Keeping the channels open: When the rice blast fungus enters a rice cell, the plasma membrane stays intact, so the rice cell remains viable. The fungus then moves to adjacent cells via plasmodesmata, the plant's intercellular channels. Sakulkoo et al. used a chemical genetic approach to selectively inhibit a single MAP (mitogen-activated protein) kinase, Pmk1, in the blast fungus. Inhibition of Pmk1 trapped the fungus within a rice cell. Pmk1 regulated the expression of a suite of effector genes involved in suppression of host immunity, allowing the fungus to manipulate plasmodesmal conductance. At the same time, Pmk1 regulated the fungus's hyphal constriction, which allows movement into new host cells. Science , this issue p. 1399

Plants producing antisense or double-stranded RNA molecules that target specific genes of eukaryotic pests or pathogens can become protected from their attack. This beneficial effect was also reported for plant–fungus interactions and is believed to reflect uptake of the RNAs by the fungus via an as yet unknown mechanism, followed by target gene silencing. Here we report that wheat plants pre-infected with Barley stripe mosaic virus (BSMV) strains containing antisense sequences against target genes of the Fusarium head blight (FHB) fungus F. culmorum caused a reduction of corresponding transcript levels in the pathogen and reduced disease symptoms. Stable transgenic wheat plants carrying an RNAi hairpin construct against the β-1, 3-glucan synthase gene FcGls1 of F. culmorum or a triple combination of FcGls1 with two additional, pre-tested target genes also showed enhanced FHB resistance in leaf and spike inoculation assays under greenhouse and near-field conditions, respectively. Microscopic evaluation of F. culmorum development in plants transiently or stably expressing FcGls1 silencing constructs revealed aberrant, swollen fungal hyphae, indicating severe hyphal cell wall defects. The results lead us to propose host-induced gene silencing (HIGS) as a plant protection approach that may also be applicable to highly FHB-susceptible wheat genotypes.

Newly emerged wheat blast disease is a serious threat to global wheat production. Wheat blast is caused by a distinct, exceptionally diverse lineage of the fungus causing rice blast disease. Through sequencing a recent field isolate, we report a reference genome that includes seven core chromosomes and mini-chromosome sequences that harbor effector genes normally found on ends of core chromosomes in other strains. No mini-chromosomes were observed in an early field strain, and at least two from another isolate each contain different effector genes and core chromosome end sequences. The mini-chromosome is enriched in transposons occurring most frequently at core chromosome ends. Additionally, transposons in mini-chromosomes lack the characteristic signature for inactivation by repeat-induced point (RIP) mutation genome defenses. Our results, collectively, indicate that dispensable mini-chromosomes and core chromosomes undergo divergent evolutionary trajectories, and mini-chromosomes and core chromosome ends are coupled as a mobile, fast-evolving effector compartment in the wheat pathogen genome. The emerging blast disease on wheat is proving even harder to control than the ancient, still-problematic rice blast disease. Potential wheat resistance identified using strains isolated soon after disease emergence are no longer effective in controlling recent aggressive field isolates from wheat in South America and South Asia. We construct a high-quality assembly of an aggressive, recently-isolated wheat blast fungal strain and the first assembled mini-chromosome genome sequence of wheat and rice blast pathogens. We report that recent wheat pathogens can contain one or two highly-variable dispensable mini-chromosomes, each with an amalgamation of fungal effector genes and other sequences that are duplicated or absent from indispensable core chromosome ends. Well-studied effectors found on different core chromosomes in rice pathogens appear side-by-side in wheat pathogen mini-chromosomes. The rice pathogen often overcomes deployed resistance genes by deleting triggering effector genes. We propose that the fast-evolving effector-rich compartment of the wheat blast fungus is a combination of core chromosome ends and mobile mini-chromosomes that are easily lost from individual strains. Localization of effectors on mini-chromosomes would therefore accelerate pathogen adaptation in the field.

β-1,3-Glucan and chitin are the most prominent polysaccharides of the fungal cell wall. Covalently linked, these polymers form a scaffold that determines the form and properties of vegetative and pathogenic hyphae. While the role of chitin in plant infection is well understood, the role of β-1,3-glucan is unknown. We functionally characterized the β-1,3-glucan synthase gene GLS1 of the maize (Zea mays) pathogen Colletotrichum graminicola, employing RNA interference (RNAi), GLS1 overexpression, live-cell imaging, and aniline blue fluorochrome staining. This hemibiotroph sequentially differentiates a melanized appressorium on the cuticle and biotrophic and necrotrophic hyphae in its host. Massive β-1,3-glucan contents were detected in cell walls of appressoria and necrotrophic hyphae. Unexpectedly, GLS1 expression and β-1,3-glucan contents were drastically reduced during biotrophic development. In appressoria of RNAi strains, downregulation of β-1,3-glucan synthesis increased cell wall elasticity, and the appressoria exploded. While the shape of biotrophic hyphae was unaffected in RNAi strains, necrotrophic hyphae showed severe distortions. Constitutive expression of GLS1 led to exposure of β-1,3-glucan on biotrophic hyphae, massive induction of broad-spectrum defense responses, and significantly reduced disease symptom severity. Thus, while β-1,3-glucan synthesis is required for cell wall rigidity in appressoria and fast-growing necrotrophic hyphae, its rigorous downregulation during biotrophic development represents a strategy for evading β-glucan–triggered immunity.

Summary: Rice blast, the most destructive disease of cultivated rice world‐wide, is caused by the filamentous fungus Magnaporthe oryzae. To cause disease in plants, M. oryzae secretes a diverse range of effector proteins to suppress plant defense responses, modulate cellular processes, and support pathogen growth. Some effectors can be secreted by appressoria even before host penetration, while others accumulate in the apoplast, or enter living plant cells where they target specific plant subcellular compartments. During plant infection, the blast fungus induces the formation of a specialized plant structure known as the biotrophic interfacial complex (BIC), which appears to be crucial for effector delivery into plant cells. Here, we review recent advances in the cell biology of M. oryzae–host interactions and show how new breakthroughs in disease control have stemmed from an increased understanding of effector proteins of M. oryzae are deployed and delivered into plant cells to enable pathogen invasion and host susceptibility.