Dynamic assembly of a higher-order septin structure during appressorium morphogenesis by the rice blast fungus
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Appressorium
Septin
Magnaporthe
Fungal protein
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Appressorium
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Abstract The pathogenic life cycle of the rice blast fungus Magnaporthe oryzae involves a series of morphogenetic changes, essential for its ability to cause disease. The smo mutation was identified > 25 years ago, and affects the shape and development of diverse cell types in M. oryzae, including conidia, appressoria, and asci. All attempts to clone the SMO1 gene by map-based cloning or complementation have failed over many years. Here, we report the identification of SMO1 by a combination of bulk segregant analysis and comparative genome analysis. SMO1 encodes a GTPase-activating protein, which regulates Ras signaling during infection-related development. Targeted deletion of SMO1 results in abnormal, nonadherent conidia, impaired in their production of spore tip mucilage. Smo1 mutants also develop smaller appressoria, with a severely reduced capacity to infect rice plants. SMO1 is necessary for the organization of microtubules and for septin-dependent remodeling of the F-actin cytoskeleton at the appressorium pore. Smo1 physically interacts with components of the Ras2 signaling complex, and a range of other signaling and cytoskeletal components, including the four core septins. SMO1 is therefore necessary for the regulation of RAS activation required for conidial morphogenesis and septin-mediated plant infection.
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Evolutionarily conserved nucleosome assembly protein Nap1 is involved in multiple cellular processes in eukaryotes. In this study, we wanted to explore the role of Nap1 in the life cycle of rice blast fungus Magnaporthe oryzae. The null mutant of M. oryzae NAP1 is viable. However, deletion of NAP1 leads to defects in growth, appressorium morphology, and appressorium turgidity. In the future, plant infection studies can be undertaken to find if these defects lead to compromised virulence of this economically important fungal pathogen.
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Summary Trimeric G‐proteins transmit extracellular signals to various downstream effectors (e.g. MAP kinases) in eukaryotes. In the rice blast fungus Magnaporthe grisea , the Pmk1 MAP kinase is essential for appressorium formation and infectious growth. The pmk1 deletion mutant fails to form appressoria but still responds to exogenous cAMP for tip deformation. Since gene disruption mutants of three Gα subunits still form appressoria and are phenotypically different from pmk1 mutants, it is likely that the Pmk1 pathway is activated by Gβ in M. grisea . In this study, we isolated and characterized the MGB1 gene that encodes the G subunit in M. grisea . Mutants disrupted in MGB1 were reduced in conidiation. Conidia from mgb1 mutants were defective in appressorium formation and failed to penetrate or grow invasively on rice leaves. Exogenous cAMP induced appressorium formation in mgb1 mutants, but these appressoria were abnormal in shape and could not penetrate. The intracellular cAMP level was reduced in mgb1 mutants and the defects in conidiation and hyphal growth were partially suppressed with 1 mM cAMP. Transformants expressing multiple copies of MGB1 were able to form appressoria on hydrophilic surfaces. Our results suggest that MGB1 may be involved in the cAMP signalling for regulating conidiation, surface recognition and appressorium formation. The Pmk1 pathway may be the downstream target of MGB1 for regulating penetration and infectious hyphae growth in M. grisea .
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Like many fungal pathogens, the conidium and appressorium play key roles during polycyclic dissemination and infection of Magnaporthe oryzae. Ran-binding protein microtubule-organizing center (RanBPM) is a highly conserved nucleocytoplasmic protein. In animalia, RanBPM has been implicated in apoptosis, cell morphology, and transcription. However, the functional roles of RanBPM, encoded by MGG_00753 (named MoRBP9) in M. oryzae, have not been elucidated. Here, the deletion mutant ΔMorbp9 for MoRBP9 was generated via homologous recombination to investigate the functions of this gene. The ΔMorbp9 exhibited normal conidial germination and vegetative growth but dramatically reduced conidiation compared with the wild type, suggesting that MoRBP9 is involved in conidial production. ΔMorbp9 conidia failed to produce appressoria on hydrophobic surfaces, whereas ΔMorbp9 still developed aberrantly shaped appressorium-like structures at hyphal tips on the same surface, suggesting that MoRBP9 is involved in the morphology of appressorium-like structures from hyphal tips and is critical for development of appressorium from germ tubes. Taken together, our results indicated that MoRBP9 played a pleiotropic role in polycyclic dissemination and infection-related morphogenesis of M. oryzae.
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The hydrophobin-encoding gene MPG1 of the rice blast fungus Magnaporthe grisea is highly expressed during the initial stages of host plant infection and targeted deletion of the gene results in a mutant strain that is reduced in virulence, conidiation, and appressorium formation. The green fluorescent protein-encoding allele sGFP was used as a reporter to investigate regulatory genes that control MPG1 expression. The MAP kinase-encoding gene PMK1 and the wide domain regulators of nitrogen source utilization, NPR1 and NUT1, were required for full expression of MPG1 in response to starvation stress. The CPKA gene, encoding the catalytic subunit of protein kinase A, was required for repression of MPG1 during growth in rich nutrient conditions. During appressorium morphogenesis, high-level MPG1 expression was found to require the CPKA and NPR1 genes. Expression of a destabilized GFP allele indicated that de novo MPG1 expression occurs during appressorium formation. Three regions of the MPG1 promoter were identified which are required for high-level expression of MPG1 during appressorium formation and are necessary for the biological activity of the MPG1 hydrophobin during spore formation and plant infection.
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AbstractAutophagy is a ubiquitous and evolutionarily conserved process found in all eukaryotic cells that allows for the degradation and recycling of old proteins and organelles. Starvation can induce autophagy, and autophagic pathway is an essential process for cellular function under starvation. In Magnaporthe grisea, starvation is one of the key induced factors for the germ tube tip to differentiate into an appressorium. Considering the importance of the rice blast fungus as a primary model for host-pathogen interaction, the role of autophagy in fungal development, appressorium turgor generation and pathogenicity of M. grisea via its role in organelle and protein turnover is a very significant subject.Addendum to:Involvement of a Magnaporthe grisea Serine/Threonine Kinase, MgATG1, in Appressorium Turgor and PathogenesisX.-H. Liu, J.-P. Lu, L. Zhang, B. Dong, H. Min and F.-C. LinEukaryotic Cell 2007; In press
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To breach the plant cuticle, many plant pathogenic fungi differentiate specialized infection structures (appressoria). In Colletotrichum orbiculare (cucumber anthracnose fungus), this differentiation requires unique proper G1 /S phase progression, regulated by two-component GTPase activating protein CoBub2/CoBfa1 and GTPase CoTem1. Since their homologues regulate mitotic exit, cytokinesis, or septum formation from yeasts to mammals, we asked whether the BUB2 function in G1 /S progression is specific to plant pathogenic fungi. Colletotrichum higginsianum and Magnaporthe oryzae were genetically analyzed to investigate conservation of BUB2 roles in cell cycle regulation, septum formation, and virulence. Expression profile of cobub2Δ was analyzed using a custom microarray. In bub2 mutants of both fungi, S phase initiation was earlier, and septum formation coordinated with a septation initiation network protein and contractile actin ring was impaired. Earlier G1 /S transition in cobub2Δ results in especially high expression of DNA replication genes and differing regulation of virulence-associated genes that encode proteins such as carbohydrate-active enzymes and small secreted proteins. The virulence of chbub2Δ and mobub2Δ was significantly reduced. Our evidence shows that BUB2 regulation of G1 /S transition and septum formation supports its specific requirement for appressorium development in plant pathogenic fungi.
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To cause disease on host plants, many phytopathogenic fungi undergo morphological transitions including development of reproductive structures as well as specialized infection structures called appressoria. Such morphological transitions display distinct nuclear dynamics. Here we report the developmental requirement of MoAND1-mediated nuclear positioning for pathogenesis of the rice blast fungus, Magnaporthe oryzae. The MoAND1 gene encodes a protein that shows high similarity to Num1 in Saccharomyces cerevisiae and ApsA in Aspergillus nidulans, both of which are cell cortex proteins involved in nuclear migration and positioning. Targeted deletion of MoAND1 did not affect radial growth of the fungus but impaired nuclear distribution along the hyphae, which is reminiscent of ApsA mutant. In contrast to the wild-type, which produces three to five spores in a sympodial manner on the conidiophore, only a single spore was borne on the conidiophore of ΔMoand1, resulting in ∼65% decrease in conidia production, compared to the wild-type. The mutant conidia displayed abnormalities in septation pattern and nuclear distribution, which were correlated with their inability to germinate. Spores of the mutant that did germinate were capable of differentiating appressoria but were defective in the execution of programmed nuclear migration and positioning during development. Furthermore, mutant appressoria were not fully functional, leading to delay in penetration of host plants. However, the ability of ΔMoand1 to grow inside host tissues was comparable to that of the wild-type. All these defects greatly decreased the virulence of the mutant. Taken together, our data suggest that there is a stringent but incomplete developmental requirement for proper migration and positioning of fungal nuclei mediated by MoAND1 during asexual reproduction and pre-penetration phase of fungal pathogenesis.
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