Septin-Mediated Plant Cell Invasion by the Rice Blast Fungus,
            <i>Magnaporthe oryzae</i>

Dagdas, Yasin; Yoshino, Kae; Dagdas, Gulay; Ryder, Lauren S.; Bielska, Ewa; Steinberg, Gero; Talbot, Nicholas J.

doi:10.1126/science.1222934

Cited by 339 publications

(499 citation statements)

References 39 publications

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“…Display rate, 1 frame /12 s. Related to Figure 5C. ; b (Berepiki et al 2011); c (Dagdas et al 2012); d (Chen and Thorner 2007); e (Semighini and Harris 2008); f (Jones and Bennett 2011); g ; h (Artiles et al 2009); i (Das et al 2013); j (Rank and Rayment 2013); k (Krappmann et al 2007); l (Pulver et al 2013); m (Park et al 1997); n (Brace et al 2011); o (Knaus et al 2007); p (Berepiki and Read 2013) (Glass and Lee 1992); g (Ferreira et al 1998); h (Hammond et al 2012); i (Li et al 2005); j (Park et al 2011) …”

Section: Figure S2mentioning

confidence: 99%

New Insights Into the Roles of NADPH Oxidases in Sexual Development and Ascospore Germination in Sordaria macrospora

et al. 2014

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NADPH oxidase (NOX)-derived reactive oxygen species (ROS) act as signaling determinants that induce different cellular processes. To characterize NOX function during fungal development, we utilized the genetically tractable ascomycete Sordaria macrospora. Genome sequencing of a sterile mutant led us to identify the NADPH oxidase encoding nox1 as a gene required for fruiting body formation, regular hyphal growth, and hyphal fusion. These phenotypes are shared by Δnor1, lacking the NOX regulator NOR1. Further phenotypic analyses revealed a high correlation between increased ROS production and hyphal fusion deficiencies in Δnox1 and other sterile mutants. A genome-wide transcriptional profiling analysis of mycelia and isolated protoperithecia from wild type and Δnox1 revealed that nox1 inactivation affects the expression of genes related to cytoskeleton remodeling, hyphal fusion, metabolism, and mitochondrial respiration. Genetic analysis of Δnox2, lacking the NADPH oxidase 2 gene, Δnor1, and transcription factor deletion mutant Δste12, revealed a strict melanin-dependent ascospore germination defect, indicating a common genetic pathway for these three genes. We report that gsa3, encoding a G-protein a-subunit, and sac1, encoding cAMP-generating adenylate cyclase, act in a separate pathway during the germination process. The finding that cAMP inhibits ascospore germination in a melanin-dependent manner supports a model in which cAMP inhibits NOX2 activity, thus suggesting a link between both pathways. Our results expand the current knowledge on the role of NOX enzymes in fungal development and provide a frame to define upstream and downstream components of the NOX signaling pathways in fungi. D URING sexual reproduction, filamentous fungi generate complex fruiting bodies that contain and protect meiosporangia. We used the ascomycetous model fungus Sordaria macrospora to identify genes directly involved in fruiting body development (Kück et al. 2009;Engh et al. 2010;Kück et al. 2009). Due to its homothallic life style, S. macrospora is able to complete the sexual life cycle without the mating of strains with opposite sex, and therefore, fruiting body-deficient mutants can be recognized directly without the need for crossing experiments. In earlier work, we generated sterile mutants showing a developmental block after formation of young fruiting bodies (protoperithecia), but being unable to generate mature perithecia, and referred to these mutants as pro. Recently, we have applied next-generation genome re-sequencing to identify the genes affected in some of these mutants . Based on this approach, we now have characterized mutant pro32 and show that it carries a mutation in the nox1 gene encoding NAPDH oxidase 1 (NOX1).NADPH oxidase (NOX) enzymes are transmembrane proteins that are highly conserved among eukaryotes and produce reactive oxygen species (ROS) through the oxidation of NADPH (Lambeth 2004;Kawahara and Lambeth 2007). ROS have long been recognized as damaging agents due to uncontrolled oxidizing re...

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Section: Figure S2mentioning

confidence: 99%

New Insights Into the Roles of NADPH Oxidases in Sexual Development and Ascospore Germination in Sordaria macrospora

et al. 2014

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“…M. oryzae infects hosts by first forming specialized infection structures, appressoria, at the tips of germ tubes emerging from spores adhered to the leaf surface. 4,5 A thin penetration peg emerging from an unmelanized patch on the base of the appressorium 6 is forced through the rice leaf cuticle under hydrostatic turgor pressure 1 . In the first penetrated cell, the peg differentiates into primary hyphae then bulbous invasive hyphae (IH) that are surrounded by the plant-derived extra-invasive hyphal membrane (EIHM).…”

Section: Authorsmentioning

confidence: 99%

“…5 Primers used to quantify the expression of rice callose synthase-encoding genes (Hao et al, 2008). 6 Primers used for screening of hygromycin resistance strains carrying the plasmid pBV591, expressing Pwl2:mCherry:NLS and Bas4: GFP ). …”

Section: Supplementary Informationmentioning

confidence: 99%

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

et al. 2017

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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 defenses to facilitate the growth and development of the important rice pathogen Magnaporthe oryzae in leaf cells. Nitronate monooxygenases encoded by NMO genes catalyze 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 defenses that impact M. oryzae growth and BIC development.Global rice yields are significantly and negatively impacted each year by blast disease caused by the hemibiotrophic fungus Magnaporthe oryzae 1-3 (synonym of Pyricularia oryzae). Defining the full spectrum of molecular pro- Marroquin-Guzman et al. in Nature Microbiology 2 (2017) 2 cesses used by M. oryzae to manipulate rice innate immunity and allow fungal colonization of host cells might reveal additional sources of pathogen resistance and improve crop health. M. oryzae infects hosts by first forming specialized infection structures, appressoria, at the tips of germ tubes emerging from spores adhered to the leaf surface. 4,5 A thin penetration peg emerging from an unmelanized patch on the base of the appressorium 6 is forced through the rice leaf cuticle under hydrostatic turgor pressure 1 . In the first penetrated cell, the peg differentiates into primary hyphae then bulbous invasive hyphae (IH) that are surrounded by the plant-derived extra-invasive hyphal membrane (EIHM). Branching IH fill the first invaded cell before spreading into neighboring living rice cells at around 44 h post-inoculation. 7,8 This biotrophic growth phase progresses for 4-5 days before M. oryzae enters its necrotrophic phase.To colonize rice cells, M. oryzae must first suppress or avoid triggering two types of plant innate immunity that protect against microbial attack [9][10][11] : pathogen-associated molecular pattern (PAMP) triggered immunity (PTI), which can be suppressed by microbial effectors, and effector-triggered immunity (ETI), if effectors are detected. The biotrophic interfacial complex (BIC), a host membrane-derived structure, is formed behind M. oryzae IH in each in...

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“…Septin function is required for cell division and viability in many eukaryotes whereas misregulation is associated with cancers and neurodegenerative disorders (5)(6)(7)(8). Furthermore, septins mediate entry of both bacterial and fungal pathogens into host cells (9)(10)(11). In vivo, septin assembly is restricted both in time and in space through local activation of small GTPases such as Cdc42.…”

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Septin assemblies form by diffusion-driven annealing on membranes

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Mehta

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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Septins assemble into filaments and higher-order structures that act as scaffolds for diverse cell functions including cytokinesis, cell polarity, and membrane remodeling. Despite their conserved role in cell organization, little is known about how septin filaments elongate and are knitted together into higher-order assemblies. Using fluorescence correlation spectroscopy, we determined that cytosolic septins are in small complexes, suggesting that septin filaments are not formed in the cytosol. When the plasma membrane of live cells is monitored by total internal reflection fluorescence microscopy, we see that septin complexes of variable size diffuse in two dimensions. Diffusing septin complexes collide and make end-on associations to form elongated filaments and higher-order structures, an assembly process we call annealing. Septin assembly by annealing can be reconstituted in vitro on supported lipid bilayers with purified septin complexes. Using the reconstitution assay, we show that septin filaments are highly flexible, grow only from free filament ends, and do not exchange subunits in the middle of filaments. This work shows that annealing is a previously unidentified intrinsic property of septins in the presence of membranes and demonstrates that cells exploit this mechanism to build large septin assemblies.cytoskeleton | biophysics S eptin filaments form rings, bars, and gauzes that serve as a scaffold at cell division sites; act to retract blebbed regions of membrane; and restrict diffusion between cell compartments (1-4). Septin function is required for cell division and viability in many eukaryotes whereas misregulation is associated with cancers and neurodegenerative disorders (5-8). Furthermore, septins mediate entry of both bacterial and fungal pathogens into host cells (9-11). In vivo, septin assembly is restricted both in time and in space through local activation of small GTPases such as Cdc42. Localized signaling leads to higher-order septin structures forming closely apposed to the plasma membrane at the plane of division, sites of polarity, and curved membranes (10,(12)(13)(14). Notably, eukaryotic cells of different geometries build higher-order septin assemblies of various shapes, sizes, and functions (4, 15, 16). Although septins are critical for spatial organization of cell plasma membranes, their assembly and disassembly dynamics are not understood (15).Electron microscopy (EM) studies of recombinant and immunoprecipitated Saccharomyces cerevisiae septins have shown that septins form nonpolar hetero-octameric rod-shaped complexes in high-salt buffers (>300 mM) and elongated filaments when dialyzed into low-salt buffers (<100 mM) (17, 18). Structural analyses of worm and mammalian septins have revealed that the heteromeric, rod-shaped complex is conserved (19-21). Thus, septin rods characterized to date contain two copies of each septin subunit assembled into a nonpolar, heteromeric complex (Fig. S1). Association of purified septin proteins with phosphoinositide-containing membrane monola...

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Septin-Mediated Plant Cell Invasion by the Rice Blast Fungus, Magnaporthe oryzae

Cited by 339 publications

References 39 publications

New Insights Into the Roles of NADPH Oxidases in Sexual Development and Ascospore Germination in Sordaria macrospora

New Insights Into the Roles of NADPH Oxidases in Sexual Development and Ascospore Germination in Sordaria macrospora

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

Septin assemblies form by diffusion-driven annealing on membranes

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