Necrosis and ethylene-inducing-like peptide patterns from crop pathogens induce differential responses within seven brassicaceous species

Henk jan Schoonbeek; Hicret Asli Yalcin; Rachel Burns; Rachel Emma Taylor; Adam Casey; Sam Holt; Guido Van den Ackerveken; Rachel Wells; Christopher J. Ridout

doi:10.1111/ppa.13615

Necrosis and ethylene-inducing-like peptide patterns from crop pathogens induce differential responses within seven brassicaceous species

Henk jan Schoonbeek, Hicret Asli Yalcin, Rachel Burns, Rachel Emma Taylor, Adam Casey, Sam Holt, Guido Van den Ackerveken, Rachel Wells, Christopher J. Ridout^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › Academic › peer-review

Abstract

Translational research is required to advance fundamental knowledge on plant immunity towards application in crop improvement. Recognition of microbe/pathogen-associated molecular patterns (MAMPs/PAMPs) triggers a first layer of immunity in plants. The broadly occurring family of necrosis- and ethylene-inducing peptide 1 (NEP1)-like proteins (NLPs) contains immunogenic peptide patterns that are recognized by a number of plant species. Arabidopsis can recognize NLPs by the pattern recognition receptor AtRLP23 and its co-receptors SOBIR1, BAK1, and BKK1, leading to induction of defence responses including the production of reactive oxygen species (ROS) and elevation of intracellular [Ca²⁺]. However, little is known about NLP perception in Brassica crop species. Within 12 diverse accessions for each of six Brassica crop species, we demonstrate variation in response to Botrytis cinerea NLP BcNEP2, with Brassica oleracea (CC genome) being nonresponsive and only two Brassica napus cultivars responding to BcNEP2. Peptides derived from four fungal pathogens of these crop species elicited responses similar to BcNEP2 in B. napus and Arabidopsis. Induction of ROS by NLP peptides was strongly reduced in Atrlp23, Atsobir1 and Atbak1-5 Atbkk1-1 mutants, confirming that recognition of Brassica pathogen NLPs occurs in a similar manner to that of HaNLP3 from Hyaloperonospora arabidopsidis in Arabidopsis. In silico analysis of the genomes of two B. napus accessions showed similar presence of homologues for AtBAK1, AtBKK1 and AtSOBIR1 but variation in the organization of AtRLP23 homologues. We could not detect a strong correlation between the ability to respond to NLP peptides and resistance to B. cinerea.

Original language	English
Pages (from-to)	2004-2016
Number of pages	13
Journal	Plant Pathology
Volume	71
Issue number	9
DOIs	https://doi.org/10.1111/ppa.13615
Publication status	Published - Dec 2022

Bibliographical note

Funding Information:
This work was funded by the Biotechnology and Biological Sciences Research Council (BBSRC) grants BB/N005007/1 (as part of the ERA-CAPS consortium ‘MAQBAT’), the John Innes Institute strategic programme grants Plant Health BB/P012574/1 (Response BBS/E/J/000PR9796) and Molecules from Nature BB/PO12523/1, Brassica Rapeseed and Vegetable Optimisation (BRAVO) BB/P003095/1. H.A.Y. received a scholarship from The Newton-Katip Celebi Fund given by British Council and The Scientific and Technological Research Council of Turkey (TUBITAK). G.V.d.A. acknowledges support from the Netherlands Organization of Scientific Research (NWO). We are grateful to Francesca Stefanato (JIC), Georgia Mitrousia, Henrik Stotz (University of Hertfordshire) and Tom Raaymakers (UU) for helpful discussions and providing stocks of previously described NLPs, Kathryn O'Connor (JIC) for help with B. cinerea expression studies, and Catherine Chinoy and James Canham for assistance in the sobir1 mutant analysis.

Funding Information:
This work was funded by the Biotechnology and Biological Sciences Research Council (BBSRC) grants BB/N005007/1 (as part of the ERA‐CAPS consortium ‘MAQBAT’), the John Innes Institute strategic programme grants Plant Health BB/P012574/1 (Response BBS/E/J/000PR9796) and Molecules from Nature BB/PO12523/1, Brassica Rapeseed and Vegetable Optimisation (BRAVO) BB/P003095/1. H.A.Y. received a scholarship from The Newton‐Katip Celebi Fund given by British Council and The Scientific and Technological Research Council of Turkey (TUBITAK). G.V.d.A. acknowledges support from the Netherlands Organization of Scientific Research (NWO). We are grateful to Francesca Stefanato (JIC), Georgia Mitrousia, Henrik Stotz (University of Hertfordshire) and Tom Raaymakers (UU) for helpful discussions and providing stocks of previously described NLPs, Kathryn O'Connor (JIC) for help with . expression studies, and Catherine Chinoy and James Canham for assistance in the mutant analysis. B cinerea sobir1

Publisher Copyright:
© 2022 The Authors. Plant Pathology published by John Wiley & Sons Ltd on behalf of British Society for Plant Pathology.

Funding

This work was funded by the Biotechnology and Biological Sciences Research Council (BBSRC) grants BB/N005007/1 (as part of the ERA-CAPS consortium ‘MAQBAT’), the John Innes Institute strategic programme grants Plant Health BB/P012574/1 (Response BBS/E/J/000PR9796) and Molecules from Nature BB/PO12523/1, Brassica Rapeseed and Vegetable Optimisation (BRAVO) BB/P003095/1. H.A.Y. received a scholarship from The Newton-Katip Celebi Fund given by British Council and The Scientific and Technological Research Council of Turkey (TUBITAK). G.V.d.A. acknowledges support from the Netherlands Organization of Scientific Research (NWO). We are grateful to Francesca Stefanato (JIC), Georgia Mitrousia, Henrik Stotz (University of Hertfordshire) and Tom Raaymakers (UU) for helpful discussions and providing stocks of previously described NLPs, Kathryn O'Connor (JIC) for help with B. cinerea expression studies, and Catherine Chinoy and James Canham for assistance in the sobir1 mutant analysis. This work was funded by the Biotechnology and Biological Sciences Research Council (BBSRC) grants BB/N005007/1 (as part of the ERA‐CAPS consortium ‘MAQBAT’), the John Innes Institute strategic programme grants Plant Health BB/P012574/1 (Response BBS/E/J/000PR9796) and Molecules from Nature BB/PO12523/1, Brassica Rapeseed and Vegetable Optimisation (BRAVO) BB/P003095/1. H.A.Y. received a scholarship from The Newton‐Katip Celebi Fund given by British Council and The Scientific and Technological Research Council of Turkey (TUBITAK). G.V.d.A. acknowledges support from the Netherlands Organization of Scientific Research (NWO). We are grateful to Francesca Stefanato (JIC), Georgia Mitrousia, Henrik Stotz (University of Hertfordshire) and Tom Raaymakers (UU) for helpful discussions and providing stocks of previously described NLPs, Kathryn O'Connor (JIC) for help with . expression studies, and Catherine Chinoy and James Canham for assistance in the mutant analysis. B cinerea sobir1

Keywords

brassica
grey mould
microbe/pathogen-associated molecular pattern
necrosis and ethylene-inducing peptide 1-like proteins

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Plant Pathology - 2022 - Schoonbeek - Necrosis and ethylene‐inducing‐like peptide patterns from crop pathogens induceFinal published version, 1.57 MBLicence: CC BY

Cite this

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title = "Necrosis and ethylene-inducing-like peptide patterns from crop pathogens induce differential responses within seven brassicaceous species",

abstract = "Translational research is required to advance fundamental knowledge on plant immunity towards application in crop improvement. Recognition of microbe/pathogen-associated molecular patterns (MAMPs/PAMPs) triggers a first layer of immunity in plants. The broadly occurring family of necrosis- and ethylene-inducing peptide 1 (NEP1)-like proteins (NLPs) contains immunogenic peptide patterns that are recognized by a number of plant species. Arabidopsis can recognize NLPs by the pattern recognition receptor AtRLP23 and its co-receptors SOBIR1, BAK1, and BKK1, leading to induction of defence responses including the production of reactive oxygen species (ROS) and elevation of intracellular [Ca2+]. However, little is known about NLP perception in Brassica crop species. Within 12 diverse accessions for each of six Brassica crop species, we demonstrate variation in response to Botrytis cinerea NLP BcNEP2, with Brassica oleracea (CC genome) being nonresponsive and only two Brassica napus cultivars responding to BcNEP2. Peptides derived from four fungal pathogens of these crop species elicited responses similar to BcNEP2 in B. napus and Arabidopsis. Induction of ROS by NLP peptides was strongly reduced in Atrlp23, Atsobir1 and Atbak1-5 Atbkk1-1 mutants, confirming that recognition of Brassica pathogen NLPs occurs in a similar manner to that of HaNLP3 from Hyaloperonospora arabidopsidis in Arabidopsis. In silico analysis of the genomes of two B. napus accessions showed similar presence of homologues for AtBAK1, AtBKK1 and AtSOBIR1 but variation in the organization of AtRLP23 homologues. We could not detect a strong correlation between the ability to respond to NLP peptides and resistance to B. cinerea.",

keywords = "brassica, grey mould, microbe/pathogen-associated molecular pattern, necrosis and ethylene-inducing peptide 1-like proteins",

author = "Schoonbeek, {Henk jan} and Yalcin, {Hicret Asli} and Rachel Burns and Taylor, {Rachel Emma} and Adam Casey and Sam Holt and {Van den Ackerveken}, Guido and Rachel Wells and Ridout, {Christopher J.}",

note = "Funding Information: This work was funded by the Biotechnology and Biological Sciences Research Council (BBSRC) grants BB/N005007/1 (as part of the ERA-CAPS consortium {\textquoteleft}MAQBAT{\textquoteright}), the John Innes Institute strategic programme grants Plant Health BB/P012574/1 (Response BBS/E/J/000PR9796) and Molecules from Nature BB/PO12523/1, Brassica Rapeseed and Vegetable Optimisation (BRAVO) BB/P003095/1. H.A.Y. received a scholarship from The Newton-Katip Celebi Fund given by British Council and The Scientific and Technological Research Council of Turkey (TUBITAK). G.V.d.A. acknowledges support from the Netherlands Organization of Scientific Research (NWO). We are grateful to Francesca Stefanato (JIC), Georgia Mitrousia, Henrik Stotz (University of Hertfordshire) and Tom Raaymakers (UU) for helpful discussions and providing stocks of previously described NLPs, Kathryn O'Connor (JIC) for help with B. cinerea expression studies, and Catherine Chinoy and James Canham for assistance in the sobir1 mutant analysis. Funding Information: This work was funded by the Biotechnology and Biological Sciences Research Council (BBSRC) grants BB/N005007/1 (as part of the ERA‐CAPS consortium {\textquoteleft}MAQBAT{\textquoteright}), the John Innes Institute strategic programme grants Plant Health BB/P012574/1 (Response BBS/E/J/000PR9796) and Molecules from Nature BB/PO12523/1, Brassica Rapeseed and Vegetable Optimisation (BRAVO) BB/P003095/1. H.A.Y. received a scholarship from The Newton‐Katip Celebi Fund given by British Council and The Scientific and Technological Research Council of Turkey (TUBITAK). G.V.d.A. acknowledges support from the Netherlands Organization of Scientific Research (NWO). We are grateful to Francesca Stefanato (JIC), Georgia Mitrousia, Henrik Stotz (University of Hertfordshire) and Tom Raaymakers (UU) for helpful discussions and providing stocks of previously described NLPs, Kathryn O'Connor (JIC) for help with . expression studies, and Catherine Chinoy and James Canham for assistance in the mutant analysis. B cinerea sobir1 Publisher Copyright: {\textcopyright} 2022 The Authors. Plant Pathology published by John Wiley & Sons Ltd on behalf of British Society for Plant Pathology.",

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doi = "10.1111/ppa.13615",

language = "English",

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AU - Taylor, Rachel Emma

AU - Casey, Adam

AU - Holt, Sam

AU - Van den Ackerveken, Guido

AU - Wells, Rachel

AU - Ridout, Christopher J.

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N2 - Translational research is required to advance fundamental knowledge on plant immunity towards application in crop improvement. Recognition of microbe/pathogen-associated molecular patterns (MAMPs/PAMPs) triggers a first layer of immunity in plants. The broadly occurring family of necrosis- and ethylene-inducing peptide 1 (NEP1)-like proteins (NLPs) contains immunogenic peptide patterns that are recognized by a number of plant species. Arabidopsis can recognize NLPs by the pattern recognition receptor AtRLP23 and its co-receptors SOBIR1, BAK1, and BKK1, leading to induction of defence responses including the production of reactive oxygen species (ROS) and elevation of intracellular [Ca2+]. However, little is known about NLP perception in Brassica crop species. Within 12 diverse accessions for each of six Brassica crop species, we demonstrate variation in response to Botrytis cinerea NLP BcNEP2, with Brassica oleracea (CC genome) being nonresponsive and only two Brassica napus cultivars responding to BcNEP2. Peptides derived from four fungal pathogens of these crop species elicited responses similar to BcNEP2 in B. napus and Arabidopsis. Induction of ROS by NLP peptides was strongly reduced in Atrlp23, Atsobir1 and Atbak1-5 Atbkk1-1 mutants, confirming that recognition of Brassica pathogen NLPs occurs in a similar manner to that of HaNLP3 from Hyaloperonospora arabidopsidis in Arabidopsis. In silico analysis of the genomes of two B. napus accessions showed similar presence of homologues for AtBAK1, AtBKK1 and AtSOBIR1 but variation in the organization of AtRLP23 homologues. We could not detect a strong correlation between the ability to respond to NLP peptides and resistance to B. cinerea.

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ER -

Necrosis and ethylene-inducing-like peptide patterns from crop pathogens induce differential responses within seven brassicaceous species

Abstract

Bibliographical note

Funding

Keywords

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