Mycorrhizal effector PaMiSSP10b alters polyamine biosynthesis in Eucalyptus root cells and promotes root colonization
Pathogenic microbes are known to manipulate the defences of their hosts through the production of secreted effector proteins. More recently, mutualistic mycorrhizal fungi have also been described as using these secreted effectors to promote host colonization. Here we characterize a mycorrhiza-induce...
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creator | Plett, Jonathan M. Plett, Krista L. Wong-Bajracharya, Johanna de Freitas Pereira, Maíra Costa, Maurício Dutra Kohler, Annegret Martin, Francis Anderson, Ian C. |
description | Pathogenic microbes are known to manipulate the defences of their hosts through the production of secreted effector proteins. More recently, mutualistic mycorrhizal fungi have also been described as using these secreted effectors to promote host colonization. Here we characterize a mycorrhiza-induced small secreted effector protein of 10 kDa produced by the ectomycorrhizal fungus Pisolithus albus, PaMiSSP10b.
We demonstrate that PaMiSSP10b is secreted from fungal hyphae, enters the cells of its host, Eucalyptus grandis, and interacts with an S-adenosyl methionine decarboxylase (AdoMetDC) in the polyamine pathway. Plant polyamines are regulatory molecules integral to the plant immune system during microbial challenge.
Using biochemical and transgenic approaches we show that expression of PaMiSSP10b influences levels of polyamines in the plant roots as it enhances the enzymatic activity of AdoMetDC and increases the biosynthesis of higher polyamines. This ultimately favours the colonization success of P. albus.
These results identify a new mechanism by which mutualistic microbes are able to manipulate the host's enzymatic pathways to favour colonization. |
doi_str_mv | 10.1111/nph.16759 |
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We demonstrate that PaMiSSP10b is secreted from fungal hyphae, enters the cells of its host, Eucalyptus grandis, and interacts with an S-adenosyl methionine decarboxylase (AdoMetDC) in the polyamine pathway. Plant polyamines are regulatory molecules integral to the plant immune system during microbial challenge.
Using biochemical and transgenic approaches we show that expression of PaMiSSP10b influences levels of polyamines in the plant roots as it enhances the enzymatic activity of AdoMetDC and increases the biosynthesis of higher polyamines. This ultimately favours the colonization success of P. albus.
These results identify a new mechanism by which mutualistic microbes are able to manipulate the host's enzymatic pathways to favour colonization.</description><identifier>ISSN: 0028-646X</identifier><identifier>EISSN: 1469-8137</identifier><identifier>DOI: 10.1111/nph.16759</identifier><identifier>PMID: 32562507</identifier><language>eng</language><publisher>England: Wiley</publisher><subject>Basidiomycota ; Biosynthesis ; Cells ; Colonization ; ectomycorrhizal fungus ; Ectomycorrhizas ; Environmental Sciences ; Enzymatic activity ; Enzyme activity ; Eucalyptus ; Fungi ; Hyphae ; Immune system ; Immunity ; Life Sciences ; Methionine ; Methionine decarboxylase ; Microorganisms ; mutualistic symbiosis ; Mycorrhizae ; nutrition ; Pathogens ; Pisolithus ; Plant Roots ; plant–microbe interactions ; Polyamines ; Proteins ; Symbiosis ; Transgenic plants</subject><ispartof>The New phytologist, 2020-10, Vol.228 (2), p.712-727</ispartof><rights>2020 The Authors © 2020 New Phytologist Trust</rights><rights>2020 The Authors. New Phytologist © 2020 New Phytologist Trust</rights><rights>2020 The Authors. New Phytologist © 2020 New Phytologist Trust.</rights><rights>Copyright © 2020 New Phytologist Trust</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5419-feba7a42c89dd43fdc51fa7ce6822cd05f3c80d05633efe1365eec8f6a3897363</citedby><cites>FETCH-LOGICAL-c5419-feba7a42c89dd43fdc51fa7ce6822cd05f3c80d05633efe1365eec8f6a3897363</cites><orcidid>0000-0001-6422-3754 ; 0000-0002-4737-3715 ; 0000-0001-6119-8645 ; 0000-0002-9575-9567 ; 0000-0002-3507-163X ; 0000-0003-4960-6225 ; 0000-0003-0514-8146 ; 0000-0002-0828-4437 ; 0000-0002-7659-957X ; 000000023507163X ; 0000000349606225 ; 0000000247373715 ; 0000000305148146 ; 0000000208284437 ; 0000000161198645 ; 0000000164223754 ; 0000000295759567</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/26968119$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/26968119$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,780,784,803,885,1417,1433,27924,27925,45574,45575,46409,46833,58017,58250</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32562507$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.univ-lorraine.fr/hal-02990429$$DView record in HAL$$Hfree_for_read</backlink><backlink>$$Uhttps://www.osti.gov/biblio/1787106$$D View this record in Osti.gov$$Hfree_for_read</backlink></links><search><creatorcontrib>Plett, Jonathan M.</creatorcontrib><creatorcontrib>Plett, Krista L.</creatorcontrib><creatorcontrib>Wong-Bajracharya, Johanna</creatorcontrib><creatorcontrib>de Freitas Pereira, Maíra</creatorcontrib><creatorcontrib>Costa, Maurício Dutra</creatorcontrib><creatorcontrib>Kohler, Annegret</creatorcontrib><creatorcontrib>Martin, Francis</creatorcontrib><creatorcontrib>Anderson, Ian C.</creatorcontrib><title>Mycorrhizal effector PaMiSSP10b alters polyamine biosynthesis in Eucalyptus root cells and promotes root colonization</title><title>The New phytologist</title><addtitle>New Phytol</addtitle><description>Pathogenic microbes are known to manipulate the defences of their hosts through the production of secreted effector proteins. More recently, mutualistic mycorrhizal fungi have also been described as using these secreted effectors to promote host colonization. Here we characterize a mycorrhiza-induced small secreted effector protein of 10 kDa produced by the ectomycorrhizal fungus Pisolithus albus, PaMiSSP10b.
We demonstrate that PaMiSSP10b is secreted from fungal hyphae, enters the cells of its host, Eucalyptus grandis, and interacts with an S-adenosyl methionine decarboxylase (AdoMetDC) in the polyamine pathway. Plant polyamines are regulatory molecules integral to the plant immune system during microbial challenge.
Using biochemical and transgenic approaches we show that expression of PaMiSSP10b influences levels of polyamines in the plant roots as it enhances the enzymatic activity of AdoMetDC and increases the biosynthesis of higher polyamines. This ultimately favours the colonization success of P. albus.
These results identify a new mechanism by which mutualistic microbes are able to manipulate the host's enzymatic pathways to favour colonization.</description><subject>Basidiomycota</subject><subject>Biosynthesis</subject><subject>Cells</subject><subject>Colonization</subject><subject>ectomycorrhizal fungus</subject><subject>Ectomycorrhizas</subject><subject>Environmental Sciences</subject><subject>Enzymatic activity</subject><subject>Enzyme activity</subject><subject>Eucalyptus</subject><subject>Fungi</subject><subject>Hyphae</subject><subject>Immune system</subject><subject>Immunity</subject><subject>Life Sciences</subject><subject>Methionine</subject><subject>Methionine decarboxylase</subject><subject>Microorganisms</subject><subject>mutualistic symbiosis</subject><subject>Mycorrhizae</subject><subject>nutrition</subject><subject>Pathogens</subject><subject>Pisolithus</subject><subject>Plant Roots</subject><subject>plant–microbe interactions</subject><subject>Polyamines</subject><subject>Proteins</subject><subject>Symbiosis</subject><subject>Transgenic plants</subject><issn>0028-646X</issn><issn>1469-8137</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kV-L1DAUxYso7rj64AdQgr7oQ3fzp02ax2VZHWFWB1bBt5BJE5qhTbpJqtRPb8bujCCYlwOX3z03h1MULxG8QPldurG7QJTV_FGxQhXlZYMIe1ysIMRNSSv6_ax4FuMeQshrip8WZwRnrSFbFdPtrHwInf0le6CN0Sr5ALby1t7dbRHcAdknHSIYfT_LwToNdtbH2aVORxuBdeBmUrKfxzRFELxPQOm-j0C6FozBDz7p49z33uUzyXr3vHhiZB_1iwc9L759uPl6vS43Xz5-ur7alKquEC-N3kkmK6wa3rYVMa2qkZFMadpgrFpYG6IamJUSoo1GhNZaq8ZQSRrOCCXnxZvF18dkRVQ2adUp71yOKRBrGIIH6P0CdbIXY7CDDLPw0or11UYcZhBzDivMf6DMvlvYnO1-0jGJwcZDYum0n6LAFaoxr7JvRt_-g-79FFyOm6mqxjVjDf97XAUfY9Dm9AMExaFckcsVf8rN7OsHx2k36PZEHtvMwOUC_LS9nv_vJD5v10fLV8vGPubeTxuYctogxMlvJ3a4WA</recordid><startdate>202010</startdate><enddate>202010</enddate><creator>Plett, Jonathan M.</creator><creator>Plett, Krista L.</creator><creator>Wong-Bajracharya, Johanna</creator><creator>de Freitas Pereira, Maíra</creator><creator>Costa, Maurício Dutra</creator><creator>Kohler, Annegret</creator><creator>Martin, Francis</creator><creator>Anderson, Ian C.</creator><general>Wiley</general><general>Wiley Subscription Services, Inc</general><general>Wiley-Blackwell</general><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>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><scope>1XC</scope><scope>OTOTI</scope><orcidid>https://orcid.org/0000-0001-6422-3754</orcidid><orcidid>https://orcid.org/0000-0002-4737-3715</orcidid><orcidid>https://orcid.org/0000-0001-6119-8645</orcidid><orcidid>https://orcid.org/0000-0002-9575-9567</orcidid><orcidid>https://orcid.org/0000-0002-3507-163X</orcidid><orcidid>https://orcid.org/0000-0003-4960-6225</orcidid><orcidid>https://orcid.org/0000-0003-0514-8146</orcidid><orcidid>https://orcid.org/0000-0002-0828-4437</orcidid><orcidid>https://orcid.org/0000-0002-7659-957X</orcidid><orcidid>https://orcid.org/000000023507163X</orcidid><orcidid>https://orcid.org/0000000349606225</orcidid><orcidid>https://orcid.org/0000000247373715</orcidid><orcidid>https://orcid.org/0000000305148146</orcidid><orcidid>https://orcid.org/0000000208284437</orcidid><orcidid>https://orcid.org/0000000161198645</orcidid><orcidid>https://orcid.org/0000000164223754</orcidid><orcidid>https://orcid.org/0000000295759567</orcidid></search><sort><creationdate>202010</creationdate><title>Mycorrhizal effector PaMiSSP10b alters polyamine biosynthesis in Eucalyptus root cells and promotes root colonization</title><author>Plett, Jonathan M. ; 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More recently, mutualistic mycorrhizal fungi have also been described as using these secreted effectors to promote host colonization. Here we characterize a mycorrhiza-induced small secreted effector protein of 10 kDa produced by the ectomycorrhizal fungus Pisolithus albus, PaMiSSP10b.
We demonstrate that PaMiSSP10b is secreted from fungal hyphae, enters the cells of its host, Eucalyptus grandis, and interacts with an S-adenosyl methionine decarboxylase (AdoMetDC) in the polyamine pathway. Plant polyamines are regulatory molecules integral to the plant immune system during microbial challenge.
Using biochemical and transgenic approaches we show that expression of PaMiSSP10b influences levels of polyamines in the plant roots as it enhances the enzymatic activity of AdoMetDC and increases the biosynthesis of higher polyamines. This ultimately favours the colonization success of P. albus.
These results identify a new mechanism by which mutualistic microbes are able to manipulate the host's enzymatic pathways to favour colonization.</abstract><cop>England</cop><pub>Wiley</pub><pmid>32562507</pmid><doi>10.1111/nph.16759</doi><tpages>16</tpages><orcidid>https://orcid.org/0000-0001-6422-3754</orcidid><orcidid>https://orcid.org/0000-0002-4737-3715</orcidid><orcidid>https://orcid.org/0000-0001-6119-8645</orcidid><orcidid>https://orcid.org/0000-0002-9575-9567</orcidid><orcidid>https://orcid.org/0000-0002-3507-163X</orcidid><orcidid>https://orcid.org/0000-0003-4960-6225</orcidid><orcidid>https://orcid.org/0000-0003-0514-8146</orcidid><orcidid>https://orcid.org/0000-0002-0828-4437</orcidid><orcidid>https://orcid.org/0000-0002-7659-957X</orcidid><orcidid>https://orcid.org/000000023507163X</orcidid><orcidid>https://orcid.org/0000000349606225</orcidid><orcidid>https://orcid.org/0000000247373715</orcidid><orcidid>https://orcid.org/0000000305148146</orcidid><orcidid>https://orcid.org/0000000208284437</orcidid><orcidid>https://orcid.org/0000000161198645</orcidid><orcidid>https://orcid.org/0000000164223754</orcidid><orcidid>https://orcid.org/0000000295759567</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Basidiomycota Biosynthesis Cells Colonization ectomycorrhizal fungus Ectomycorrhizas Environmental Sciences Enzymatic activity Enzyme activity Eucalyptus Fungi Hyphae Immune system Immunity Life Sciences Methionine Methionine decarboxylase Microorganisms mutualistic symbiosis Mycorrhizae nutrition Pathogens Pisolithus Plant Roots plant–microbe interactions Polyamines Proteins Symbiosis Transgenic plants |
title | Mycorrhizal effector PaMiSSP10b alters polyamine biosynthesis in Eucalyptus root cells and promotes root colonization |
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