Pattern-recognition receptors are required for NLR-mediated plant immunity
The plant immune system is fundamental for plant survival in natural ecosystems and for productivity in crop fields. Substantial evidence supports the prevailing notion that plants possess a two-tiered innate immune system, called pattern-triggered immunity (PTI) and effector-triggered immunity (ETI...
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Veröffentlicht in: | Nature (London) 2021-04, Vol.592 (7852), p.105-109 |
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description | The plant immune system is fundamental for plant survival in natural ecosystems and for productivity in crop fields. Substantial evidence supports the prevailing notion that plants possess a two-tiered innate immune system, called pattern-triggered immunity (PTI) and effector-triggered immunity (ETI). PTI is triggered by microbial patterns via cell surface-localized pattern-recognition receptors (PRRs), whereas ETI is activated by pathogen effector proteins via predominantly intracellularly localized receptors called nucleotide-binding, leucine-rich repeat receptors (NLRs)
1
–
4
. PTI and ETI are initiated by distinct activation mechanisms and involve different early signalling cascades
5
,
6
. Here we show that
Arabidopsis
PRR and PRR co-receptor mutants—
fls2 efr cerk1
and
bak1 bkk1 cerk1
triple mutants—are markedly impaired in ETI responses when challenged with incompatible
Pseudomonas syrinage
bacteria. We further show that the production of reactive oxygen species by the NADPH oxidase RBOHD is a critical early signalling event connecting PRR- and NLR-mediated immunity, and that the receptor-like cytoplasmic kinase BIK1 is necessary for full activation of RBOHD, gene expression and bacterial resistance during ETI. Moreover, NLR signalling rapidly augments the transcript and/or protein levels of key PTI components. Our study supports a revised model in which potentiation of PTI is an indispensable component of ETI during bacterial infection. This revised model conceptually unites two major immune signalling cascades in plants and mechanistically explains some of the long-observed similarities in downstream defence outputs between PTI and ETI.
Bacteria elicit two distinct immune responses in
Arabidopsis thaliana
, mediated by diverse signalling receptors but working in a synergistic manner. |
doi_str_mv | 10.1038/s41586-021-03316-6 |
format | Article |
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1
–
4
. PTI and ETI are initiated by distinct activation mechanisms and involve different early signalling cascades
5
,
6
. Here we show that
Arabidopsis
PRR and PRR co-receptor mutants—
fls2 efr cerk1
and
bak1 bkk1 cerk1
triple mutants—are markedly impaired in ETI responses when challenged with incompatible
Pseudomonas syrinage
bacteria. We further show that the production of reactive oxygen species by the NADPH oxidase RBOHD is a critical early signalling event connecting PRR- and NLR-mediated immunity, and that the receptor-like cytoplasmic kinase BIK1 is necessary for full activation of RBOHD, gene expression and bacterial resistance during ETI. Moreover, NLR signalling rapidly augments the transcript and/or protein levels of key PTI components. Our study supports a revised model in which potentiation of PTI is an indispensable component of ETI during bacterial infection. This revised model conceptually unites two major immune signalling cascades in plants and mechanistically explains some of the long-observed similarities in downstream defence outputs between PTI and ETI.
Bacteria elicit two distinct immune responses in
Arabidopsis thaliana
, mediated by diverse signalling receptors but working in a synergistic manner.</description><identifier>ISSN: 0028-0836</identifier><identifier>EISSN: 1476-4687</identifier><identifier>DOI: 10.1038/s41586-021-03316-6</identifier><identifier>PMID: 33692546</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>14/19 ; 14/5 ; 38/39 ; 38/90 ; 631/449/2169/2107 ; 631/449/2169/2673 ; 631/449/2661/2666 ; 631/449/2675 ; 82 ; 82/1 ; 82/29 ; 82/80 ; 96 ; 96/34 ; Arabidopsis - genetics ; Arabidopsis - immunology ; Arabidopsis - microbiology ; Arabidopsis Proteins - metabolism ; Bacteria ; Bacterial diseases ; Bacterial infections ; Cell surface ; Crop fields ; Gene expression ; Humanities and Social Sciences ; Immune system ; Immunity ; Innate immunity ; Kinases ; Leucine ; Microorganisms ; multidisciplinary ; Mutants ; NAD(P)H oxidase ; NADPH Oxidases - metabolism ; NLR Proteins - immunology ; Nucleotides ; Oxygen ; Pathogens ; Pattern recognition ; Plant Diseases - genetics ; Plant Diseases - immunology ; Plant Diseases - microbiology ; Plant immunity ; Plant Immunity - immunology ; Protein Serine-Threonine Kinases - metabolism ; Proteins ; Pseudomonas syringae - immunology ; Reactive oxygen species ; Reactive Oxygen Species - metabolism ; Receptors ; Receptors, Pattern Recognition - immunology ; Science ; Science (multidisciplinary) ; Signal Transduction - immunology ; Signaling ; Transcription</subject><ispartof>Nature (London), 2021-04, Vol.592 (7852), p.105-109</ispartof><rights>The Author(s), under exclusive licence to Springer Nature Limited part of Springer Nature 2021</rights><rights>Copyright Nature Publishing Group Apr 1, 2021</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c577t-a9e20503c86976cc6f814604429ffaaef16b9cb9ea5d0d88091382179a6409a53</citedby><cites>FETCH-LOGICAL-c577t-a9e20503c86976cc6f814604429ffaaef16b9cb9ea5d0d88091382179a6409a53</cites><orcidid>0000-0002-9943-2975 ; 0000-0002-4037-3528</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1038/s41586-021-03316-6$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1038/s41586-021-03316-6$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>230,314,776,780,881,27901,27902,41464,42533,51294</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33692546$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Yuan, Minhang</creatorcontrib><creatorcontrib>Jiang, Zeyu</creatorcontrib><creatorcontrib>Bi, Guozhi</creatorcontrib><creatorcontrib>Nomura, Kinya</creatorcontrib><creatorcontrib>Liu, Menghui</creatorcontrib><creatorcontrib>Wang, Yiping</creatorcontrib><creatorcontrib>Cai, Boying</creatorcontrib><creatorcontrib>Zhou, Jian-Min</creatorcontrib><creatorcontrib>He, Sheng Yang</creatorcontrib><creatorcontrib>Xin, Xiu-Fang</creatorcontrib><title>Pattern-recognition receptors are required for NLR-mediated plant immunity</title><title>Nature (London)</title><addtitle>Nature</addtitle><addtitle>Nature</addtitle><description>The plant immune system is fundamental for plant survival in natural ecosystems and for productivity in crop fields. Substantial evidence supports the prevailing notion that plants possess a two-tiered innate immune system, called pattern-triggered immunity (PTI) and effector-triggered immunity (ETI). PTI is triggered by microbial patterns via cell surface-localized pattern-recognition receptors (PRRs), whereas ETI is activated by pathogen effector proteins via predominantly intracellularly localized receptors called nucleotide-binding, leucine-rich repeat receptors (NLRs)
1
–
4
. PTI and ETI are initiated by distinct activation mechanisms and involve different early signalling cascades
5
,
6
. Here we show that
Arabidopsis
PRR and PRR co-receptor mutants—
fls2 efr cerk1
and
bak1 bkk1 cerk1
triple mutants—are markedly impaired in ETI responses when challenged with incompatible
Pseudomonas syrinage
bacteria. We further show that the production of reactive oxygen species by the NADPH oxidase RBOHD is a critical early signalling event connecting PRR- and NLR-mediated immunity, and that the receptor-like cytoplasmic kinase BIK1 is necessary for full activation of RBOHD, gene expression and bacterial resistance during ETI. Moreover, NLR signalling rapidly augments the transcript and/or protein levels of key PTI components. Our study supports a revised model in which potentiation of PTI is an indispensable component of ETI during bacterial infection. This revised model conceptually unites two major immune signalling cascades in plants and mechanistically explains some of the long-observed similarities in downstream defence outputs between PTI and ETI.
Bacteria elicit two distinct immune responses in
Arabidopsis thaliana
, mediated by diverse signalling receptors but working in a synergistic manner.</description><subject>14/19</subject><subject>14/5</subject><subject>38/39</subject><subject>38/90</subject><subject>631/449/2169/2107</subject><subject>631/449/2169/2673</subject><subject>631/449/2661/2666</subject><subject>631/449/2675</subject><subject>82</subject><subject>82/1</subject><subject>82/29</subject><subject>82/80</subject><subject>96</subject><subject>96/34</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - immunology</subject><subject>Arabidopsis - microbiology</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Bacteria</subject><subject>Bacterial diseases</subject><subject>Bacterial infections</subject><subject>Cell surface</subject><subject>Crop fields</subject><subject>Gene expression</subject><subject>Humanities and Social Sciences</subject><subject>Immune system</subject><subject>Immunity</subject><subject>Innate immunity</subject><subject>Kinases</subject><subject>Leucine</subject><subject>Microorganisms</subject><subject>multidisciplinary</subject><subject>Mutants</subject><subject>NAD(P)H oxidase</subject><subject>NADPH Oxidases - metabolism</subject><subject>NLR Proteins - immunology</subject><subject>Nucleotides</subject><subject>Oxygen</subject><subject>Pathogens</subject><subject>Pattern recognition</subject><subject>Plant Diseases - genetics</subject><subject>Plant Diseases - immunology</subject><subject>Plant Diseases - microbiology</subject><subject>Plant immunity</subject><subject>Plant Immunity - immunology</subject><subject>Protein Serine-Threonine Kinases - metabolism</subject><subject>Proteins</subject><subject>Pseudomonas syringae - immunology</subject><subject>Reactive oxygen species</subject><subject>Reactive Oxygen Species - metabolism</subject><subject>Receptors</subject><subject>Receptors, Pattern Recognition - immunology</subject><subject>Science</subject><subject>Science 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receptors are required for NLR-mediated plant immunity</title><author>Yuan, Minhang ; Jiang, Zeyu ; Bi, Guozhi ; Nomura, Kinya ; Liu, Menghui ; Wang, Yiping ; Cai, Boying ; Zhou, Jian-Min ; He, Sheng Yang ; Xin, Xiu-Fang</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c577t-a9e20503c86976cc6f814604429ffaaef16b9cb9ea5d0d88091382179a6409a53</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>14/19</topic><topic>14/5</topic><topic>38/39</topic><topic>38/90</topic><topic>631/449/2169/2107</topic><topic>631/449/2169/2673</topic><topic>631/449/2661/2666</topic><topic>631/449/2675</topic><topic>82</topic><topic>82/1</topic><topic>82/29</topic><topic>82/80</topic><topic>96</topic><topic>96/34</topic><topic>Arabidopsis - genetics</topic><topic>Arabidopsis - immunology</topic><topic>Arabidopsis - microbiology</topic><topic>Arabidopsis Proteins - 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(London)</jtitle><stitle>Nature</stitle><addtitle>Nature</addtitle><date>2021-04-01</date><risdate>2021</risdate><volume>592</volume><issue>7852</issue><spage>105</spage><epage>109</epage><pages>105-109</pages><issn>0028-0836</issn><eissn>1476-4687</eissn><abstract>The plant immune system is fundamental for plant survival in natural ecosystems and for productivity in crop fields. Substantial evidence supports the prevailing notion that plants possess a two-tiered innate immune system, called pattern-triggered immunity (PTI) and effector-triggered immunity (ETI). PTI is triggered by microbial patterns via cell surface-localized pattern-recognition receptors (PRRs), whereas ETI is activated by pathogen effector proteins via predominantly intracellularly localized receptors called nucleotide-binding, leucine-rich repeat receptors (NLRs)
1
–
4
. PTI and ETI are initiated by distinct activation mechanisms and involve different early signalling cascades
5
,
6
. Here we show that
Arabidopsis
PRR and PRR co-receptor mutants—
fls2 efr cerk1
and
bak1 bkk1 cerk1
triple mutants—are markedly impaired in ETI responses when challenged with incompatible
Pseudomonas syrinage
bacteria. We further show that the production of reactive oxygen species by the NADPH oxidase RBOHD is a critical early signalling event connecting PRR- and NLR-mediated immunity, and that the receptor-like cytoplasmic kinase BIK1 is necessary for full activation of RBOHD, gene expression and bacterial resistance during ETI. Moreover, NLR signalling rapidly augments the transcript and/or protein levels of key PTI components. Our study supports a revised model in which potentiation of PTI is an indispensable component of ETI during bacterial infection. This revised model conceptually unites two major immune signalling cascades in plants and mechanistically explains some of the long-observed similarities in downstream defence outputs between PTI and ETI.
Bacteria elicit two distinct immune responses in
Arabidopsis thaliana
, mediated by diverse signalling receptors but working in a synergistic manner.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>33692546</pmid><doi>10.1038/s41586-021-03316-6</doi><tpages>5</tpages><orcidid>https://orcid.org/0000-0002-9943-2975</orcidid><orcidid>https://orcid.org/0000-0002-4037-3528</orcidid><oa>free_for_read</oa></addata></record> |
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identifier | ISSN: 0028-0836 |
ispartof | Nature (London), 2021-04, Vol.592 (7852), p.105-109 |
issn | 0028-0836 1476-4687 |
language | eng |
recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_8016741 |
source | MEDLINE; Nature; SpringerLink Journals - AutoHoldings |
subjects | 14/19 14/5 38/39 38/90 631/449/2169/2107 631/449/2169/2673 631/449/2661/2666 631/449/2675 82 82/1 82/29 82/80 96 96/34 Arabidopsis - genetics Arabidopsis - immunology Arabidopsis - microbiology Arabidopsis Proteins - metabolism Bacteria Bacterial diseases Bacterial infections Cell surface Crop fields Gene expression Humanities and Social Sciences Immune system Immunity Innate immunity Kinases Leucine Microorganisms multidisciplinary Mutants NAD(P)H oxidase NADPH Oxidases - metabolism NLR Proteins - immunology Nucleotides Oxygen Pathogens Pattern recognition Plant Diseases - genetics Plant Diseases - immunology Plant Diseases - microbiology Plant immunity Plant Immunity - immunology Protein Serine-Threonine Kinases - metabolism Proteins Pseudomonas syringae - immunology Reactive oxygen species Reactive Oxygen Species - metabolism Receptors Receptors, Pattern Recognition - immunology Science Science (multidisciplinary) Signal Transduction - immunology Signaling Transcription |
title | Pattern-recognition receptors are required for NLR-mediated plant immunity |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-03T16%3A13%3A44IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Pattern-recognition%20receptors%20are%20required%20for%20NLR-mediated%20plant%20immunity&rft.jtitle=Nature%20(London)&rft.au=Yuan,%20Minhang&rft.date=2021-04-01&rft.volume=592&rft.issue=7852&rft.spage=105&rft.epage=109&rft.pages=105-109&rft.issn=0028-0836&rft.eissn=1476-4687&rft_id=info:doi/10.1038/s41586-021-03316-6&rft_dat=%3Cproquest_pubme%3E2509035543%3C/proquest_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2509035543&rft_id=info:pmid/33692546&rfr_iscdi=true |