Signatures of plant defense response specificity mediated by herbivore‐associated molecular patterns in legumes

SUMMARY Chewing herbivores activate plant defense responses through a combination of mechanical wounding and elicitation by herbivore‐associated molecular patterns (HAMPs). HAMPs are wound response amplifiers; however, specific defense outputs may also exist that strictly require HAMP‐mediated defen...

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Veröffentlicht in:The Plant journal : for cell and molecular biology 2022-06, Vol.110 (5), p.1255-1270
Hauptverfasser: Steinbrenner, Adam D., Saldivar, Evan, Hodges, Nile, Guayazán‐Palacios, Natalia, Chaparro, Antonio F., Schmelz, Eric A.
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container_title The Plant journal : for cell and molecular biology
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creator Steinbrenner, Adam D.
Saldivar, Evan
Hodges, Nile
Guayazán‐Palacios, Natalia
Chaparro, Antonio F.
Schmelz, Eric A.
description SUMMARY Chewing herbivores activate plant defense responses through a combination of mechanical wounding and elicitation by herbivore‐associated molecular patterns (HAMPs). HAMPs are wound response amplifiers; however, specific defense outputs may also exist that strictly require HAMP‐mediated defense signaling. To investigate HAMP‐mediated signaling and defense responses, we characterized cowpea (Vigna unguiculata) transcriptome changes following elicitation by inceptin, a peptide HAMP common in Lepidoptera larvae oral secretions. Following inceptin treatment, we observed large‐scale reprogramming of the transcriptome consistent with three different response categories: (i) amplification of mechanical wound responses, (ii) temporal extension through accelerated or prolonged responses, and (iii) examples of inceptin‐specific elicitation and suppression. At both early and late timepoints, namely 1 and 6 h, large sets of transcripts specifically accumulated following inceptin elicitation. Further early inceptin‐regulated transcripts were classified as reversing changes induced by wounding alone. Within key signaling‐ and defense‐related gene families, inceptin‐elicited responses included target subsets of wound‐induced transcripts. Transcripts displaying the largest inceptin‐elicited fold changes included transcripts encoding terpene synthases (TPSs) and peroxidases (POXs) that correspond with induced volatile production and increased POX activity in cowpea. Characterization of inceptin‐elicited cowpea defenses via heterologous expression in Nicotiana benthamiana demonstrated that specific cowpea TPSs and POXs were able to confer terpene emission and the reduced growth of beet armyworm (Spodoptera exigua) herbivores, respectively. Collectively, our present findings in cowpea support a model where HAMP elicitation both amplifies concurrent wound responses and specifically contributes to the activation of selective outputs associated with direct and indirect antiherbivore defenses. Significance Statement Plants recognize herbivore‐associated molecular patterns (HAMPs) and increase defense production, but interactions with the more general wound response are not well understood. We examined an established HAMP–receptor interaction to characterize the transcriptomic modulation of wound responses by the HAMP peptide inceptin. Inceptin not only amplifies wound responses, but can also specifically induce or suppress transcripts with demonstrated functions in direct
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HAMPs are wound response amplifiers; however, specific defense outputs may also exist that strictly require HAMP‐mediated defense signaling. To investigate HAMP‐mediated signaling and defense responses, we characterized cowpea (Vigna unguiculata) transcriptome changes following elicitation by inceptin, a peptide HAMP common in Lepidoptera larvae oral secretions. Following inceptin treatment, we observed large‐scale reprogramming of the transcriptome consistent with three different response categories: (i) amplification of mechanical wound responses, (ii) temporal extension through accelerated or prolonged responses, and (iii) examples of inceptin‐specific elicitation and suppression. At both early and late timepoints, namely 1 and 6 h, large sets of transcripts specifically accumulated following inceptin elicitation. Further early inceptin‐regulated transcripts were classified as reversing changes induced by wounding alone. Within key signaling‐ and defense‐related gene families, inceptin‐elicited responses included target subsets of wound‐induced transcripts. Transcripts displaying the largest inceptin‐elicited fold changes included transcripts encoding terpene synthases (TPSs) and peroxidases (POXs) that correspond with induced volatile production and increased POX activity in cowpea. Characterization of inceptin‐elicited cowpea defenses via heterologous expression in Nicotiana benthamiana demonstrated that specific cowpea TPSs and POXs were able to confer terpene emission and the reduced growth of beet armyworm (Spodoptera exigua) herbivores, respectively. Collectively, our present findings in cowpea support a model where HAMP elicitation both amplifies concurrent wound responses and specifically contributes to the activation of selective outputs associated with direct and indirect antiherbivore defenses. Significance Statement Plants recognize herbivore‐associated molecular patterns (HAMPs) and increase defense production, but interactions with the more general wound response are not well understood. We examined an established HAMP–receptor interaction to characterize the transcriptomic modulation of wound responses by the HAMP peptide inceptin. Inceptin not only amplifies wound responses, but can also specifically induce or suppress transcripts with demonstrated functions in direct and indirect defense against herbivores. 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HAMPs are wound response amplifiers; however, specific defense outputs may also exist that strictly require HAMP‐mediated defense signaling. To investigate HAMP‐mediated signaling and defense responses, we characterized cowpea (Vigna unguiculata) transcriptome changes following elicitation by inceptin, a peptide HAMP common in Lepidoptera larvae oral secretions. Following inceptin treatment, we observed large‐scale reprogramming of the transcriptome consistent with three different response categories: (i) amplification of mechanical wound responses, (ii) temporal extension through accelerated or prolonged responses, and (iii) examples of inceptin‐specific elicitation and suppression. At both early and late timepoints, namely 1 and 6 h, large sets of transcripts specifically accumulated following inceptin elicitation. Further early inceptin‐regulated transcripts were classified as reversing changes induced by wounding alone. Within key signaling‐ and defense‐related gene families, inceptin‐elicited responses included target subsets of wound‐induced transcripts. Transcripts displaying the largest inceptin‐elicited fold changes included transcripts encoding terpene synthases (TPSs) and peroxidases (POXs) that correspond with induced volatile production and increased POX activity in cowpea. Characterization of inceptin‐elicited cowpea defenses via heterologous expression in Nicotiana benthamiana demonstrated that specific cowpea TPSs and POXs were able to confer terpene emission and the reduced growth of beet armyworm (Spodoptera exigua) herbivores, respectively. Collectively, our present findings in cowpea support a model where HAMP elicitation both amplifies concurrent wound responses and specifically contributes to the activation of selective outputs associated with direct and indirect antiherbivore defenses. 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HAMPs are wound response amplifiers; however, specific defense outputs may also exist that strictly require HAMP‐mediated defense signaling. To investigate HAMP‐mediated signaling and defense responses, we characterized cowpea (Vigna unguiculata) transcriptome changes following elicitation by inceptin, a peptide HAMP common in Lepidoptera larvae oral secretions. Following inceptin treatment, we observed large‐scale reprogramming of the transcriptome consistent with three different response categories: (i) amplification of mechanical wound responses, (ii) temporal extension through accelerated or prolonged responses, and (iii) examples of inceptin‐specific elicitation and suppression. At both early and late timepoints, namely 1 and 6 h, large sets of transcripts specifically accumulated following inceptin elicitation. Further early inceptin‐regulated transcripts were classified as reversing changes induced by wounding alone. Within key signaling‐ and defense‐related gene families, inceptin‐elicited responses included target subsets of wound‐induced transcripts. Transcripts displaying the largest inceptin‐elicited fold changes included transcripts encoding terpene synthases (TPSs) and peroxidases (POXs) that correspond with induced volatile production and increased POX activity in cowpea. Characterization of inceptin‐elicited cowpea defenses via heterologous expression in Nicotiana benthamiana demonstrated that specific cowpea TPSs and POXs were able to confer terpene emission and the reduced growth of beet armyworm (Spodoptera exigua) herbivores, respectively. Collectively, our present findings in cowpea support a model where HAMP elicitation both amplifies concurrent wound responses and specifically contributes to the activation of selective outputs associated with direct and indirect antiherbivore defenses. Significance Statement Plants recognize herbivore‐associated molecular patterns (HAMPs) and increase defense production, but interactions with the more general wound response are not well understood. We examined an established HAMP–receptor interaction to characterize the transcriptomic modulation of wound responses by the HAMP peptide inceptin. Inceptin not only amplifies wound responses, but can also specifically induce or suppress transcripts with demonstrated functions in direct and indirect defense against herbivores. The plant immune system thus recognizes HAMPs to fine‐tune wound responses against insect herbivores.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>35315556</pmid><doi>10.1111/tpj.15732</doi><tpages>1270</tpages><orcidid>https://orcid.org/0000-0002-2837-734X</orcidid><orcidid>https://orcid.org/0000-0002-7493-678X</orcidid><oa>free_for_read</oa></addata></record>
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subjects Animals
cowpea
Cowpeas
Defense mechanisms
Emissions control
Fabaceae - genetics
Gene Expression Regulation, Plant
Gene families
HAMP
Herbivores
Herbivory - physiology
inceptin
INR
Larvae
Legumes
peroxidase
Plants
Secretions
Signaling
Spodoptera
Spodoptera exigua
terpene
Terpenes - metabolism
Transcriptomes
Vigna - genetics
Vigna unguiculata
Wounding
title Signatures of plant defense response specificity mediated by herbivore‐associated molecular patterns in legumes
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