The phagocytosis oxidase/Bem1p domain‐containing protein PB1CP negatively regulates the NADPH oxidase RBOHD in plant immunity
Summary Perception of pathogen‐associated molecular patterns (PAMPs) by surface‐localized pattern recognition receptors activates RESPIRATORY BURST OXIDASE HOMOLOG D (RBOHD) through direct phosphorylation by BOTRYTIS‐INDUCED KINASE 1 (BIK1) and induces the production of reactive oxygen species (ROS)...
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| Veröffentlicht in: | The New phytologist 2024-02, Vol.241 (4), p.1763-1779 |
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| container_title | The New phytologist |
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| creator | Goto, Yukihisa Maki, Noriko Sklenar, Jan Derbyshire, Paul Menke, Frank L. H. Zipfel, Cyril Kadota, Yasuhiro Shirasu, Ken |
| description | Summary
Perception of pathogen‐associated molecular patterns (PAMPs) by surface‐localized pattern recognition receptors activates RESPIRATORY BURST OXIDASE HOMOLOG D (RBOHD) through direct phosphorylation by BOTRYTIS‐INDUCED KINASE 1 (BIK1) and induces the production of reactive oxygen species (ROS). RBOHD activity must be tightly controlled to avoid the detrimental effects of ROS, but little is known about RBOHD downregulation.
To understand the regulation of RBOHD, we used co‐immunoprecipitation of RBOHD with mass spectrometry analysis and identified PHAGOCYTOSIS OXIDASE/BEM1P (PB1) DOMAIN‐CONTAINING PROTEIN (PB1CP).
PB1CP negatively regulates RBOHD and the resistance against the fungal pathogen Colletotrichum higginsianum. PB1CP competes with BIK1 for binding to RBOHD in vitro. Furthermore, PAMP treatment enhances the PB1CP‐RBOHD interaction, thereby leading to the dissociation of phosphorylated BIK1 from RBOHD in vivo. PB1CP localizes at the cell periphery and PAMP treatment induces relocalization of PB1CP and RBOHD to the same small endomembrane compartments. Additionally, overexpression of PB1CP in Arabidopsis leads to a reduction in the abundance of RBOHD protein, suggesting the possible involvement of PB1CP in RBOHD endocytosis.
We found PB1CP, a novel negative regulator of RBOHD, and revealed its possible regulatory mechanisms involving the removal of phosphorylated BIK1 from RBOHD and the promotion of RBOHD endocytosis.
See also the Commentary on this article by Torres, 241: 1384–1386. |
| doi_str_mv | 10.1111/nph.19302 |
| format | Article |
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Perception of pathogen‐associated molecular patterns (PAMPs) by surface‐localized pattern recognition receptors activates RESPIRATORY BURST OXIDASE HOMOLOG D (RBOHD) through direct phosphorylation by BOTRYTIS‐INDUCED KINASE 1 (BIK1) and induces the production of reactive oxygen species (ROS). RBOHD activity must be tightly controlled to avoid the detrimental effects of ROS, but little is known about RBOHD downregulation.
To understand the regulation of RBOHD, we used co‐immunoprecipitation of RBOHD with mass spectrometry analysis and identified PHAGOCYTOSIS OXIDASE/BEM1P (PB1) DOMAIN‐CONTAINING PROTEIN (PB1CP).
PB1CP negatively regulates RBOHD and the resistance against the fungal pathogen Colletotrichum higginsianum. PB1CP competes with BIK1 for binding to RBOHD in vitro. Furthermore, PAMP treatment enhances the PB1CP‐RBOHD interaction, thereby leading to the dissociation of phosphorylated BIK1 from RBOHD in vivo. PB1CP localizes at the cell periphery and PAMP treatment induces relocalization of PB1CP and RBOHD to the same small endomembrane compartments. Additionally, overexpression of PB1CP in Arabidopsis leads to a reduction in the abundance of RBOHD protein, suggesting the possible involvement of PB1CP in RBOHD endocytosis.
We found PB1CP, a novel negative regulator of RBOHD, and revealed its possible regulatory mechanisms involving the removal of phosphorylated BIK1 from RBOHD and the promotion of RBOHD endocytosis.
See also the Commentary on this article by Torres, 241: 1384–1386.</description><identifier>ISSN: 0028-646X</identifier><identifier>EISSN: 1469-8137</identifier><identifier>DOI: 10.1111/nph.19302</identifier><identifier>PMID: 37823353</identifier><language>eng</language><publisher>England: Wiley Subscription Services, Inc</publisher><subject>Arabidopsis ; Arabidopsis - metabolism ; Arabidopsis Proteins - metabolism ; Dissociation ; Down-regulation ; Endocytosis ; Gene Expression Regulation, Plant ; Immunity ; Immunoprecipitation ; Kinases ; Mass spectrometry ; Mass spectroscopy ; NAD(P)H oxidase ; NADPH oxidase RESPIRATORY BURST OXIDASE HOMOLOG D ; NADPH Oxidases - metabolism ; Oxidase ; Oxidoreductases - metabolism ; Pathogens ; pathogen‐associated molecular patterns ; Pattern recognition ; Pattern recognition receptors ; pattern recognition receptor‐triggered immunity ; Phagocytosis ; Phosphorylation ; Plant immunity ; Plant Immunity - genetics ; Plant Immunity - physiology ; Protein Serine-Threonine Kinases - metabolism ; Proteins ; Reactive oxygen species ; Reactive Oxygen Species - metabolism ; Regulatory mechanisms (biology) ; Respiration ; Respiratory burst oxidase</subject><ispartof>The New phytologist, 2024-02, Vol.241 (4), p.1763-1779</ispartof><rights>2023 The Authors © 2023 New Phytologist Foundation</rights><rights>2023 The Authors New Phytologist © 2023 New Phytologist Foundation.</rights><rights>2023. This article is published under http://creativecommons.org/licenses/by-nc-nd/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-c3882-ebf5a1a70065494ac39914e8219be78cfab39f1d2320c9c5c5d6af5bf28771823</citedby><cites>FETCH-LOGICAL-c3882-ebf5a1a70065494ac39914e8219be78cfab39f1d2320c9c5c5d6af5bf28771823</cites><orcidid>0000-0002-8750-7685 ; 0000-0002-5095-9397 ; 0000-0003-1858-2574 ; 0000-0002-0349-3870 ; 0000-0003-2490-4824 ; 0000-0003-3616-320X ; 0000-0002-4782-1418 ; 0000-0003-4935-8583</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fnph.19302$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fnph.19302$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>314,776,780,1411,27901,27902,45550,45551</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37823353$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Goto, Yukihisa</creatorcontrib><creatorcontrib>Maki, Noriko</creatorcontrib><creatorcontrib>Sklenar, Jan</creatorcontrib><creatorcontrib>Derbyshire, Paul</creatorcontrib><creatorcontrib>Menke, Frank L. H.</creatorcontrib><creatorcontrib>Zipfel, Cyril</creatorcontrib><creatorcontrib>Kadota, Yasuhiro</creatorcontrib><creatorcontrib>Shirasu, Ken</creatorcontrib><title>The phagocytosis oxidase/Bem1p domain‐containing protein PB1CP negatively regulates the NADPH oxidase RBOHD in plant immunity</title><title>The New phytologist</title><addtitle>New Phytol</addtitle><description>Summary
Perception of pathogen‐associated molecular patterns (PAMPs) by surface‐localized pattern recognition receptors activates RESPIRATORY BURST OXIDASE HOMOLOG D (RBOHD) through direct phosphorylation by BOTRYTIS‐INDUCED KINASE 1 (BIK1) and induces the production of reactive oxygen species (ROS). RBOHD activity must be tightly controlled to avoid the detrimental effects of ROS, but little is known about RBOHD downregulation.
To understand the regulation of RBOHD, we used co‐immunoprecipitation of RBOHD with mass spectrometry analysis and identified PHAGOCYTOSIS OXIDASE/BEM1P (PB1) DOMAIN‐CONTAINING PROTEIN (PB1CP).
PB1CP negatively regulates RBOHD and the resistance against the fungal pathogen Colletotrichum higginsianum. PB1CP competes with BIK1 for binding to RBOHD in vitro. Furthermore, PAMP treatment enhances the PB1CP‐RBOHD interaction, thereby leading to the dissociation of phosphorylated BIK1 from RBOHD in vivo. PB1CP localizes at the cell periphery and PAMP treatment induces relocalization of PB1CP and RBOHD to the same small endomembrane compartments. Additionally, overexpression of PB1CP in Arabidopsis leads to a reduction in the abundance of RBOHD protein, suggesting the possible involvement of PB1CP in RBOHD endocytosis.
We found PB1CP, a novel negative regulator of RBOHD, and revealed its possible regulatory mechanisms involving the removal of phosphorylated BIK1 from RBOHD and the promotion of RBOHD endocytosis.
See also the Commentary on this article by Torres, 241: 1384–1386.</description><subject>Arabidopsis</subject><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Dissociation</subject><subject>Down-regulation</subject><subject>Endocytosis</subject><subject>Gene Expression Regulation, Plant</subject><subject>Immunity</subject><subject>Immunoprecipitation</subject><subject>Kinases</subject><subject>Mass spectrometry</subject><subject>Mass spectroscopy</subject><subject>NAD(P)H oxidase</subject><subject>NADPH oxidase RESPIRATORY BURST OXIDASE HOMOLOG D</subject><subject>NADPH Oxidases - metabolism</subject><subject>Oxidase</subject><subject>Oxidoreductases - metabolism</subject><subject>Pathogens</subject><subject>pathogen‐associated molecular patterns</subject><subject>Pattern recognition</subject><subject>Pattern recognition receptors</subject><subject>pattern recognition receptor‐triggered immunity</subject><subject>Phagocytosis</subject><subject>Phosphorylation</subject><subject>Plant immunity</subject><subject>Plant Immunity - genetics</subject><subject>Plant Immunity - physiology</subject><subject>Protein Serine-Threonine Kinases - metabolism</subject><subject>Proteins</subject><subject>Reactive oxygen species</subject><subject>Reactive Oxygen Species - metabolism</subject><subject>Regulatory mechanisms (biology)</subject><subject>Respiration</subject><subject>Respiratory burst oxidase</subject><issn>0028-646X</issn><issn>1469-8137</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>EIF</sourceid><recordid>eNp1kc1u1DAURi0EokNhwQsgS2zoIh3_JI697EwLg1S1I1Qkdpbj3My4Suw0ToCs4BF4Rp4Ew7QskLgb38Xx0Xf1IfSSklOaZun7_SlVnLBHaEFzoTJJefkYLQhhMhO5-HSEnsV4SwhRhWBP0REvJeO84Av07WYPuN-bXbDzGKKLOHx1tYmwXEFHe1yHzjj_8_sPG_yYNud3uB_CCM7j7Yqut9jDzozuM7QzHmA3tWaEiMdkvTo7324edPjD6npzjtOvvjV-xK7rJu_G-Tl60pg2wov79xh9fHtxs95kl9fv3q_PLjPLpWQZVE1hqCkJEUWucmO5UjQHyaiqoJS2MRVXDa0ZZ8QqW9iiFqYpqobJsqTp2GP05uBN4e8miKPuXLTQpjAQpqgTJ0ROclYm9PU_6G2YBp_SaaZoqaSUXCTq5EDZIcQ4QKP7wXVmmDUl-ncrOrWi_7SS2Ff3xqnqoP5LPtSQgOUB-OJamP9v0lfbzUH5C-UNl1g</recordid><startdate>202402</startdate><enddate>202402</enddate><creator>Goto, Yukihisa</creator><creator>Maki, Noriko</creator><creator>Sklenar, Jan</creator><creator>Derbyshire, Paul</creator><creator>Menke, Frank L. 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H. ; Zipfel, Cyril ; Kadota, Yasuhiro ; Shirasu, Ken</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3882-ebf5a1a70065494ac39914e8219be78cfab39f1d2320c9c5c5d6af5bf28771823</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Arabidopsis</topic><topic>Arabidopsis - metabolism</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>Dissociation</topic><topic>Down-regulation</topic><topic>Endocytosis</topic><topic>Gene Expression Regulation, Plant</topic><topic>Immunity</topic><topic>Immunoprecipitation</topic><topic>Kinases</topic><topic>Mass spectrometry</topic><topic>Mass spectroscopy</topic><topic>NAD(P)H oxidase</topic><topic>NADPH oxidase RESPIRATORY BURST OXIDASE HOMOLOG D</topic><topic>NADPH Oxidases - metabolism</topic><topic>Oxidase</topic><topic>Oxidoreductases - metabolism</topic><topic>Pathogens</topic><topic>pathogen‐associated molecular patterns</topic><topic>Pattern recognition</topic><topic>Pattern recognition receptors</topic><topic>pattern recognition receptor‐triggered immunity</topic><topic>Phagocytosis</topic><topic>Phosphorylation</topic><topic>Plant immunity</topic><topic>Plant Immunity - genetics</topic><topic>Plant Immunity - physiology</topic><topic>Protein Serine-Threonine Kinases - metabolism</topic><topic>Proteins</topic><topic>Reactive oxygen species</topic><topic>Reactive Oxygen Species - metabolism</topic><topic>Regulatory mechanisms (biology)</topic><topic>Respiration</topic><topic>Respiratory burst oxidase</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Goto, Yukihisa</creatorcontrib><creatorcontrib>Maki, Noriko</creatorcontrib><creatorcontrib>Sklenar, Jan</creatorcontrib><creatorcontrib>Derbyshire, Paul</creatorcontrib><creatorcontrib>Menke, Frank L. H.</creatorcontrib><creatorcontrib>Zipfel, Cyril</creatorcontrib><creatorcontrib>Kadota, Yasuhiro</creatorcontrib><creatorcontrib>Shirasu, Ken</creatorcontrib><collection>Wiley Online Library Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Biotechnology Research Abstracts</collection><collection>Ecology Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Engineering Research Database</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>The New phytologist</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Goto, Yukihisa</au><au>Maki, Noriko</au><au>Sklenar, Jan</au><au>Derbyshire, Paul</au><au>Menke, Frank L. H.</au><au>Zipfel, Cyril</au><au>Kadota, Yasuhiro</au><au>Shirasu, Ken</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The phagocytosis oxidase/Bem1p domain‐containing protein PB1CP negatively regulates the NADPH oxidase RBOHD in plant immunity</atitle><jtitle>The New phytologist</jtitle><addtitle>New Phytol</addtitle><date>2024-02</date><risdate>2024</risdate><volume>241</volume><issue>4</issue><spage>1763</spage><epage>1779</epage><pages>1763-1779</pages><issn>0028-646X</issn><eissn>1469-8137</eissn><abstract>Summary
Perception of pathogen‐associated molecular patterns (PAMPs) by surface‐localized pattern recognition receptors activates RESPIRATORY BURST OXIDASE HOMOLOG D (RBOHD) through direct phosphorylation by BOTRYTIS‐INDUCED KINASE 1 (BIK1) and induces the production of reactive oxygen species (ROS). RBOHD activity must be tightly controlled to avoid the detrimental effects of ROS, but little is known about RBOHD downregulation.
To understand the regulation of RBOHD, we used co‐immunoprecipitation of RBOHD with mass spectrometry analysis and identified PHAGOCYTOSIS OXIDASE/BEM1P (PB1) DOMAIN‐CONTAINING PROTEIN (PB1CP).
PB1CP negatively regulates RBOHD and the resistance against the fungal pathogen Colletotrichum higginsianum. PB1CP competes with BIK1 for binding to RBOHD in vitro. Furthermore, PAMP treatment enhances the PB1CP‐RBOHD interaction, thereby leading to the dissociation of phosphorylated BIK1 from RBOHD in vivo. PB1CP localizes at the cell periphery and PAMP treatment induces relocalization of PB1CP and RBOHD to the same small endomembrane compartments. Additionally, overexpression of PB1CP in Arabidopsis leads to a reduction in the abundance of RBOHD protein, suggesting the possible involvement of PB1CP in RBOHD endocytosis.
We found PB1CP, a novel negative regulator of RBOHD, and revealed its possible regulatory mechanisms involving the removal of phosphorylated BIK1 from RBOHD and the promotion of RBOHD endocytosis.
See also the Commentary on this article by Torres, 241: 1384–1386.</abstract><cop>England</cop><pub>Wiley Subscription Services, Inc</pub><pmid>37823353</pmid><doi>10.1111/nph.19302</doi><tpages>1779</tpages><orcidid>https://orcid.org/0000-0002-8750-7685</orcidid><orcidid>https://orcid.org/0000-0002-5095-9397</orcidid><orcidid>https://orcid.org/0000-0003-1858-2574</orcidid><orcidid>https://orcid.org/0000-0002-0349-3870</orcidid><orcidid>https://orcid.org/0000-0003-2490-4824</orcidid><orcidid>https://orcid.org/0000-0003-3616-320X</orcidid><orcidid>https://orcid.org/0000-0002-4782-1418</orcidid><orcidid>https://orcid.org/0000-0003-4935-8583</orcidid><oa>free_for_read</oa></addata></record> |
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| ispartof | The New phytologist, 2024-02, Vol.241 (4), p.1763-1779 |
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| source | MEDLINE; Wiley Online Library Journals Frontfile Complete; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals |
| subjects | Arabidopsis Arabidopsis - metabolism Arabidopsis Proteins - metabolism Dissociation Down-regulation Endocytosis Gene Expression Regulation, Plant Immunity Immunoprecipitation Kinases Mass spectrometry Mass spectroscopy NAD(P)H oxidase NADPH oxidase RESPIRATORY BURST OXIDASE HOMOLOG D NADPH Oxidases - metabolism Oxidase Oxidoreductases - metabolism Pathogens pathogen‐associated molecular patterns Pattern recognition Pattern recognition receptors pattern recognition receptor‐triggered immunity Phagocytosis Phosphorylation Plant immunity Plant Immunity - genetics Plant Immunity - physiology Protein Serine-Threonine Kinases - metabolism Proteins Reactive oxygen species Reactive Oxygen Species - metabolism Regulatory mechanisms (biology) Respiration Respiratory burst oxidase |
| title | The phagocytosis oxidase/Bem1p domain‐containing protein PB1CP negatively regulates the NADPH oxidase RBOHD in plant immunity |
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