic Regulation Orchestrating Rice Infection by the Blast Fungus Magnaporthe oryzae

Rice blast disease caused by the notorious fungus Magnaporthe oryzae threatens global food security. To achieve infection, it accesses rice plants by forming appressorial cells that disrupt the leaf cuticle using internal turgor acting on a thin penetration peg. Once inside, the fungus elaborates bulbous invasive hyphae (IH) and grows for the first few days of infection as a symptomless biotroph, acquiring nutrients and evading rice innate immune responses as it spreads cell-to- cell. How this occurs at the molecular level is largely unknown. We thus seek to understand the molecular mechanisms connecting fungal metabolism and growth in rice cells with host defense suppression. Such knowledge contributes to the development of robust strategies aimed at providing sustainable crop protection from blast and other debilitating plant diseases. This work focused on the conserved Target of Rapamycin (TOR) nutrient-sensing pathway that plays status-dependent roles in appressorium formation and biotrophic growth. Inactive TOR signaling is required for appressorium formation on the host surface, whereas active TOR signaling is required for biotrophic growth in rice cells. Activating TOR on the surface or inactivating TOR in the host cell abolishes infection. During the course of our investigations into TOR function, we uncovered a novel cell glucose-ABL1-TOR signaling axis, required to fine-tune the cell cycle, and have shown how it interacts with the cAMP/PKA signaling pathway in G2 phase to promote appressorium formation. After penetration, M. oryzae IH are surrounded by the plant membrane derived extra invasive hyphae membrane (EIHM), and form the plant membrane-rich biotrophic interface complex (BIC), for apoplastic and cytoplasmic effector deployment and secretion, respectively. We characterized a novel TOR signaling component, Imp1 (Integral membrane protein 1), discovered in a forward genetic screen, and determined that it mediates TOR-dependent autophagy in order to maintain the integrity of the EIHM and BIC for effector secretion. Therefore, for the first time in any system, we described a TOR-Imp1-autophagy signal regulating effector secretion by M.oryzae during biotrophic growth. Together, our results shed light on basic principles of M. oryzae development during disease progression and improve our understanding of the plant-fungal metabolic interface