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Fatty acid modulation and desaturase gene expression are differentially triggered in grapevine incompatible interaction with biotrophs and necrotrophs
Grapevine (Vitis vinifera L.) is prone to fungal and oomycete diseases. Downy and powdery mildews and grey mold, are caused by Plasmopara viticola, Erisiphe necator and Botrytis cinerea, respectively. P. viticola and E. necator are obligatory biotrophs whereas B. cinerea is a necrotroph. In tolerant...
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Published in: | Plant physiology and biochemistry 2021-06, Vol.163, p.230-238 |
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description | Grapevine (Vitis vinifera L.) is prone to fungal and oomycete diseases. Downy and powdery mildews and grey mold, are caused by Plasmopara viticola, Erisiphe necator and Botrytis cinerea, respectively. P. viticola and E. necator are obligatory biotrophs whereas B. cinerea is a necrotroph. In tolerant grapevine cultivars, plant-pathogen interaction induces defence responses, including metabolite and protein accumulation and hypersensitive reaction. Lipid and lipid-derived molecules may have a key role in the activation of defence mechanisms. Previous results suggest that V. vinifera cv Regent tolerance to P. viticola may be mediated in the first hours post inoculation by fatty acid (FA) associated signalling. In the present study we characterized FA modulation in V. vinifera cv Regent leaves upon inoculation with P. viticola, E. necator and B. cinerea and correlated FA modulation with the expression profiles of genes encoding the FA desaturases FAD6 and FAD8. In all the interactions, a progressive desaturation of stearic acid to α-linolenic acid, precursor of jasmonic acid, occurred, which was observed for a longer period against B. cinerea. Our results provide evidence of a distinct FA meditated signalling pattern in grapevine interaction with biotrophs and necrotrophs. While the interaction with the biotrophs may trigger a higher synthesis of polyunsaturated FA (PUFA) at early time-points with a tendency to return to basal levels, the interaction with B. cinerea may trigger a later and more durable induction of PUFA synthesis. In all interactions, membrane fluidity modulation occurred, which may be crucial to maintain cellular function during infection.
•Fatty acid signalling is differentially modulated in grapevine defence to P. viticola, E. necator and B. cinerea.•α-linolenic acid synthesis is induced in the first hours against biotrophs, and later against the necrotroph.•The interaction with biotrophs and the necrotroph triggers different FAD6 and FAD8 expression patterns.•An adjustment of the fatty acids degree of unsaturation occurs during the infection. |
doi_str_mv | 10.1016/j.plaphy.2021.04.001 |
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•Fatty acid signalling is differentially modulated in grapevine defence to P. viticola, E. necator and B. cinerea.•α-linolenic acid synthesis is induced in the first hours against biotrophs, and later against the necrotroph.•The interaction with biotrophs and the necrotroph triggers different FAD6 and FAD8 expression patterns.•An adjustment of the fatty acids degree of unsaturation occurs during the infection.</description><identifier>ISSN: 0981-9428</identifier><identifier>EISSN: 1873-2690</identifier><identifier>DOI: 10.1016/j.plaphy.2021.04.001</identifier><identifier>PMID: 33862502</identifier><language>eng</language><publisher>France: Elsevier Masson SAS</publisher><subject>Biotrophy ; Botrytis ; Disease Resistance ; Downy mildew ; Fatty acid desaturases ; Fatty Acids ; Gene Expression ; Gene Expression Regulation, Plant ; Grey mold ; Necrotrophy ; Oomycetes ; Plant Diseases ; Powdery mildew ; Vitis - genetics ; Vitis vinifera</subject><ispartof>Plant physiology and biochemistry, 2021-06, Vol.163, p.230-238</ispartof><rights>2021 Elsevier Masson SAS</rights><rights>Copyright © 2021 Elsevier Masson SAS. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c362t-82918e68c82472a313b9442b6f91f79b15242989db3d417c6b0d6292b72dcce63</citedby><cites>FETCH-LOGICAL-c362t-82918e68c82472a313b9442b6f91f79b15242989db3d417c6b0d6292b72dcce63</cites><orcidid>0000-0001-8156-7700 ; 0000-0001-8364-655X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33862502$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Cavaco, Ana Rita</creatorcontrib><creatorcontrib>Laureano, Gonçalo</creatorcontrib><creatorcontrib>Cunha, Jorge</creatorcontrib><creatorcontrib>Eiras-Dias, José</creatorcontrib><creatorcontrib>Matos, Ana Rita</creatorcontrib><creatorcontrib>Figueiredo, Andreia</creatorcontrib><title>Fatty acid modulation and desaturase gene expression are differentially triggered in grapevine incompatible interaction with biotrophs and necrotrophs</title><title>Plant physiology and biochemistry</title><addtitle>Plant Physiol Biochem</addtitle><description>Grapevine (Vitis vinifera L.) is prone to fungal and oomycete diseases. Downy and powdery mildews and grey mold, are caused by Plasmopara viticola, Erisiphe necator and Botrytis cinerea, respectively. P. viticola and E. necator are obligatory biotrophs whereas B. cinerea is a necrotroph. In tolerant grapevine cultivars, plant-pathogen interaction induces defence responses, including metabolite and protein accumulation and hypersensitive reaction. Lipid and lipid-derived molecules may have a key role in the activation of defence mechanisms. Previous results suggest that V. vinifera cv Regent tolerance to P. viticola may be mediated in the first hours post inoculation by fatty acid (FA) associated signalling. In the present study we characterized FA modulation in V. vinifera cv Regent leaves upon inoculation with P. viticola, E. necator and B. cinerea and correlated FA modulation with the expression profiles of genes encoding the FA desaturases FAD6 and FAD8. In all the interactions, a progressive desaturation of stearic acid to α-linolenic acid, precursor of jasmonic acid, occurred, which was observed for a longer period against B. cinerea. Our results provide evidence of a distinct FA meditated signalling pattern in grapevine interaction with biotrophs and necrotrophs. While the interaction with the biotrophs may trigger a higher synthesis of polyunsaturated FA (PUFA) at early time-points with a tendency to return to basal levels, the interaction with B. cinerea may trigger a later and more durable induction of PUFA synthesis. In all interactions, membrane fluidity modulation occurred, which may be crucial to maintain cellular function during infection.
•Fatty acid signalling is differentially modulated in grapevine defence to P. viticola, E. necator and B. cinerea.•α-linolenic acid synthesis is induced in the first hours against biotrophs, and later against the necrotroph.•The interaction with biotrophs and the necrotroph triggers different FAD6 and FAD8 expression patterns.•An adjustment of the fatty acids degree of unsaturation occurs during the infection.</description><subject>Biotrophy</subject><subject>Botrytis</subject><subject>Disease Resistance</subject><subject>Downy mildew</subject><subject>Fatty acid desaturases</subject><subject>Fatty Acids</subject><subject>Gene Expression</subject><subject>Gene Expression Regulation, Plant</subject><subject>Grey mold</subject><subject>Necrotrophy</subject><subject>Oomycetes</subject><subject>Plant Diseases</subject><subject>Powdery mildew</subject><subject>Vitis - genetics</subject><subject>Vitis vinifera</subject><issn>0981-9428</issn><issn>1873-2690</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><recordid>eNp9kc2O1DAQhC0EYoeFN0DIRy4J_hvHviChFQtIK3GBs-XYnRmPEifYzsK8CM-L5weOnKySq7q69SH0mpKWEirfHdpltMv-2DLCaEtESwh9gjZUdbxhUpOnaEO0oo0WTN2gFzkfCCFMdPw5uuFcSbYlbIN-39tSjti64PE0-3W0JcwR2-ixh2zLmmwGvIMIGH4tCXI-fyfAPgwDJIgl2HE84pLCble1xyHiXbILPIYaCtHN01KH9uNJFEjWnRt-hrLHfZhLmpd9PhdGcOmqX6Jngx0zvLq-t-j7_cdvd5-bh6-fvtx9eGgcl6w0immqQCqn6mHMcsp7LQTr5aDp0OmebplgWmnfcy9o52RPvGSa9R3zzoHkt-jtZe6S5h8r5GKmkB2Mo40wr9mwLRWScClPVnGx1iVzTjCYJYXJpqOhxJyImIO5EDEnIoYIU4nU2Jtrw9pP4P-F_iKohvcXA9Q7HwMkk12A6MCHBK4YP4f_N_wB3GSibg</recordid><startdate>202106</startdate><enddate>202106</enddate><creator>Cavaco, Ana Rita</creator><creator>Laureano, Gonçalo</creator><creator>Cunha, Jorge</creator><creator>Eiras-Dias, José</creator><creator>Matos, Ana Rita</creator><creator>Figueiredo, Andreia</creator><general>Elsevier Masson SAS</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>7X8</scope><orcidid>https://orcid.org/0000-0001-8156-7700</orcidid><orcidid>https://orcid.org/0000-0001-8364-655X</orcidid></search><sort><creationdate>202106</creationdate><title>Fatty acid modulation and desaturase gene expression are differentially triggered in grapevine incompatible interaction with biotrophs and necrotrophs</title><author>Cavaco, Ana Rita ; Laureano, Gonçalo ; Cunha, Jorge ; Eiras-Dias, José ; Matos, Ana Rita ; Figueiredo, Andreia</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c362t-82918e68c82472a313b9442b6f91f79b15242989db3d417c6b0d6292b72dcce63</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Biotrophy</topic><topic>Botrytis</topic><topic>Disease Resistance</topic><topic>Downy mildew</topic><topic>Fatty acid desaturases</topic><topic>Fatty Acids</topic><topic>Gene Expression</topic><topic>Gene Expression Regulation, Plant</topic><topic>Grey mold</topic><topic>Necrotrophy</topic><topic>Oomycetes</topic><topic>Plant Diseases</topic><topic>Powdery mildew</topic><topic>Vitis - genetics</topic><topic>Vitis vinifera</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Cavaco, Ana Rita</creatorcontrib><creatorcontrib>Laureano, Gonçalo</creatorcontrib><creatorcontrib>Cunha, Jorge</creatorcontrib><creatorcontrib>Eiras-Dias, José</creatorcontrib><creatorcontrib>Matos, Ana Rita</creatorcontrib><creatorcontrib>Figueiredo, Andreia</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Plant physiology and biochemistry</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Cavaco, Ana Rita</au><au>Laureano, Gonçalo</au><au>Cunha, Jorge</au><au>Eiras-Dias, José</au><au>Matos, Ana Rita</au><au>Figueiredo, Andreia</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Fatty acid modulation and desaturase gene expression are differentially triggered in grapevine incompatible interaction with biotrophs and necrotrophs</atitle><jtitle>Plant physiology and biochemistry</jtitle><addtitle>Plant Physiol Biochem</addtitle><date>2021-06</date><risdate>2021</risdate><volume>163</volume><spage>230</spage><epage>238</epage><pages>230-238</pages><issn>0981-9428</issn><eissn>1873-2690</eissn><abstract>Grapevine (Vitis vinifera L.) is prone to fungal and oomycete diseases. Downy and powdery mildews and grey mold, are caused by Plasmopara viticola, Erisiphe necator and Botrytis cinerea, respectively. P. viticola and E. necator are obligatory biotrophs whereas B. cinerea is a necrotroph. In tolerant grapevine cultivars, plant-pathogen interaction induces defence responses, including metabolite and protein accumulation and hypersensitive reaction. Lipid and lipid-derived molecules may have a key role in the activation of defence mechanisms. Previous results suggest that V. vinifera cv Regent tolerance to P. viticola may be mediated in the first hours post inoculation by fatty acid (FA) associated signalling. In the present study we characterized FA modulation in V. vinifera cv Regent leaves upon inoculation with P. viticola, E. necator and B. cinerea and correlated FA modulation with the expression profiles of genes encoding the FA desaturases FAD6 and FAD8. In all the interactions, a progressive desaturation of stearic acid to α-linolenic acid, precursor of jasmonic acid, occurred, which was observed for a longer period against B. cinerea. Our results provide evidence of a distinct FA meditated signalling pattern in grapevine interaction with biotrophs and necrotrophs. While the interaction with the biotrophs may trigger a higher synthesis of polyunsaturated FA (PUFA) at early time-points with a tendency to return to basal levels, the interaction with B. cinerea may trigger a later and more durable induction of PUFA synthesis. In all interactions, membrane fluidity modulation occurred, which may be crucial to maintain cellular function during infection.
•Fatty acid signalling is differentially modulated in grapevine defence to P. viticola, E. necator and B. cinerea.•α-linolenic acid synthesis is induced in the first hours against biotrophs, and later against the necrotroph.•The interaction with biotrophs and the necrotroph triggers different FAD6 and FAD8 expression patterns.•An adjustment of the fatty acids degree of unsaturation occurs during the infection.</abstract><cop>France</cop><pub>Elsevier Masson SAS</pub><pmid>33862502</pmid><doi>10.1016/j.plaphy.2021.04.001</doi><tpages>9</tpages><orcidid>https://orcid.org/0000-0001-8156-7700</orcidid><orcidid>https://orcid.org/0000-0001-8364-655X</orcidid></addata></record> |
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subjects | Biotrophy Botrytis Disease Resistance Downy mildew Fatty acid desaturases Fatty Acids Gene Expression Gene Expression Regulation, Plant Grey mold Necrotrophy Oomycetes Plant Diseases Powdery mildew Vitis - genetics Vitis vinifera |
title | Fatty acid modulation and desaturase gene expression are differentially triggered in grapevine incompatible interaction with biotrophs and necrotrophs |
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