To cause rice blast disease, the fungus Magnaporthe oryzae breaches the tough outer cuticle of the rice leaf by using specialized
infection structures called appressoria. These cells allow the fungus to invade the host plant and proliferate rapidly within leaf tissue. Here, we show that a unique
NADPH-dependent genetic switch regulates plant
infection in response to the changing nutritional and redox conditions encountered by the pathogen. The biosynthetic
enzyme trehalose-6-phosphate synthase (Tps1) integrates control of
glucose-6-phosphate metabolism and
nitrogen source utilization by regulating the oxidative pentose phosphate pathway, the generation of
NADPH, and the activity of
nitrate reductase. We report that Tps1 directly binds to
NADPH and, thereby, regulates a set of related transcriptional
corepressors, comprising three
proteins, Nmr1, Nmr2, and Nmr3, which can each bind
NADP. Targeted deletion of any of the Nmr-encoding genes partially suppresses the nonpathogenic phenotype of a Δtps1 mutant. Tps1-dependent Nmr
corepressors control the expression of a set of virulence-associated genes that are derepressed during appressorium-mediated plant
infection. When considered together, these results suggest that initiation of rice blast disease by M. oryzae requires a regulatory mechanism involving an
NADPH sensor
protein, Tps1, a set of
NADP-dependent transcriptional
corepressors, and the nonconsuming interconversion of
NADPH and
NADP acting as signal transducer.