Abstract
The blast fungus Magnaporthe oryzae threatens global food security through the widespread destruction of cultivated rice. Foliar infection requires a specialized cell called an appressorium that generates turgor to force a thin penetration hypha through the rice cuticle and into the underlying epidermal cells, where the fungus grows for the first days of infection as a symptomless biotroph. Understanding what controls biotrophic growth could open new avenues for developing sustainable blast intervention programs. Here, using molecular genetics and live-cell imaging, we dismantled M. oryzae glucose-metabolizing pathways to reveal that the transketolase enzyme, encoded by TKL1, plays an essential role in facilitating host colonization during rice blast disease. In the absence of transketolase, Δtkl1 mutant strains formed functional appressoria that penetrated rice cuticles successfully and developed invasive hyphae (IH) in rice cells from primary hyphae. However, Δtkl1 could not undertake sustained biotrophic growth or cell-to-cell movement. Transcript data and observations using fluorescently labeled histone H1:RFP fusion proteins indicated Δtkl1 mutant strains were alive in host cells but were delayed in mitosis. Mitotic delay could be reversed and IH growth restored by the addition of exogenous ATP, a metabolite depleted in Δtkl1 mutant strains. We show that ATP might act via the TOR signaling pathway, and TOR is likely a downstream target of activation for TKL1. TKL1 is also involved in controlling the migration of appressorial nuclei into primary hyphae in host cells. When taken together, our results indicate transketolase has a novel role in mediating - via ATP and TOR signaling - an in planta-specific metabolic checkpoint that controls nuclear migration from appressoria into primary hyphae, prevents mitotic delay in early IH and promotes biotrophic growth. This work thus provides new information about the metabolic strategies employed by M. oryzae to enable rice cell colonization.
Highlights
The rice blast fungus Magnaporthe oryzae causes the most serious disease of cultivated rice [1], [2] and is a significant challenge to global food security [3], [4]
Following penetration into the rice cell, M. oryzae elaborates bulbous invasive hyphae that grow in living rice cells for most of the infection cycle without causing disease symptoms
Loss of transketolase did not affect the ability of the fungus to gain entry into rice cells, but invasive hyphal growth was curtailed in transketolase null mutants
Summary
The rice blast fungus Magnaporthe oryzae causes the most serious disease of cultivated rice [1], [2] and is a significant challenge to global food security [3], [4]. Enormous turgor is generated in the appressorium through the accumulation of glycerol and the ingress of water that becomes trapped due to a layer of melanin deposited on the wall of the appressorium [10], [11]. This hydrostatic pressure acts on a penetration peg [5], [6], forcing it through the leaf cuticle. After four to five days of biotrophic growth in susceptible cultivars, host cells die and M. oryzae enters its necrotrophic growth phase, causing spreading necrotic lesions on the leaf surface from which conidia are produced on aerial hyphae [1]
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