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Abstract
Magnaporthe oryzae, the fungus causing rice blast disease, should contend with host innate immunity to develop invasive hyphae (IH) within living host cells. However, molecular strategies to establish the biotrophic interactions are largely unknown. Here, we report the biological function of a M. oryzae-specific gene, R equired-for-Focal- B IC- F ormation 1 (RBF1). RBF1 expression was induced in appressoria and IH only when the fungus was inoculated to living plant tissues. Long-term successive imaging of live cell fluorescence revealed that the expression of RBF1 was upregulated each time the fungus crossed a host cell wall. Like other symplastic effector proteins of the rice blast fungus, Rbf1 accumulated in the biotrophic interfacial complex (BIC) and was translocated into the rice cytoplasm. RBF1-knockout mutants (Δrbf1) were severely deficient in their virulence to rice leaves, but were capable of proliferating in abscisic acid-treated or salicylic acid-deficient rice plants. In rice leaves, Δrbf1 inoculation caused necrosis and induced defense-related gene expression, which led to a higher level of diterpenoid phytoalexin accumulation than the wild-type fungus did. Δrbf1 showed unusual differentiation of IH and dispersal of the normally BIC-focused effectors around the short primary hypha and the first bulbous cell. In the Δrbf1-invaded cells, symplastic effectors were still translocated into rice cells but with a lower efficiency. These data indicate that RBF1 is a virulence gene essential for the focal BIC formation, which is critical for the rice blast fungus to suppress host immune responses.
Highlights
Biotrophic fungi colonize inside living host tissues
We focused on Required-for-Focal-biotrophic interfacial complex (BIC)-Formation 1 (RBF1) because it is one of the top five genes with regard to the expression levels after invasion [17] and its knockout mutant exhibited a drastic decrease in pathogenicity
A genomic DNA hybridization analysis using probe fragments derived from RBF1 indicated that RBF1 exists in M. oryzae rice isolates and other M. oryzae strains isolated from barley, oat, proso millet, finger millet, and Italian ryegrass (S2 Fig)
Summary
Biotrophic fungi colonize inside living host tissues. To facilitate the biotrophic invasion, fungal pathogens secrete proteins called effectors and modulate host physiology, including the suppression of immune responses [1,2,3].Magnaporthe oryzae (synonym of Pyricularia oryzae [4]) is the fungus causing blast disease in several graminaceous crops and is highly damaging to rice worldwide [5,6,7]. Biotrophic fungi colonize inside living host tissues. M. oryzae is a hemibiotroph; it colonizes living host cells during the early infection stages, which is followed by the necrotrophic stage during which conidia are produced [7]. The penetration peg emerges from the appressorium to pierce the host cell wall and subsequently differentiates into invasive hyphae (IH). Primary IH are thin tubular structures and differentiate into bulbous pseudohyphae, which branch inside the infected cells [8]. At this stage, the invaded cells of the susceptible host remain alive (compatible interaction), while in the resistant host, the invaded cells show hypersensitive response-induced cell death (incompatible interaction) [8,9]
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