Genome-wide functional analysis reveals that infection-related fungal autophagy is necessary for rice blast disease

School of Biosciences, University of Exeter, Geoffrey Pope Building, Stocker Road, Exeter EX4 4QD, United Kingdom.
Proceedings of the National Academy of Sciences (Impact Factor: 9.67). 09/2009; 106(37):15967-72. DOI: 10.1073/pnas.0901477106
Source: PubMed


To cause rice blast disease, the fungus Magnaporthe oryzae elaborates specialized infection structures called appressoria, which use enormous turgor to rupture the tough outer cuticle of a rice leaf. Here, we report the generation of a set of 22 isogenic M. oryzae mutants each differing by a single component of the predicted autophagic machinery of the fungus. Analysis of this set of targeted deletion mutants demonstrated that loss of any of the 16 genes necessary for nonselective macroautophagy renders the fungus unable to cause rice blast disease, due to impairment of both conidial programmed cell death and appressorium maturation. In contrast, genes necessary only for selective forms of autophagy, such as pexophagy and mitophagy, are dispensable for appressorium-mediated plant infection. A genome-wide analysis therefore demonstrates the importance of infection-associated, nonselective autophagy for the establishment of rice blast disease.

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    • "This coincides with autophagy, where all the contents of the three-celled spore are degraded before being transferred to the incipient appressorium, resulting in an enormous turgor generation of between 6 and 8 MPa (Veneault-Fourrey et al., 2006). Targeted gene deletion of any of the 16 genes involved in the non-selective macroautophagy pathway is sufficient to render the fungus non-pathogenic (Kershaw and Talbot, 2009;Deng et al., 2012;Khan et al., 2012). Alternatively, autophagy is up-regulated when the TOR signalling pathway is inactivated. "
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    ABSTRACT: The rice blast fungus, Magnaporthe oryzae, is responsible for the most serious disease of rice and is a continuing threat to ensuring global food security. The fungus has also, however, emerged as a model experimental organism for understanding plant infection processes by pathogenic fungi. This is largely due to its amenability to both classical and molecular genetics, coupled with the efforts of a very large international research community. This review, which is based on a plenary presentation at the 28th Fungal Genetics Conference in Asilomar, California in March 2015, describes recent progress in understanding how M. oryzae uses specialized cell called appressoria to bring about plant infection and the underlying biology of this developmental process. We also review how the fungus is then able to proliferate within rice tissue, deploying effector proteins to facilitate its spread by suppressing plant immunity and promoting growth and development of the fungus.
    No preview · Article · Dec 2015 · Fungal Genetics and Biology
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    • "Appressorium development occurs in response to the hard, hydrophobic rice (Oryza sativa) leaf surface (Veneault-Fourrey et al., 2006; Saunders et al., 2010). The appressorium generates pressure by accumulating osmolytes, such as glycerol, to very high concentrations and uses autophagic cell death of the conidium to recycle cellular components to the developing appressorium (Veneault-Fourrey et al., 2006; Kershaw and Talbot, 2009). "
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    ABSTRACT: Magnaporthe oryzae is the causal agent of rice blast disease, the most devastating disease of cultivated rice (Oryza sativa) and a continuing threat to global food security. To cause disease, the fungus elaborates a specialized infection cell called an appressorium, which breaches the cuticle of the rice leaf, allowing the fungus entry to plant tissue. Here, we show that the exocyst complex localizes to the tips of growing hyphae during vegetative growth, ahead of the Spitzenkörper, and is required for polarized exocytosis. However, during infection-related development, the exocyst specifically assembles in the appressorium at the point of plant infection. The exocyst components Sec3, Sec5, Sec6, Sec8, and Sec15, and exocyst complex proteins Exo70 and Exo84 localize specifically in a ring formation at the appressorium pore. Targeted gene deletion, or conditional mutation, of genes encoding exocyst components leads to impaired plant infection. We demonstrate that organization of the exocyst complex at the appressorium pore is a septin-dependent process, which also requires regulated synthesis of reactive oxygen species by the NoxR-dependent Nox2 NADPH oxidase complex. We conclude that septin-mediated assembly of the exocyst is necessary for appressorium repolarization and host cell invasion.
    Full-text · Article · Nov 2015 · The Plant Cell
    • "The CRISPR-Cas9 system is highly efficient, Box 2. Functional Genomics For functional genomic analysis of fungal virulence, researchers have generated collections of mutant strains which each lack a gene encoding a specific component of cellular machinery and/or biochemical pathway. For example, analysis of 22 Magnaporthe oryzae isolate mutants, each lacking a specific gene encoding part of the autophagic apparatus, revealed that nonselective autophagy is necessary for rice blast appressorial formation and virulence[106]. In a similar global approach, genome-wide deletion of every putative polyketide synthase in Fusarium graminearum revealed a diverse mycotoxin arsenal[110]. Other functional genomic strategies involve generation of large mutant libraries and subsequent phenotypic screening. "
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    ABSTRACT: Fungal pathogens pose serious threats to human, plant, and ecosystem health. Improved diagnostics and antifungal strategies are therefore urgently required. Here, we review recent developments in online bioinformatic tools and associated interactive data archives, which enable sophisticated comparative genomics and functional analysis of fungal pathogens in silico. Additionally, we highlight cutting-edge experimental techniques, including conditional expression systems, recyclable markers, RNA interference, genome editing, compound screens, infection models, and robotic automation, which are promising to revolutionize the study of both human and plant pathogenic fungi. These novel techniques will allow vital knowledge gaps to be addressed with regard to the evolution of virulence, host-pathogen interactions and antifungal drug therapies in both the clinic and agriculture. This, in turn, will enable delivery of improved diagnosis and durable disease-control strategies.
    No preview · Article · Nov 2015 · Trends in Microbiology
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