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Genome-wide functional analysis reveals that infection-associated fungal autophagy is necessary for rice blast disease
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...
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Published in: | Proceedings of the National Academy of Sciences - PNAS 2009-09, Vol.106 (37), p.15967-15972 |
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description | 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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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.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.0901477106</identifier><identifier>PMID: 19717456</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Apoptosis ; Appressoria ; autophagy ; Autophagy - genetics ; Autophagy - physiology ; Biological Sciences ; blast disease ; Blasts ; Cell death ; Conidia ; Fungi ; Gene Deletion ; Gene expression regulation ; Genes ; Genes, Fungal ; Genome, Fungal ; Genome-Wide Association Study ; Genomics ; Green Fluorescent Proteins - genetics ; Host-Pathogen Interactions - genetics ; Host-Pathogen Interactions - physiology ; host-pathogen relationships ; Infections ; Magnaporthe ; Magnaporthe - genetics ; Magnaporthe - pathogenicity ; Magnaporthe - physiology ; Magnaporthe grisea ; Magnaporthe oryzae ; microbial genetics ; Microscopy, Fluorescence ; mutants ; Mutation ; Oryza - microbiology ; Oryza sativa ; Plant diseases ; Plant Diseases - microbiology ; Recombinant Proteins - genetics ; Rice</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2009-09, Vol.106 (37), p.15967-15972</ispartof><rights>Copyright National Academy of Sciences Sep 15, 2009</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c554t-9f864a8e363b63f57d5837fc289fbebb15b713ebcf1091250101d07b2777123a3</citedby><cites>FETCH-LOGICAL-c554t-9f864a8e363b63f57d5837fc289fbebb15b713ebcf1091250101d07b2777123a3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Uhttp://www.pnas.org/content/106/37.cover.gif</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/40484831$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/40484831$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793,58238,58471</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/19717456$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kershaw, Michael J</creatorcontrib><creatorcontrib>Talbot, Nicholas J</creatorcontrib><title>Genome-wide functional analysis reveals that infection-associated fungal autophagy is necessary for rice blast disease</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>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.</description><subject>Apoptosis</subject><subject>Appressoria</subject><subject>autophagy</subject><subject>Autophagy - genetics</subject><subject>Autophagy - physiology</subject><subject>Biological Sciences</subject><subject>blast disease</subject><subject>Blasts</subject><subject>Cell death</subject><subject>Conidia</subject><subject>Fungi</subject><subject>Gene Deletion</subject><subject>Gene expression regulation</subject><subject>Genes</subject><subject>Genes, Fungal</subject><subject>Genome, Fungal</subject><subject>Genome-Wide Association Study</subject><subject>Genomics</subject><subject>Green Fluorescent Proteins - genetics</subject><subject>Host-Pathogen Interactions - genetics</subject><subject>Host-Pathogen Interactions - physiology</subject><subject>host-pathogen relationships</subject><subject>Infections</subject><subject>Magnaporthe</subject><subject>Magnaporthe - genetics</subject><subject>Magnaporthe - pathogenicity</subject><subject>Magnaporthe - physiology</subject><subject>Magnaporthe grisea</subject><subject>Magnaporthe oryzae</subject><subject>microbial genetics</subject><subject>Microscopy, Fluorescence</subject><subject>mutants</subject><subject>Mutation</subject><subject>Oryza - microbiology</subject><subject>Oryza sativa</subject><subject>Plant diseases</subject><subject>Plant Diseases - microbiology</subject><subject>Recombinant Proteins - genetics</subject><subject>Rice</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2009</creationdate><recordtype>article</recordtype><recordid>eNqFkc1v1DAQxSMEokvhzAmwekDikHb8FScXJFRBQarEAXq2nGS861U2XmxnYf_7OuyqC1y42If5vad584riJYVLCopfbUcTL6EBKpSiUD0qFhQaWlaigcfFAoCpshZMnBXPYlwDQCNreFqc0UZRJWS1KHY3OPoNlj9dj8ROY5ecH81ATH720UUScIdmiCStTCJutPibKE2MvnMmYT-rlrNiSn67Mss9yaoRO4zRhD2xPpDgOiTtYGIivYtoIj4vntjsii-O_3lx9-nj9-vP5e3Xmy_XH27LTkqRysbWlTA18oq3FbdS9bLmynasbmyLbUtlqyjHtrNzbCaBAu1BtUzlczBu-Hnx_uC7ndoN9h2OKZhBb4Pb5OW0N07_PRndSi_9TjMlFGMqG7w9GgT_Y8KY9MbFDofBjOinqBmlALKhGbz4B1z7KeQrZibXQ1nNRYauDlAXfIwB7cMmFPRcqJ4L1adCs-L1nwFO_LHBDLw7ArPyZFdprjSVTaW0nYYh4a-UWfIfNiOvDsg6Jh8eGAGiFjWfY745zK3x2iyDi_ruWw7IgVY1SKn4PWFEyho</recordid><startdate>20090915</startdate><enddate>20090915</enddate><creator>Kershaw, Michael J</creator><creator>Talbot, Nicholas J</creator><general>National Academy of Sciences</general><general>National Acad Sciences</general><scope>FBQ</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>F1W</scope><scope>H95</scope><scope>L.G</scope><scope>5PM</scope></search><sort><creationdate>20090915</creationdate><title>Genome-wide functional analysis reveals that infection-associated fungal autophagy is necessary for rice blast disease</title><author>Kershaw, Michael J ; Talbot, Nicholas J</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c554t-9f864a8e363b63f57d5837fc289fbebb15b713ebcf1091250101d07b2777123a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2009</creationdate><topic>Apoptosis</topic><topic>Appressoria</topic><topic>autophagy</topic><topic>Autophagy - genetics</topic><topic>Autophagy - physiology</topic><topic>Biological Sciences</topic><topic>blast disease</topic><topic>Blasts</topic><topic>Cell death</topic><topic>Conidia</topic><topic>Fungi</topic><topic>Gene Deletion</topic><topic>Gene expression regulation</topic><topic>Genes</topic><topic>Genes, Fungal</topic><topic>Genome, Fungal</topic><topic>Genome-Wide Association Study</topic><topic>Genomics</topic><topic>Green Fluorescent Proteins - genetics</topic><topic>Host-Pathogen Interactions - genetics</topic><topic>Host-Pathogen Interactions - physiology</topic><topic>host-pathogen relationships</topic><topic>Infections</topic><topic>Magnaporthe</topic><topic>Magnaporthe - genetics</topic><topic>Magnaporthe - pathogenicity</topic><topic>Magnaporthe - physiology</topic><topic>Magnaporthe grisea</topic><topic>Magnaporthe oryzae</topic><topic>microbial genetics</topic><topic>Microscopy, Fluorescence</topic><topic>mutants</topic><topic>Mutation</topic><topic>Oryza - microbiology</topic><topic>Oryza sativa</topic><topic>Plant diseases</topic><topic>Plant Diseases - microbiology</topic><topic>Recombinant Proteins - genetics</topic><topic>Rice</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kershaw, Michael J</creatorcontrib><creatorcontrib>Talbot, Nicholas J</creatorcontrib><collection>AGRIS</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kershaw, Michael J</au><au>Talbot, Nicholas J</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Genome-wide functional analysis reveals that infection-associated fungal autophagy is necessary for rice blast disease</atitle><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle><addtitle>Proc Natl Acad Sci U S A</addtitle><date>2009-09-15</date><risdate>2009</risdate><volume>106</volume><issue>37</issue><spage>15967</spage><epage>15972</epage><pages>15967-15972</pages><issn>0027-8424</issn><eissn>1091-6490</eissn><abstract>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. 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subjects | Apoptosis Appressoria autophagy Autophagy - genetics Autophagy - physiology Biological Sciences blast disease Blasts Cell death Conidia Fungi Gene Deletion Gene expression regulation Genes Genes, Fungal Genome, Fungal Genome-Wide Association Study Genomics Green Fluorescent Proteins - genetics Host-Pathogen Interactions - genetics Host-Pathogen Interactions - physiology host-pathogen relationships Infections Magnaporthe Magnaporthe - genetics Magnaporthe - pathogenicity Magnaporthe - physiology Magnaporthe grisea Magnaporthe oryzae microbial genetics Microscopy, Fluorescence mutants Mutation Oryza - microbiology Oryza sativa Plant diseases Plant Diseases - microbiology Recombinant Proteins - genetics Rice |
title | Genome-wide functional analysis reveals that infection-associated fungal autophagy is necessary for rice blast disease |
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