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

Gang Li, Ziwen Gong, Nawaraj Dulal, Margarita Marroquin-Guzman, Raquel O. Rocha, Michael Richter and Richard A. Wilson ()
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Gang Li: University of Nebraska-Lincoln
Ziwen Gong: University of Nebraska-Lincoln
Nawaraj Dulal: University of Nebraska-Lincoln
Margarita Marroquin-Guzman: University of Nebraska-Lincoln
Raquel O. Rocha: University of Nebraska-Lincoln
Michael Richter: University of Nebraska-Lincoln
Richard A. Wilson: University of Nebraska-Lincoln

Nature Communications, 2023, vol. 14, issue 1, 1-15

Abstract: Abstract The blast fungus Magnaporthe oryzae produces invasive hyphae in living rice cells during early infection, separated from the host cytoplasm by plant-derived 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 NAD-dependent 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.

Date: 2023
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DOI: 10.1038/s41467-023-39880-w

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