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The Phytophthora sojae RXLR effector Avh238 destabilizes soybean Type2 GmACSs to suppress ethylene biosynthesis and promote infection
• Phytophthora pathogens secrete many effector proteins to manipulate host innate immunity. PsAvh238 is a Phytophthora sojae N-terminal Arg-X-Leu-Arg (RXLR) effector, which evolved to escape host recognition by mutating one nucleotide while retaining plant immunity- suppressing activity to enhance i...
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Published in: | The New phytologist 2019-04, Vol.222 (1), p.425-437 |
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container_title | The New phytologist |
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creator | Yang, Bo Wang, Yuyin Guo, Baodian Jing, Maofeng Zhou, Hao Li, Yufei Wang, Haonan Huang, Jie Wang, Yan Ye, Wenwu Dong, Suomeng Wang, Yuanchao |
description | • Phytophthora pathogens secrete many effector proteins to manipulate host innate immunity. PsAvh238 is a Phytophthora sojae N-terminal Arg-X-Leu-Arg (RXLR) effector, which evolved to escape host recognition by mutating one nucleotide while retaining plant immunity- suppressing activity to enhance infection. However, the molecular basis of the PsAvh238 virulence function remains largely enigmatic.
• By using coimmunoprecipitation and liquid chromatography-tandem mass spectrometry analysis, we identified the 1-aminocyclopropane-1-carboxylate synthase (ACS) isoforms, the key enzymes in ethylene (ET) biosynthesis, as a host target of PsAvh238.
• We show that PsAvh238 interacts with soybean ACSs (GmACSs) in vivo and in vitro. By destabilizing Type2 GmACSs, PsAvh238 suppresses Type2 ACS-catalyzed ET biosynthesis and facilitates Phytophthora infection. Silencing of Type2 GmACSs, and inhibition of ET biosynthesis or signaling, increase soybean susceptibility to P. sojae infection, supporting a role for Type2 GmACSs and ET in plant immunity against P. sojae. Moreover, wild-type P. sojae but not the PsAvh238-disrupted mutants, inhibits ET induction and promotes P. sojae infection in soybean.
• Our results highlight the ET biosynthesis pathway as an essential part in plant immunity against P. sojae and a direct effector target. |
doi_str_mv | 10.1111/nph.15581 |
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• By using coimmunoprecipitation and liquid chromatography-tandem mass spectrometry analysis, we identified the 1-aminocyclopropane-1-carboxylate synthase (ACS) isoforms, the key enzymes in ethylene (ET) biosynthesis, as a host target of PsAvh238.
• We show that PsAvh238 interacts with soybean ACSs (GmACSs) in vivo and in vitro. By destabilizing Type2 GmACSs, PsAvh238 suppresses Type2 ACS-catalyzed ET biosynthesis and facilitates Phytophthora infection. Silencing of Type2 GmACSs, and inhibition of ET biosynthesis or signaling, increase soybean susceptibility to P. sojae infection, supporting a role for Type2 GmACSs and ET in plant immunity against P. sojae. Moreover, wild-type P. sojae but not the PsAvh238-disrupted mutants, inhibits ET induction and promotes P. sojae infection in soybean.
• Our results highlight the ET biosynthesis pathway as an essential part in plant immunity against P. sojae and a direct effector target.</description><identifier>ISSN: 0028-646X</identifier><identifier>EISSN: 1469-8137</identifier><identifier>DOI: 10.1111/nph.15581</identifier><identifier>PMID: 30394556</identifier><language>eng</language><publisher>England: Wiley</publisher><subject>Biosynthesis ; Disease Resistance ; Enzyme Stability ; Ethene ; Ethylene ; Ethylenes - metabolism ; Gene Silencing ; Glycine max ; Glycine max - immunology ; Glycine max - metabolism ; Glycine max - microbiology ; Immunity ; Infections ; Innate immunity ; Isoforms ; Liquid chromatography ; Lyases - metabolism ; Mass spectrometry ; Mass spectroscopy ; Mutants ; Mutation - genetics ; Nicotiana - genetics ; Nicotiana - microbiology ; Nucleotides ; Pathogens ; Phytophthora ; Phytophthora - physiology ; Phytophthora sojae ; Plant Diseases - microbiology ; Plant immunity ; Plants, Genetically Modified ; Proteasome Endopeptidase Complex - metabolism ; Protein Binding ; Proteins ; Proteins - metabolism ; RXLR effector ; Secretion ; Soybeans ; Type2 ACS ; Virulence</subject><ispartof>The New phytologist, 2019-04, Vol.222 (1), p.425-437</ispartof><rights>2018 The Authors © 2018 New Phytologist Trust</rights><rights>2018 The Authors. New Phytologist © 2018 New Phytologist Trust</rights><rights>2018 The Authors. New Phytologist © 2018 New Phytologist Trust.</rights><rights>Copyright © 2019 New Phytologist Trust</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><orcidid>0000-0001-5803-5343 ; 0000-0002-9623-6776 ; 0000-0002-6657-8740</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/26629257$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/26629257$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>314,776,780,27901,27902,58213,58446</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30394556$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Yang, Bo</creatorcontrib><creatorcontrib>Wang, Yuyin</creatorcontrib><creatorcontrib>Guo, Baodian</creatorcontrib><creatorcontrib>Jing, Maofeng</creatorcontrib><creatorcontrib>Zhou, Hao</creatorcontrib><creatorcontrib>Li, Yufei</creatorcontrib><creatorcontrib>Wang, Haonan</creatorcontrib><creatorcontrib>Huang, Jie</creatorcontrib><creatorcontrib>Wang, Yan</creatorcontrib><creatorcontrib>Ye, Wenwu</creatorcontrib><creatorcontrib>Dong, Suomeng</creatorcontrib><creatorcontrib>Wang, Yuanchao</creatorcontrib><title>The Phytophthora sojae RXLR effector Avh238 destabilizes soybean Type2 GmACSs to suppress ethylene biosynthesis and promote infection</title><title>The New phytologist</title><addtitle>New Phytol</addtitle><description>• Phytophthora pathogens secrete many effector proteins to manipulate host innate immunity. PsAvh238 is a Phytophthora sojae N-terminal Arg-X-Leu-Arg (RXLR) effector, which evolved to escape host recognition by mutating one nucleotide while retaining plant immunity- suppressing activity to enhance infection. However, the molecular basis of the PsAvh238 virulence function remains largely enigmatic.
• By using coimmunoprecipitation and liquid chromatography-tandem mass spectrometry analysis, we identified the 1-aminocyclopropane-1-carboxylate synthase (ACS) isoforms, the key enzymes in ethylene (ET) biosynthesis, as a host target of PsAvh238.
• We show that PsAvh238 interacts with soybean ACSs (GmACSs) in vivo and in vitro. By destabilizing Type2 GmACSs, PsAvh238 suppresses Type2 ACS-catalyzed ET biosynthesis and facilitates Phytophthora infection. Silencing of Type2 GmACSs, and inhibition of ET biosynthesis or signaling, increase soybean susceptibility to P. sojae infection, supporting a role for Type2 GmACSs and ET in plant immunity against P. sojae. Moreover, wild-type P. sojae but not the PsAvh238-disrupted mutants, inhibits ET induction and promotes P. sojae infection in soybean.
• Our results highlight the ET biosynthesis pathway as an essential part in plant immunity against P. sojae and a direct effector target.</description><subject>Biosynthesis</subject><subject>Disease Resistance</subject><subject>Enzyme Stability</subject><subject>Ethene</subject><subject>Ethylene</subject><subject>Ethylenes - metabolism</subject><subject>Gene Silencing</subject><subject>Glycine max</subject><subject>Glycine max - immunology</subject><subject>Glycine max - metabolism</subject><subject>Glycine max - microbiology</subject><subject>Immunity</subject><subject>Infections</subject><subject>Innate immunity</subject><subject>Isoforms</subject><subject>Liquid chromatography</subject><subject>Lyases - metabolism</subject><subject>Mass spectrometry</subject><subject>Mass spectroscopy</subject><subject>Mutants</subject><subject>Mutation - genetics</subject><subject>Nicotiana - genetics</subject><subject>Nicotiana - microbiology</subject><subject>Nucleotides</subject><subject>Pathogens</subject><subject>Phytophthora</subject><subject>Phytophthora - physiology</subject><subject>Phytophthora sojae</subject><subject>Plant Diseases - microbiology</subject><subject>Plant immunity</subject><subject>Plants, Genetically Modified</subject><subject>Proteasome Endopeptidase Complex - metabolism</subject><subject>Protein Binding</subject><subject>Proteins</subject><subject>Proteins - metabolism</subject><subject>RXLR effector</subject><subject>Secretion</subject><subject>Soybeans</subject><subject>Type2 ACS</subject><subject>Virulence</subject><issn>0028-646X</issn><issn>1469-8137</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><recordid>eNpdkcFO3DAQhi1EVba0Bx4AZIlLLwHbEzvJcbWiUGlFEd1K3CInmSiOEjvECVV673vXsMChc5mR5vtHM_MTcsLZBQ9xaYfmgkuZ8gOy4rHKopRDckhWjIk0UrF6OCKfvG8ZY5lU4iM5AgZZLKVakb-7Bulds0xuaKbGjZp612qk9w_be4p1jeXkRrp-agSktEI_6cJ05g_6wC0Fakt3y4CCXvfrzU9PJ0f9PAwjek9xapYOLdLCOL_YqUFvPNW2osPoejchNfZ5vnH2M_lQ687jl9d8TH59u9ptbqLtj-vvm_U2agEUj0CJRPIyTUoQsU4zXUGlBNegdFLIWpaa6VgojkUtsjorigpRJKKsAcpSKw7H5Ot-btjgcQ7X5L3xJXadtuhmnwsOjMk0Fiyg5_-hrZtHG7YLVKoUgEziQJ29UnPRY5UPo-n1uORvDw7A5R74bTpc3vuc5c_O5cG5_MW5_Pbu5qUIitO9ovXh9e8KoZTIhEzgHyyElZ8</recordid><startdate>20190401</startdate><enddate>20190401</enddate><creator>Yang, Bo</creator><creator>Wang, Yuyin</creator><creator>Guo, Baodian</creator><creator>Jing, Maofeng</creator><creator>Zhou, Hao</creator><creator>Li, Yufei</creator><creator>Wang, Haonan</creator><creator>Huang, Jie</creator><creator>Wang, Yan</creator><creator>Ye, Wenwu</creator><creator>Dong, Suomeng</creator><creator>Wang, Yuanchao</creator><general>Wiley</general><general>Wiley Subscription Services, Inc</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>7QO</scope><scope>7SN</scope><scope>8FD</scope><scope>C1K</scope><scope>F1W</scope><scope>FR3</scope><scope>H95</scope><scope>L.G</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0001-5803-5343</orcidid><orcidid>https://orcid.org/0000-0002-9623-6776</orcidid><orcidid>https://orcid.org/0000-0002-6657-8740</orcidid></search><sort><creationdate>20190401</creationdate><title>The Phytophthora sojae RXLR effector Avh238 destabilizes soybean Type2 GmACSs to suppress ethylene biosynthesis and promote infection</title><author>Yang, Bo ; Wang, Yuyin ; Guo, Baodian ; Jing, Maofeng ; Zhou, Hao ; Li, Yufei ; Wang, Haonan ; Huang, Jie ; Wang, Yan ; Ye, Wenwu ; Dong, Suomeng ; Wang, Yuanchao</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-j3361-362751c87c324a89ad3d621a36a7b5f5ca0a4261ebf29f9bbdee272cf33cca613</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Biosynthesis</topic><topic>Disease Resistance</topic><topic>Enzyme Stability</topic><topic>Ethene</topic><topic>Ethylene</topic><topic>Ethylenes - metabolism</topic><topic>Gene Silencing</topic><topic>Glycine max</topic><topic>Glycine max - immunology</topic><topic>Glycine max - metabolism</topic><topic>Glycine max - microbiology</topic><topic>Immunity</topic><topic>Infections</topic><topic>Innate immunity</topic><topic>Isoforms</topic><topic>Liquid chromatography</topic><topic>Lyases - metabolism</topic><topic>Mass spectrometry</topic><topic>Mass spectroscopy</topic><topic>Mutants</topic><topic>Mutation - genetics</topic><topic>Nicotiana - genetics</topic><topic>Nicotiana - microbiology</topic><topic>Nucleotides</topic><topic>Pathogens</topic><topic>Phytophthora</topic><topic>Phytophthora - physiology</topic><topic>Phytophthora sojae</topic><topic>Plant Diseases - microbiology</topic><topic>Plant immunity</topic><topic>Plants, Genetically Modified</topic><topic>Proteasome Endopeptidase Complex - metabolism</topic><topic>Protein Binding</topic><topic>Proteins</topic><topic>Proteins - metabolism</topic><topic>RXLR effector</topic><topic>Secretion</topic><topic>Soybeans</topic><topic>Type2 ACS</topic><topic>Virulence</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Yang, Bo</creatorcontrib><creatorcontrib>Wang, Yuyin</creatorcontrib><creatorcontrib>Guo, Baodian</creatorcontrib><creatorcontrib>Jing, Maofeng</creatorcontrib><creatorcontrib>Zhou, Hao</creatorcontrib><creatorcontrib>Li, Yufei</creatorcontrib><creatorcontrib>Wang, Haonan</creatorcontrib><creatorcontrib>Huang, Jie</creatorcontrib><creatorcontrib>Wang, Yan</creatorcontrib><creatorcontrib>Ye, Wenwu</creatorcontrib><creatorcontrib>Dong, Suomeng</creatorcontrib><creatorcontrib>Wang, Yuanchao</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>Biotechnology Research Abstracts</collection><collection>Ecology Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Engineering Research Database</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>The New phytologist</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Yang, Bo</au><au>Wang, Yuyin</au><au>Guo, Baodian</au><au>Jing, Maofeng</au><au>Zhou, Hao</au><au>Li, Yufei</au><au>Wang, Haonan</au><au>Huang, Jie</au><au>Wang, Yan</au><au>Ye, Wenwu</au><au>Dong, Suomeng</au><au>Wang, Yuanchao</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The Phytophthora sojae RXLR effector Avh238 destabilizes soybean Type2 GmACSs to suppress ethylene biosynthesis and promote infection</atitle><jtitle>The New phytologist</jtitle><addtitle>New Phytol</addtitle><date>2019-04-01</date><risdate>2019</risdate><volume>222</volume><issue>1</issue><spage>425</spage><epage>437</epage><pages>425-437</pages><issn>0028-646X</issn><eissn>1469-8137</eissn><abstract>• Phytophthora pathogens secrete many effector proteins to manipulate host innate immunity. PsAvh238 is a Phytophthora sojae N-terminal Arg-X-Leu-Arg (RXLR) effector, which evolved to escape host recognition by mutating one nucleotide while retaining plant immunity- suppressing activity to enhance infection. However, the molecular basis of the PsAvh238 virulence function remains largely enigmatic.
• By using coimmunoprecipitation and liquid chromatography-tandem mass spectrometry analysis, we identified the 1-aminocyclopropane-1-carboxylate synthase (ACS) isoforms, the key enzymes in ethylene (ET) biosynthesis, as a host target of PsAvh238.
• We show that PsAvh238 interacts with soybean ACSs (GmACSs) in vivo and in vitro. By destabilizing Type2 GmACSs, PsAvh238 suppresses Type2 ACS-catalyzed ET biosynthesis and facilitates Phytophthora infection. Silencing of Type2 GmACSs, and inhibition of ET biosynthesis or signaling, increase soybean susceptibility to P. sojae infection, supporting a role for Type2 GmACSs and ET in plant immunity against P. sojae. Moreover, wild-type P. sojae but not the PsAvh238-disrupted mutants, inhibits ET induction and promotes P. sojae infection in soybean.
• Our results highlight the ET biosynthesis pathway as an essential part in plant immunity against P. sojae and a direct effector target.</abstract><cop>England</cop><pub>Wiley</pub><pmid>30394556</pmid><doi>10.1111/nph.15581</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0001-5803-5343</orcidid><orcidid>https://orcid.org/0000-0002-9623-6776</orcidid><orcidid>https://orcid.org/0000-0002-6657-8740</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Biosynthesis Disease Resistance Enzyme Stability Ethene Ethylene Ethylenes - metabolism Gene Silencing Glycine max Glycine max - immunology Glycine max - metabolism Glycine max - microbiology Immunity Infections Innate immunity Isoforms Liquid chromatography Lyases - metabolism Mass spectrometry Mass spectroscopy Mutants Mutation - genetics Nicotiana - genetics Nicotiana - microbiology Nucleotides Pathogens Phytophthora Phytophthora - physiology Phytophthora sojae Plant Diseases - microbiology Plant immunity Plants, Genetically Modified Proteasome Endopeptidase Complex - metabolism Protein Binding Proteins Proteins - metabolism RXLR effector Secretion Soybeans Type2 ACS Virulence |
title | The Phytophthora sojae RXLR effector Avh238 destabilizes soybean Type2 GmACSs to suppress ethylene biosynthesis and promote infection |
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