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The Magnaporthe oryzae nitrooxidative stress response suppresses rice innate immunity during blast disease


Understanding how microorganisms manipulate plant innate immunity and colonize host cells is a major goal of plant pathology. Here, we report that the fungal nitrooxidative stress response suppresses host defences to facilitate the growth and development of the important rice pathogen Magnaporthe oryzae in leaf cells. Nitronate monooxygenases encoded by NMO genes catalyse the oxidative denitrification of nitroalkanes. We show that the M. oryzae NMO2 gene is required for mitigating damaging lipid nitration under nitrooxidative stress conditions and, consequently, for using nitrate and nitrite as nitrogen sources. On plants, the Δnmo2 mutant strain penetrated host cuticles like wild type, but invasive hyphal growth in rice cells was restricted and elicited plant immune responses that included the formation of cellular deposits and a host reactive oxygen species burst. Development of the M. oryzae effector-secreting biotrophic interfacial complex (BIC) was misregulated in the Δnmo2 mutant. Inhibiting or quenching host reactive oxygen species suppressed rice innate immune responses and allowed the Δnmo2 mutant to grow and develop normally in infected cells. NMO2 is thus essential for mitigating nitrooxidative cellular damage and, in rice cells, maintaining redox balance to avoid triggering plant defences that impact M. oryzae growth and BIC development.

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Figure 1: NMO2, encoding a nitronate monooxygenase, is required for nitrate utilization.
Figure 2: NMO2 is required for growth on media containing nitrate or nitrite as the sole nitrogen source.
Figure 3: NMO2 is required for tolerating nitrooxidative stress.
Figure 4: NMO2 is essential for neutralizing the host ROS burst and suppressing plant innate immune responses.
Figure 5: The Pwl2 effector is mislocalized in Δnmo2 mutant strains during early rice infection.
Figure 6: Δnmo2 mutant strains develop multiple BIC foci by late rice infection.


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The authors thank B. Valent (Kansas State University) for the gift of pBV591. This work was supported by grants from the National Science Foundation (IOS-1557943) and the USDA-NIFA (2014-67013-21559) to R.A.W. A UNL ARD bridging fund award supported M.M.-G.

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R.A.W. conceived the project, designed the experiments and interpreted the data. M.M.-G., D.H., J.D.W., C.E., T.J.B. and R.A.W. performed experiments and analysed the data. R.A.W. wrote the manuscript.

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Correspondence to Richard A. Wilson.

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Marroquin-Guzman, M., Hartline, D., Wright, J. et al. The Magnaporthe oryzae nitrooxidative stress response suppresses rice innate immunity during blast disease. Nat Microbiol 2, 17054 (2017).

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