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Immunity-associated volatile emissions of β-ionone and nonanal propagate defence responses in neighbouring barley plants
Infected barley plants send airborne cues that are recognized as defence signals in conspecific neighbours. β-Ionone and nonanal from the volatile blend of infected barley contribute to defence priming. Abstract Plants activate biochemical responses to combat stress. (Hemi-)biotrophic pathogens are...
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Published in: | Journal of experimental botany 2022-01, Vol.73 (2), p.615-630 |
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description | Infected barley plants send airborne cues that are recognized as defence signals in conspecific neighbours. β-Ionone and nonanal from the volatile blend of infected barley contribute to defence priming.
Abstract
Plants activate biochemical responses to combat stress. (Hemi-)biotrophic pathogens are fended off by systemic acquired resistance (SAR), a primed state allowing plants to respond faster and more strongly upon subsequent infection. Here, we show that SAR-like defences in barley (Hordeum vulgare) are propagated between neighbouring plants, which respond with enhanced resistance to the volatile cues from infected senders. The emissions of the sender plants contained 15 volatile organic compounds (VOCs) associated with infection. Two of these, β-ionone and nonanal, elicited resistance upon plant exposure. Whole-genome transcriptomics analysis confirmed that interplant propagation of defence in barley is established as a form of priming. Although gene expression changes were more pronounced after challenge infection of the receiver plants with Blumeria graminis f. sp. hordei, differential gene expression in response to the volatile cues of the sender plants included an induction of HISTONE DEACETYLASE 2 (HvHDA2) and priming of TETRATRICOPEPTIDE REPEAT-LIKE superfamily protein (HvTPL). Because HvHDA2 and HvTPL transcript accumulation was also enhanced by exposure of barley to β-ionone and nonanal, our data identify both genes as possible defence/priming markers in barley. Our results suggest that VOCs and plant–plant interactions are relevant for possible crop protection strategies priming defence responses in barley. |
doi_str_mv | 10.1093/jxb/erab520 |
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Abstract
Plants activate biochemical responses to combat stress. (Hemi-)biotrophic pathogens are fended off by systemic acquired resistance (SAR), a primed state allowing plants to respond faster and more strongly upon subsequent infection. Here, we show that SAR-like defences in barley (Hordeum vulgare) are propagated between neighbouring plants, which respond with enhanced resistance to the volatile cues from infected senders. The emissions of the sender plants contained 15 volatile organic compounds (VOCs) associated with infection. Two of these, β-ionone and nonanal, elicited resistance upon plant exposure. Whole-genome transcriptomics analysis confirmed that interplant propagation of defence in barley is established as a form of priming. Although gene expression changes were more pronounced after challenge infection of the receiver plants with Blumeria graminis f. sp. hordei, differential gene expression in response to the volatile cues of the sender plants included an induction of HISTONE DEACETYLASE 2 (HvHDA2) and priming of TETRATRICOPEPTIDE REPEAT-LIKE superfamily protein (HvTPL). Because HvHDA2 and HvTPL transcript accumulation was also enhanced by exposure of barley to β-ionone and nonanal, our data identify both genes as possible defence/priming markers in barley. Our results suggest that VOCs and plant–plant interactions are relevant for possible crop protection strategies priming defence responses in barley.</description><identifier>ISSN: 0022-0957</identifier><identifier>EISSN: 1460-2431</identifier><identifier>DOI: 10.1093/jxb/erab520</identifier><identifier>PMID: 34849759</identifier><language>eng</language><publisher>UK: Oxford University Press</publisher><subject>Aldehydes ; Hordeum - genetics ; Norisoprenoids ; Plant Diseases ; Plant Proteins - genetics ; Plants</subject><ispartof>Journal of experimental botany, 2022-01, Vol.73 (2), p.615-630</ispartof><rights>The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved. For permissions, please email: journals.permissions@oup.com 2021</rights><rights>The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved. For permissions, please email: journals.permissions@oup.com.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c357t-317111f7bf8c0f6dcfee948a9afe109a1b62aeb3775f66ccae3bcb5d0e206f193</citedby><cites>FETCH-LOGICAL-c357t-317111f7bf8c0f6dcfee948a9afe109a1b62aeb3775f66ccae3bcb5d0e206f193</cites><orcidid>0000-0002-1389-2939 ; 0000-0003-1973-4007 ; 0000-0002-8146-6018 ; 0000-0002-9825-867X ; 0000-0002-7228-1177 ; 0000-0003-1179-4056</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/34849759$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Monaghan, Jacqueline</contributor><creatorcontrib>Brambilla, Alessandro</creatorcontrib><creatorcontrib>Sommer, Anna</creatorcontrib><creatorcontrib>Ghirardo, Andrea</creatorcontrib><creatorcontrib>Wenig, Marion</creatorcontrib><creatorcontrib>Knappe, Claudia</creatorcontrib><creatorcontrib>Weber, Baris</creatorcontrib><creatorcontrib>Amesmaier, Melissa</creatorcontrib><creatorcontrib>Lenk, Miriam</creatorcontrib><creatorcontrib>Schnitzler, Jörg-Peter</creatorcontrib><creatorcontrib>Vlot, A Corina</creatorcontrib><title>Immunity-associated volatile emissions of β-ionone and nonanal propagate defence responses in neighbouring barley plants</title><title>Journal of experimental botany</title><addtitle>J Exp Bot</addtitle><description>Infected barley plants send airborne cues that are recognized as defence signals in conspecific neighbours. β-Ionone and nonanal from the volatile blend of infected barley contribute to defence priming.
Abstract
Plants activate biochemical responses to combat stress. (Hemi-)biotrophic pathogens are fended off by systemic acquired resistance (SAR), a primed state allowing plants to respond faster and more strongly upon subsequent infection. Here, we show that SAR-like defences in barley (Hordeum vulgare) are propagated between neighbouring plants, which respond with enhanced resistance to the volatile cues from infected senders. The emissions of the sender plants contained 15 volatile organic compounds (VOCs) associated with infection. Two of these, β-ionone and nonanal, elicited resistance upon plant exposure. Whole-genome transcriptomics analysis confirmed that interplant propagation of defence in barley is established as a form of priming. Although gene expression changes were more pronounced after challenge infection of the receiver plants with Blumeria graminis f. sp. hordei, differential gene expression in response to the volatile cues of the sender plants included an induction of HISTONE DEACETYLASE 2 (HvHDA2) and priming of TETRATRICOPEPTIDE REPEAT-LIKE superfamily protein (HvTPL). Because HvHDA2 and HvTPL transcript accumulation was also enhanced by exposure of barley to β-ionone and nonanal, our data identify both genes as possible defence/priming markers in barley. Our results suggest that VOCs and plant–plant interactions are relevant for possible crop protection strategies priming defence responses in barley.</description><subject>Aldehydes</subject><subject>Hordeum - genetics</subject><subject>Norisoprenoids</subject><subject>Plant Diseases</subject><subject>Plant Proteins - genetics</subject><subject>Plants</subject><issn>0022-0957</issn><issn>1460-2431</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><recordid>eNp9kL1u3DAQhAkjgX3-qdIHrAIDhuIlJUqn0jDiH8BAmqQWltTyTEMiZVIycq-VB8kzhcadXbraKb4ZzA5jXwR8F9CWl09_9CVF1ErCAVuJqoZCVqX4xFYAUhbQquaIHaf0BAAKlDpkR2W1rtpGtSu2vR_Hxbt5W2BKwTicqecvYcDZDcRpdCm54BMPlv_7W2QZPHH0Pc8CPQ58imHCTbbxnix5QzxSmrKFEneee3KbRx2W6PyGa4wDbfk0oJ_TKftscUh0tr8n7PfNj1_Xd8XDz9v766uHwpSqmYtSNEII22i7NmDr3liitlpji5by-yh0LZF02TTK1rUxSKU2WvVAEmor2vKEne9yc9PnhdLc5acMDbkEhSV1sgYlZVNJyOjFDjUxpBTJdlN0I8ZtJ6B73brLW3f7rTP9dR-86JH6d_Zt3Ax82wFhmT5M-g_3Ooz-</recordid><startdate>20220113</startdate><enddate>20220113</enddate><creator>Brambilla, Alessandro</creator><creator>Sommer, Anna</creator><creator>Ghirardo, Andrea</creator><creator>Wenig, Marion</creator><creator>Knappe, Claudia</creator><creator>Weber, Baris</creator><creator>Amesmaier, Melissa</creator><creator>Lenk, Miriam</creator><creator>Schnitzler, Jörg-Peter</creator><creator>Vlot, A Corina</creator><general>Oxford University Press</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/0000-0002-1389-2939</orcidid><orcidid>https://orcid.org/0000-0003-1973-4007</orcidid><orcidid>https://orcid.org/0000-0002-8146-6018</orcidid><orcidid>https://orcid.org/0000-0002-9825-867X</orcidid><orcidid>https://orcid.org/0000-0002-7228-1177</orcidid><orcidid>https://orcid.org/0000-0003-1179-4056</orcidid></search><sort><creationdate>20220113</creationdate><title>Immunity-associated volatile emissions of β-ionone and nonanal propagate defence responses in neighbouring barley plants</title><author>Brambilla, Alessandro ; Sommer, Anna ; Ghirardo, Andrea ; Wenig, Marion ; Knappe, Claudia ; Weber, Baris ; Amesmaier, Melissa ; Lenk, Miriam ; Schnitzler, Jörg-Peter ; Vlot, A Corina</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c357t-317111f7bf8c0f6dcfee948a9afe109a1b62aeb3775f66ccae3bcb5d0e206f193</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Aldehydes</topic><topic>Hordeum - genetics</topic><topic>Norisoprenoids</topic><topic>Plant Diseases</topic><topic>Plant Proteins - genetics</topic><topic>Plants</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Brambilla, Alessandro</creatorcontrib><creatorcontrib>Sommer, Anna</creatorcontrib><creatorcontrib>Ghirardo, Andrea</creatorcontrib><creatorcontrib>Wenig, Marion</creatorcontrib><creatorcontrib>Knappe, Claudia</creatorcontrib><creatorcontrib>Weber, Baris</creatorcontrib><creatorcontrib>Amesmaier, Melissa</creatorcontrib><creatorcontrib>Lenk, Miriam</creatorcontrib><creatorcontrib>Schnitzler, Jörg-Peter</creatorcontrib><creatorcontrib>Vlot, A Corina</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>Journal of experimental botany</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Brambilla, Alessandro</au><au>Sommer, Anna</au><au>Ghirardo, Andrea</au><au>Wenig, Marion</au><au>Knappe, Claudia</au><au>Weber, Baris</au><au>Amesmaier, Melissa</au><au>Lenk, Miriam</au><au>Schnitzler, Jörg-Peter</au><au>Vlot, A Corina</au><au>Monaghan, Jacqueline</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Immunity-associated volatile emissions of β-ionone and nonanal propagate defence responses in neighbouring barley plants</atitle><jtitle>Journal of experimental botany</jtitle><addtitle>J Exp Bot</addtitle><date>2022-01-13</date><risdate>2022</risdate><volume>73</volume><issue>2</issue><spage>615</spage><epage>630</epage><pages>615-630</pages><issn>0022-0957</issn><eissn>1460-2431</eissn><abstract>Infected barley plants send airborne cues that are recognized as defence signals in conspecific neighbours. β-Ionone and nonanal from the volatile blend of infected barley contribute to defence priming.
Abstract
Plants activate biochemical responses to combat stress. (Hemi-)biotrophic pathogens are fended off by systemic acquired resistance (SAR), a primed state allowing plants to respond faster and more strongly upon subsequent infection. Here, we show that SAR-like defences in barley (Hordeum vulgare) are propagated between neighbouring plants, which respond with enhanced resistance to the volatile cues from infected senders. The emissions of the sender plants contained 15 volatile organic compounds (VOCs) associated with infection. Two of these, β-ionone and nonanal, elicited resistance upon plant exposure. Whole-genome transcriptomics analysis confirmed that interplant propagation of defence in barley is established as a form of priming. Although gene expression changes were more pronounced after challenge infection of the receiver plants with Blumeria graminis f. sp. hordei, differential gene expression in response to the volatile cues of the sender plants included an induction of HISTONE DEACETYLASE 2 (HvHDA2) and priming of TETRATRICOPEPTIDE REPEAT-LIKE superfamily protein (HvTPL). Because HvHDA2 and HvTPL transcript accumulation was also enhanced by exposure of barley to β-ionone and nonanal, our data identify both genes as possible defence/priming markers in barley. Our results suggest that VOCs and plant–plant interactions are relevant for possible crop protection strategies priming defence responses in barley.</abstract><cop>UK</cop><pub>Oxford University Press</pub><pmid>34849759</pmid><doi>10.1093/jxb/erab520</doi><tpages>16</tpages><orcidid>https://orcid.org/0000-0002-1389-2939</orcidid><orcidid>https://orcid.org/0000-0003-1973-4007</orcidid><orcidid>https://orcid.org/0000-0002-8146-6018</orcidid><orcidid>https://orcid.org/0000-0002-9825-867X</orcidid><orcidid>https://orcid.org/0000-0002-7228-1177</orcidid><orcidid>https://orcid.org/0000-0003-1179-4056</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Aldehydes Hordeum - genetics Norisoprenoids Plant Diseases Plant Proteins - genetics Plants |
title | Immunity-associated volatile emissions of β-ionone and nonanal propagate defence responses in neighbouring barley plants |
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