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The Small GTPase OsRac1 Forms Two Distinct Immune Receptor Complexes Containing the PRR OsCERK1 and the NLR Pit
Abstract Plants employ two different types of immune receptors, cell surface pattern recognition receptors (PRRs) and intracellular nucleotide-binding and leucine-rich repeat-containing proteins (NLRs), to cope with pathogen invasion. Both immune receptors often share similar downstream components a...
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Published in: | Plant and cell physiology 2021-12, Vol.62 (11), p.1662-1675 |
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creator | Akamatsu, Akira Fujiwara, Masayuki Hamada, Satoshi Wakabayashi, Megumi Yao, Ai Wang, Qiong Kosami, Ken-ichi Dang, Thu Thi Kaneko-Kawano, Takako Fukada, Fumi Shimamoto, Ko Kawano, Yoji |
description | Abstract
Plants employ two different types of immune receptors, cell surface pattern recognition receptors (PRRs) and intracellular nucleotide-binding and leucine-rich repeat-containing proteins (NLRs), to cope with pathogen invasion. Both immune receptors often share similar downstream components and responses but it remains unknown whether a PRR and an NLR assemble into the same protein complex or two distinct receptor complexes. We have previously found that the small GTPase OsRac1 plays key roles in the signaling of OsCERK1, a PRR for fungal chitin, and of Pit, an NLR for rice blast fungus, and associates directly and indirectly with both of these immune receptors. In this study, using biochemical and bioimaging approaches, we revealed that OsRac1 formed two distinct receptor complexes with OsCERK1 and with Pit. Supporting this result, OsCERK1 and Pit utilized different transport systems for anchorage to the plasma membrane (PM). Activation of OsCERK1 and Pit led to OsRac1 activation and, concomitantly, OsRac1 shifted from a small to a large protein complex fraction. We also found that the chaperone Hsp90 contributed to the proper transport of Pit to the PM and the immune induction of Pit. These findings illuminate how the PRR OsCERK1 and the NLR Pit orchestrate rice immunity through the small GTPase OsRac1. |
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Plants employ two different types of immune receptors, cell surface pattern recognition receptors (PRRs) and intracellular nucleotide-binding and leucine-rich repeat-containing proteins (NLRs), to cope with pathogen invasion. Both immune receptors often share similar downstream components and responses but it remains unknown whether a PRR and an NLR assemble into the same protein complex or two distinct receptor complexes. We have previously found that the small GTPase OsRac1 plays key roles in the signaling of OsCERK1, a PRR for fungal chitin, and of Pit, an NLR for rice blast fungus, and associates directly and indirectly with both of these immune receptors. In this study, using biochemical and bioimaging approaches, we revealed that OsRac1 formed two distinct receptor complexes with OsCERK1 and with Pit. Supporting this result, OsCERK1 and Pit utilized different transport systems for anchorage to the plasma membrane (PM). Activation of OsCERK1 and Pit led to OsRac1 activation and, concomitantly, OsRac1 shifted from a small to a large protein complex fraction. We also found that the chaperone Hsp90 contributed to the proper transport of Pit to the PM and the immune induction of Pit. These findings illuminate how the PRR OsCERK1 and the NLR Pit orchestrate rice immunity through the small GTPase OsRac1.</description><identifier>ISSN: 0032-0781</identifier><identifier>EISSN: 1471-9053</identifier><identifier>DOI: 10.1093/pcp/pcab121</identifier><identifier>PMID: 34329461</identifier><language>eng</language><publisher>UK: Oxford University Press</publisher><subject>Cellular Biology ; GTP Phosphohydrolases - genetics ; GTP Phosphohydrolases - metabolism ; Life Sciences ; NLR Proteins - genetics ; NLR Proteins - metabolism ; Oryza - genetics ; Oryza - metabolism ; Plant Immunity - genetics ; Plant Proteins - genetics ; Plant Proteins - metabolism ; Receptors, Pattern Recognition - genetics ; Receptors, Pattern Recognition - metabolism ; Vegetal Biology</subject><ispartof>Plant and cell physiology, 2021-12, Vol.62 (11), p.1662-1675</ispartof><rights>The Author(s) 2021. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com 2021</rights><rights>The Author(s) 2021. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c501t-718c9a1364f5ae6c480d1e2276d85b8c7562b548eaa527b3ca3ea75299f5e67d3</citedby><cites>FETCH-LOGICAL-c501t-718c9a1364f5ae6c480d1e2276d85b8c7562b548eaa527b3ca3ea75299f5e67d3</cites><orcidid>0000-0002-3313-7447 ; 0000-0003-0687-2777</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,778,782,883,27911,27912</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34329461$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.inrae.fr/hal-03521723$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Akamatsu, Akira</creatorcontrib><creatorcontrib>Fujiwara, Masayuki</creatorcontrib><creatorcontrib>Hamada, Satoshi</creatorcontrib><creatorcontrib>Wakabayashi, Megumi</creatorcontrib><creatorcontrib>Yao, Ai</creatorcontrib><creatorcontrib>Wang, Qiong</creatorcontrib><creatorcontrib>Kosami, Ken-ichi</creatorcontrib><creatorcontrib>Dang, Thu Thi</creatorcontrib><creatorcontrib>Kaneko-Kawano, Takako</creatorcontrib><creatorcontrib>Fukada, Fumi</creatorcontrib><creatorcontrib>Shimamoto, Ko</creatorcontrib><creatorcontrib>Kawano, Yoji</creatorcontrib><title>The Small GTPase OsRac1 Forms Two Distinct Immune Receptor Complexes Containing the PRR OsCERK1 and the NLR Pit</title><title>Plant and cell physiology</title><addtitle>Plant Cell Physiol</addtitle><description>Abstract
Plants employ two different types of immune receptors, cell surface pattern recognition receptors (PRRs) and intracellular nucleotide-binding and leucine-rich repeat-containing proteins (NLRs), to cope with pathogen invasion. Both immune receptors often share similar downstream components and responses but it remains unknown whether a PRR and an NLR assemble into the same protein complex or two distinct receptor complexes. We have previously found that the small GTPase OsRac1 plays key roles in the signaling of OsCERK1, a PRR for fungal chitin, and of Pit, an NLR for rice blast fungus, and associates directly and indirectly with both of these immune receptors. In this study, using biochemical and bioimaging approaches, we revealed that OsRac1 formed two distinct receptor complexes with OsCERK1 and with Pit. Supporting this result, OsCERK1 and Pit utilized different transport systems for anchorage to the plasma membrane (PM). Activation of OsCERK1 and Pit led to OsRac1 activation and, concomitantly, OsRac1 shifted from a small to a large protein complex fraction. We also found that the chaperone Hsp90 contributed to the proper transport of Pit to the PM and the immune induction of Pit. These findings illuminate how the PRR OsCERK1 and the NLR Pit orchestrate rice immunity through the small GTPase OsRac1.</description><subject>Cellular Biology</subject><subject>GTP Phosphohydrolases - genetics</subject><subject>GTP Phosphohydrolases - metabolism</subject><subject>Life Sciences</subject><subject>NLR Proteins - genetics</subject><subject>NLR Proteins - metabolism</subject><subject>Oryza - genetics</subject><subject>Oryza - metabolism</subject><subject>Plant Immunity - genetics</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - metabolism</subject><subject>Receptors, Pattern Recognition - genetics</subject><subject>Receptors, Pattern Recognition - metabolism</subject><subject>Vegetal Biology</subject><issn>0032-0781</issn><issn>1471-9053</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><recordid>eNp9kU1v1DAQhq0K1C6FU-_IJ1SEUjx2HCfHavspVu0qbM_WxJmlQUmcxgkf_x6XXXrkMJrRq0fPYV7GTkCcgSjU58ENcbACCQdsAamBpBBavWILIZRMhMnhiL0J4bsQ8VbikB2pVMkizWDB_OaR-NcO25Zfb9YYiN-HEh3wKz92gW9-en7RhKnp3cRvu27uiZfkaJj8yJe-G1r6RSFe_YRN3_Tf-BR967KMmuVl-QU49vXf7G5V8nUzvWWvt9gGerffx-zh6nKzvElW99e3y_NV4rSAKTGQuwJBZelWI2UuzUUNJKXJ6lxXuTM6k5VOc0LU0lTKoSI0WhbFVlNmanXMPu68j9jaYWw6HH9bj429OV_Z50woLcFI9QMie7pjh9E_zRQm2zXBUdtiT34OVmodQcgyFdFPO9SNPoSRti9uEPa5DRvbsPs2Iv1-L56rjuoX9t_7I_BhB_h5-K_pD8q4kE8</recordid><startdate>20211210</startdate><enddate>20211210</enddate><creator>Akamatsu, Akira</creator><creator>Fujiwara, Masayuki</creator><creator>Hamada, Satoshi</creator><creator>Wakabayashi, Megumi</creator><creator>Yao, Ai</creator><creator>Wang, Qiong</creator><creator>Kosami, Ken-ichi</creator><creator>Dang, Thu Thi</creator><creator>Kaneko-Kawano, Takako</creator><creator>Fukada, Fumi</creator><creator>Shimamoto, Ko</creator><creator>Kawano, Yoji</creator><general>Oxford University Press</general><general>Oxford University Press (OUP)</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><scope>1XC</scope><orcidid>https://orcid.org/0000-0002-3313-7447</orcidid><orcidid>https://orcid.org/0000-0003-0687-2777</orcidid></search><sort><creationdate>20211210</creationdate><title>The Small GTPase OsRac1 Forms Two Distinct Immune Receptor Complexes Containing the PRR OsCERK1 and the NLR Pit</title><author>Akamatsu, Akira ; Fujiwara, Masayuki ; Hamada, Satoshi ; Wakabayashi, Megumi ; Yao, Ai ; Wang, Qiong ; Kosami, Ken-ichi ; Dang, Thu Thi ; Kaneko-Kawano, Takako ; Fukada, Fumi ; Shimamoto, Ko ; Kawano, Yoji</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c501t-718c9a1364f5ae6c480d1e2276d85b8c7562b548eaa527b3ca3ea75299f5e67d3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Cellular Biology</topic><topic>GTP Phosphohydrolases - genetics</topic><topic>GTP Phosphohydrolases - metabolism</topic><topic>Life Sciences</topic><topic>NLR Proteins - genetics</topic><topic>NLR Proteins - metabolism</topic><topic>Oryza - genetics</topic><topic>Oryza - metabolism</topic><topic>Plant Immunity - genetics</topic><topic>Plant Proteins - genetics</topic><topic>Plant Proteins - metabolism</topic><topic>Receptors, Pattern Recognition - genetics</topic><topic>Receptors, Pattern Recognition - metabolism</topic><topic>Vegetal Biology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Akamatsu, Akira</creatorcontrib><creatorcontrib>Fujiwara, Masayuki</creatorcontrib><creatorcontrib>Hamada, Satoshi</creatorcontrib><creatorcontrib>Wakabayashi, Megumi</creatorcontrib><creatorcontrib>Yao, Ai</creatorcontrib><creatorcontrib>Wang, Qiong</creatorcontrib><creatorcontrib>Kosami, Ken-ichi</creatorcontrib><creatorcontrib>Dang, Thu Thi</creatorcontrib><creatorcontrib>Kaneko-Kawano, Takako</creatorcontrib><creatorcontrib>Fukada, Fumi</creatorcontrib><creatorcontrib>Shimamoto, Ko</creatorcontrib><creatorcontrib>Kawano, Yoji</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><collection>Hyper Article en Ligne (HAL)</collection><jtitle>Plant and cell physiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Akamatsu, Akira</au><au>Fujiwara, Masayuki</au><au>Hamada, Satoshi</au><au>Wakabayashi, Megumi</au><au>Yao, Ai</au><au>Wang, Qiong</au><au>Kosami, Ken-ichi</au><au>Dang, Thu Thi</au><au>Kaneko-Kawano, Takako</au><au>Fukada, Fumi</au><au>Shimamoto, Ko</au><au>Kawano, Yoji</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The Small GTPase OsRac1 Forms Two Distinct Immune Receptor Complexes Containing the PRR OsCERK1 and the NLR Pit</atitle><jtitle>Plant and cell physiology</jtitle><addtitle>Plant Cell Physiol</addtitle><date>2021-12-10</date><risdate>2021</risdate><volume>62</volume><issue>11</issue><spage>1662</spage><epage>1675</epage><pages>1662-1675</pages><issn>0032-0781</issn><eissn>1471-9053</eissn><abstract>Abstract
Plants employ two different types of immune receptors, cell surface pattern recognition receptors (PRRs) and intracellular nucleotide-binding and leucine-rich repeat-containing proteins (NLRs), to cope with pathogen invasion. Both immune receptors often share similar downstream components and responses but it remains unknown whether a PRR and an NLR assemble into the same protein complex or two distinct receptor complexes. We have previously found that the small GTPase OsRac1 plays key roles in the signaling of OsCERK1, a PRR for fungal chitin, and of Pit, an NLR for rice blast fungus, and associates directly and indirectly with both of these immune receptors. In this study, using biochemical and bioimaging approaches, we revealed that OsRac1 formed two distinct receptor complexes with OsCERK1 and with Pit. Supporting this result, OsCERK1 and Pit utilized different transport systems for anchorage to the plasma membrane (PM). Activation of OsCERK1 and Pit led to OsRac1 activation and, concomitantly, OsRac1 shifted from a small to a large protein complex fraction. We also found that the chaperone Hsp90 contributed to the proper transport of Pit to the PM and the immune induction of Pit. These findings illuminate how the PRR OsCERK1 and the NLR Pit orchestrate rice immunity through the small GTPase OsRac1.</abstract><cop>UK</cop><pub>Oxford University Press</pub><pmid>34329461</pmid><doi>10.1093/pcp/pcab121</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0002-3313-7447</orcidid><orcidid>https://orcid.org/0000-0003-0687-2777</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Cellular Biology GTP Phosphohydrolases - genetics GTP Phosphohydrolases - metabolism Life Sciences NLR Proteins - genetics NLR Proteins - metabolism Oryza - genetics Oryza - metabolism Plant Immunity - genetics Plant Proteins - genetics Plant Proteins - metabolism Receptors, Pattern Recognition - genetics Receptors, Pattern Recognition - metabolism Vegetal Biology |
title | The Small GTPase OsRac1 Forms Two Distinct Immune Receptor Complexes Containing the PRR OsCERK1 and the NLR Pit |
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