Molecular and cellular analysis of the biotrophic interaction between rice and Magnaporthe oryzae – Exploring situations in which the blast fungus controls the infection

Mochizuki, Susumu; Yokotani, Naoki; Nishimura, Takeshi; Minami, Eiichi

doi:10.1016/j.pmpp.2016.02.001

Cited by 14 publications

(14 citation statements)

References 48 publications

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“…Instead, preferential accumulation in the BIC, which is a prominent feature of the blast fungus-rice cell interface, is the major predictor of translocation into the rice cell. Previously, the Nishizawa lab reported that a cytoplasmic effector is packaged in vesicles in the outer region of the BIC (Mochizuki et al, 2015;Nishimura et al, 2016;Nishizawa et al, 2016). Here, we have used live-cell fluorescence imaging to characterize the nature and dynamics of membrane-bound effector vesicles within BICs and in surrounding host cytoplasm.…”

Section: Introductionmentioning

confidence: 99%

Clathrin-mediated Endocytosis Facilitates Internalization ofMagnaporthe oryzaeEffectors into Rice Cells

Oliveira-Garcia

Tamang

Park

et al. 2021

Preprint

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Many filamentous eukaryotic plant pathogens, such as fungi and oomycetes, deliver effectors into living plant cells to suppress defenses and control plant processes needed for infection. To date, little is known about the mechanism by which these pathogens translocate effector proteins across the plasma membrane into the plant cytoplasm. The blast fungus Magnaporthe oryzae secretes cytoplasmic effectors into a specialized biotrophic interfacial complex (BIC) before translocation. Here we show that cytoplasmic effectors within BICs are packaged into dynamic vesicles that can occasionally be found separated from BICs in the host cytoplasm. Live cell imaging with fluorescently-labelled rice lines, showed that BICs are enriched in plant plasma membrane, actin, and Clathrin Light Chain-1, a marker for clathrin-mediated endocytosis (CME). We report that a novel cytoplasmic effector, Bas83, labels empty membrane vesicles surrounding BICs. Inhibition of CME using VIGS and chemical treatments results in a distinctive swollen BIC phenotype lacking effector vesicles. In contrast, fluorescent marker co-localization, VIGS and chemical inhibitor studies failed to implicate clathrin-independent endocytosis in effector vesicle formation. Taken together, this study provides evidence that cytoplasmic effector translocation is mediated by clathrin-mediated endocytosis in BICs and suggests a role for M. oryzae effectors in co-opting plant endocytosis.

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Section: Introductionmentioning

confidence: 99%

Clathrin-mediated Endocytosis Facilitates Internalization ofMagnaporthe oryzaeEffectors into Rice Cells

Oliveira-Garcia

Tamang

Park

et al. 2021

Preprint

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“…Recently, high-resolution imaging analysis of BICs demonstrated that not only host membranes but also cytosolic components are enriched in the BIC, and symplastic effectors accumulate in the BIC in a punctate form [ 13 ]. When the EIHM was labeled with the green fluorescent protein (GFP), each punctum appeared to be encircled by GFP signals, implying that the BIC is a compex of membrane vesicles that contain symplastic effectors [ 16 ]. These results strongly suggest that the BIC is the active site of translocation for symplastic effectors in the host cell.…”

Section: Introductionmentioning

confidence: 99%

Magnaporthe oryzae Glycine-Rich Secretion Protein, Rbf1 Critically Participates in Pathogenicity through the Focal Formation of the Biotrophic Interfacial Complex

et al. 2016

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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.

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“…After gaining entry into host cells, M. oryzae invades in a hemibiotrophic lifestyle. Invasive hyphae are enclosed by the host extra-invasive-hyphal membrane within 36 hours of biotrophic growth and extend into the neighbouring cells via the plasmodesmata to cause the necrosis of host tissues (Couch et al 2005; Kankanala et al 2007; Nishizawa et al 2016). Although the genetic determinants facilitating this hemi-biotrophic transition are mostly unknown, there are suggestions that effector proteins secreted by M. oryzae play a prominent role in suppressing host immunity during this transition (Zhang et al 2014b).…”

Section: Introductionmentioning

confidence: 99%

Regulatory network of genes associated with stimuli sensing, signal transduction and physiological transformation of appressorium inMagnaporthe oryzae

et al. 2018

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Rice blast caused by Magnaporthe oryzae is the most destructive disease affecting the rice production (Oryza sativa), with an average global loss of 10–30% per annum. Recent reports have indicated that the fungus also inflicts blast disease on wheat (Triticum aestivum) posing a serious threat to the wheat production. Due to its easily detected infectious process and manoeuvrable genetic manipulation, M. oryzae is considered a model organism for exploring the molecular mechanism underlying fungal pathogenicity during the pathogen–host interaction. M. oryzae utilises an infectious structure called appressorium to breach the host surface by generating high turgor pressure. The appressorium development is induced by physical and chemical cues which are coordinated by the highly conserved cAMP/PKA, MAPK and calcium signalling cascades. Genes involved in the appressorium development have been identified and well studied in M. oryzae, a summary of the working gene network linking stimuli sensing and physiological transformation of appressorium is needed. This review provides a comprehensive discussion regarding the regulatory networks underlying appressorium development with particular emphasis on sensing of appressorium inducing stimuli, signal transduction, transcriptional regulation and the corresponding developmental and physiological responses. We also discussed the crosstalk and interaction of various pathways during the appressorium development.

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Molecular and cellular analysis of the biotrophic interaction between rice and Magnaporthe oryzae – Exploring situations in which the blast fungus controls the infection

Cited by 14 publications

References 48 publications

Clathrin-mediated Endocytosis Facilitates Internalization ofMagnaporthe oryzaeEffectors into Rice Cells

Clathrin-mediated Endocytosis Facilitates Internalization ofMagnaporthe oryzaeEffectors into Rice Cells

Magnaporthe oryzae Glycine-Rich Secretion Protein, Rbf1 Critically Participates in Pathogenicity through the Focal Formation of the Biotrophic Interfacial Complex

Regulatory network of genes associated with stimuli sensing, signal transduction and physiological transformation of appressorium inMagnaporthe oryzae

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