Medicarpin confers powdery mildew resistance in Medicago truncatula and activates the salicylic acid signalling pathway
Powdery mildew (PM) caused by the obligate biotrophic fungal pathogen Erysiphe pisi is an economically important disease of legumes. Legumes are rich in isoflavonoids, a class of secondary metabolites whose role in PM resistance is ambiguous. Here we show that the pterocarpan medicarpin accumulates...
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Veröffentlicht in: | Molecular plant pathology 2022-07, Vol.23 (7), p.966-983 |
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description | Powdery mildew (PM) caused by the obligate biotrophic fungal pathogen Erysiphe pisi is an economically important disease of legumes. Legumes are rich in isoflavonoids, a class of secondary metabolites whose role in PM resistance is ambiguous. Here we show that the pterocarpan medicarpin accumulates at fungal infection sites, as analysed by fluorescein‐tagged medicarpin, and provides penetration and post‐penetration resistance against E. pisi in Medicago truncatula in part through the activation of the salicylic acid (SA) signalling pathway. Comparative gene expression and metabolite analyses revealed an early induction of isoflavonoid biosynthesis and accumulation of the defence phytohormones SA and jasmonic acid (JA) in the highly resistant M. truncatula genotype A17 but not in moderately susceptible R108 in response to PM infection. Pretreatment of R108 leaves with medicarpin increased SA levels, SA‐associated gene expression, and accumulation of hydrogen peroxide at PM infection sites, and reduced fungal penetration and colony formation. Strong parallels in the levels of medicarpin and SA, but not JA, were observed on medicarpin/SA treatment pre‐ or post‐PM infection. Collectively, our results suggest that medicarpin and SA may act in concert to restrict E. pisi growth, providing new insights into the metabolic and signalling pathways required for PM resistance in legumes.
Infection‐localized accumulation of the isoflavonoid phytoalexin medicarpin provides resistance against the pea powdery mildew pathogen and activates salicylic acid signalling in Medicago truncatula. |
doi_str_mv | 10.1111/mpp.13202 |
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Infection‐localized accumulation of the isoflavonoid phytoalexin medicarpin provides resistance against the pea powdery mildew pathogen and activates salicylic acid signalling in Medicago truncatula.</description><identifier>ISSN: 1464-6722</identifier><identifier>EISSN: 1364-3703</identifier><identifier>DOI: 10.1111/mpp.13202</identifier><identifier>PMID: 35263504</identifier><language>eng</language><publisher>England: John Wiley & Sons, Inc</publisher><subject>Accumulation ; Airborne microorganisms ; Alfalfa ; Biosynthesis ; Economic importance ; Flavonoids ; Fluorescein ; fluorescein‐tagged medicarpin ; Fungi ; Gene expression ; Genomes ; Genotypes ; Hydrogen peroxide ; Infections ; isoflavone reductase ; Isoflavonoids ; Jasmonic acid ; Legumes ; Medicago truncatula ; Metabolites ; Original ; Pathogens ; Penetration ; Penetration resistance ; phytoalexin ; Plant diseases ; Plant hormones ; Powdery mildew ; Salicylic acid ; Secondary metabolites ; Signal transduction ; Signaling</subject><ispartof>Molecular plant pathology, 2022-07, Vol.23 (7), p.966-983</ispartof><rights>2022 The Authors. published by British Society for Plant Pathology and John Wiley & Sons Ltd.</rights><rights>2022 The Authors. Molecular Plant Pathology published by British Society for Plant Pathology and John Wiley & Sons Ltd.</rights><rights>2022. This work is published under http://creativecommons.org/licenses/by-nc/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4432-1a737fb423e3163dcd7c378b09a5ce4bcfd4ac3ce4623a5364f30d4c88901c833</citedby><cites>FETCH-LOGICAL-c4432-1a737fb423e3163dcd7c378b09a5ce4bcfd4ac3ce4623a5364f30d4c88901c833</cites><orcidid>0000-0003-2758-2461 ; 0000-0001-6206-8826</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9190973/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9190973/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,1417,11562,27924,27925,45574,45575,46052,46476,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35263504$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Gupta, Arunima</creatorcontrib><creatorcontrib>Awasthi, Pallavi</creatorcontrib><creatorcontrib>Sharma, Neha</creatorcontrib><creatorcontrib>Parveen, Sajiya</creatorcontrib><creatorcontrib>Vats, Ravi P.</creatorcontrib><creatorcontrib>Singh, Nirpendra</creatorcontrib><creatorcontrib>Kumar, Yashwant</creatorcontrib><creatorcontrib>Goel, Atul</creatorcontrib><creatorcontrib>Chandran, Divya</creatorcontrib><title>Medicarpin confers powdery mildew resistance in Medicago truncatula and activates the salicylic acid signalling pathway</title><title>Molecular plant pathology</title><addtitle>Mol Plant Pathol</addtitle><description>Powdery mildew (PM) caused by the obligate biotrophic fungal pathogen Erysiphe pisi is an economically important disease of legumes. Legumes are rich in isoflavonoids, a class of secondary metabolites whose role in PM resistance is ambiguous. Here we show that the pterocarpan medicarpin accumulates at fungal infection sites, as analysed by fluorescein‐tagged medicarpin, and provides penetration and post‐penetration resistance against E. pisi in Medicago truncatula in part through the activation of the salicylic acid (SA) signalling pathway. Comparative gene expression and metabolite analyses revealed an early induction of isoflavonoid biosynthesis and accumulation of the defence phytohormones SA and jasmonic acid (JA) in the highly resistant M. truncatula genotype A17 but not in moderately susceptible R108 in response to PM infection. Pretreatment of R108 leaves with medicarpin increased SA levels, SA‐associated gene expression, and accumulation of hydrogen peroxide at PM infection sites, and reduced fungal penetration and colony formation. Strong parallels in the levels of medicarpin and SA, but not JA, were observed on medicarpin/SA treatment pre‐ or post‐PM infection. Collectively, our results suggest that medicarpin and SA may act in concert to restrict E. pisi growth, providing new insights into the metabolic and signalling pathways required for PM resistance in legumes.
Infection‐localized accumulation of the isoflavonoid phytoalexin medicarpin provides resistance against the pea powdery mildew pathogen and activates salicylic acid signalling in Medicago truncatula.</description><subject>Accumulation</subject><subject>Airborne microorganisms</subject><subject>Alfalfa</subject><subject>Biosynthesis</subject><subject>Economic importance</subject><subject>Flavonoids</subject><subject>Fluorescein</subject><subject>fluorescein‐tagged medicarpin</subject><subject>Fungi</subject><subject>Gene expression</subject><subject>Genomes</subject><subject>Genotypes</subject><subject>Hydrogen peroxide</subject><subject>Infections</subject><subject>isoflavone reductase</subject><subject>Isoflavonoids</subject><subject>Jasmonic acid</subject><subject>Legumes</subject><subject>Medicago truncatula</subject><subject>Metabolites</subject><subject>Original</subject><subject>Pathogens</subject><subject>Penetration</subject><subject>Penetration resistance</subject><subject>phytoalexin</subject><subject>Plant diseases</subject><subject>Plant hormones</subject><subject>Powdery mildew</subject><subject>Salicylic acid</subject><subject>Secondary metabolites</subject><subject>Signal 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truncatula and activates the salicylic acid signalling pathway</title><author>Gupta, Arunima ; Awasthi, Pallavi ; Sharma, Neha ; Parveen, Sajiya ; Vats, Ravi P. ; Singh, Nirpendra ; Kumar, Yashwant ; Goel, Atul ; Chandran, Divya</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4432-1a737fb423e3163dcd7c378b09a5ce4bcfd4ac3ce4623a5364f30d4c88901c833</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Accumulation</topic><topic>Airborne microorganisms</topic><topic>Alfalfa</topic><topic>Biosynthesis</topic><topic>Economic importance</topic><topic>Flavonoids</topic><topic>Fluorescein</topic><topic>fluorescein‐tagged medicarpin</topic><topic>Fungi</topic><topic>Gene expression</topic><topic>Genomes</topic><topic>Genotypes</topic><topic>Hydrogen peroxide</topic><topic>Infections</topic><topic>isoflavone reductase</topic><topic>Isoflavonoids</topic><topic>Jasmonic 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Pathol</addtitle><date>2022-07</date><risdate>2022</risdate><volume>23</volume><issue>7</issue><spage>966</spage><epage>983</epage><pages>966-983</pages><issn>1464-6722</issn><eissn>1364-3703</eissn><abstract>Powdery mildew (PM) caused by the obligate biotrophic fungal pathogen Erysiphe pisi is an economically important disease of legumes. Legumes are rich in isoflavonoids, a class of secondary metabolites whose role in PM resistance is ambiguous. Here we show that the pterocarpan medicarpin accumulates at fungal infection sites, as analysed by fluorescein‐tagged medicarpin, and provides penetration and post‐penetration resistance against E. pisi in Medicago truncatula in part through the activation of the salicylic acid (SA) signalling pathway. Comparative gene expression and metabolite analyses revealed an early induction of isoflavonoid biosynthesis and accumulation of the defence phytohormones SA and jasmonic acid (JA) in the highly resistant M. truncatula genotype A17 but not in moderately susceptible R108 in response to PM infection. Pretreatment of R108 leaves with medicarpin increased SA levels, SA‐associated gene expression, and accumulation of hydrogen peroxide at PM infection sites, and reduced fungal penetration and colony formation. Strong parallels in the levels of medicarpin and SA, but not JA, were observed on medicarpin/SA treatment pre‐ or post‐PM infection. Collectively, our results suggest that medicarpin and SA may act in concert to restrict E. pisi growth, providing new insights into the metabolic and signalling pathways required for PM resistance in legumes.
Infection‐localized accumulation of the isoflavonoid phytoalexin medicarpin provides resistance against the pea powdery mildew pathogen and activates salicylic acid signalling in Medicago truncatula.</abstract><cop>England</cop><pub>John Wiley & Sons, Inc</pub><pmid>35263504</pmid><doi>10.1111/mpp.13202</doi><tpages>18</tpages><orcidid>https://orcid.org/0000-0003-2758-2461</orcidid><orcidid>https://orcid.org/0000-0001-6206-8826</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Accumulation Airborne microorganisms Alfalfa Biosynthesis Economic importance Flavonoids Fluorescein fluorescein‐tagged medicarpin Fungi Gene expression Genomes Genotypes Hydrogen peroxide Infections isoflavone reductase Isoflavonoids Jasmonic acid Legumes Medicago truncatula Metabolites Original Pathogens Penetration Penetration resistance phytoalexin Plant diseases Plant hormones Powdery mildew Salicylic acid Secondary metabolites Signal transduction Signaling |
title | Medicarpin confers powdery mildew resistance in Medicago truncatula and activates the salicylic acid signalling pathway |
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