A protein kinase coordinates cycles of autophagy and glutaminolysis in invasive hyphae of the fungus Magnaporthe oryzae within rice cells

Authors

Gang Li, University of Nebraska - LincolnFollow
Ziwen Gong, University of Nebraska - Lincoln
Nawaraj Dulal, University of Nebraska - LincolnFollow
Margarita Marroquin-Guzman, University of Nebraska - Lincoln
Raquel O. Rocha, University of Nebraska - Lincoln
Michael Richter, University of Nebraska - Lincoln
Richard Wilson, University of Nebraska-LincolnFollow

Date of this Version

7-12-2023

Abstract

The blast fungus Magnaporthe oryzae produces invasive hyphae in living rice cells during early infection, separated from the host cytoplasm by plantderived interfacial membranes. However, the mechanisms underpinning this intracellular biotrophic growth phase are poorly understood. Here, we show that the M. oryzae serine/threonine protein kinase Rim15 promotes biotrophic growth by coordinating cycles of autophagy and glutaminolysis in invasive hyphae. Alongside inducing autophagy, Rim15 phosphorylates NADdependent glutamate dehydrogenase, resulting in increased levels of α- ketoglutarate that reactivate target-of-rapamycin (TOR) kinase signaling, which inhibits autophagy. Deleting RIM15 attenuates invasive hyphal growth and triggers plant immunity; exogenous addition of α-ketoglutarate prevents these effects, while glucose addition only suppresses host defenses. Our results indicate that Rim15-dependent cycles of autophagic flux liberate α-ketoglutarate – via glutaminolysis – to reactivate TOR signaling and fuel biotrophic growth while conserving glucose for antioxidation-mediated host innate immunity suppression.