Cysteine protease RD21A regulated by E3 ligase SINAT4 is required for drought-induced resistance to Pseudomonas syringae in Arabidopsis

Abstract Plants can be simultaneously exposed to multiple stresses. The interplay of abiotic and biotic stresses may result in synergistic or antagonistic effects on plant development and health. Temporary drought stress can stimulate plant immunity; however, the molecular mechanism of drought-induc...

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Veröffentlicht in:Journal of experimental botany 2020-09, Vol.71 (18), p.5562-5576
Hauptverfasser: Liu, Yi, Wang, Kunru, Cheng, Qiang, Kong, Danyu, Zhang, Xunzhong, Wang, Zhibo, Wang, Qian, Xie, Qi, Yan, Jijun, Chu, Jinfang, Ling, Hong-Qing, Li, Qi, Miao, Jiamin, Zhao, Bingyu
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container_issue 18
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container_title Journal of experimental botany
container_volume 71
creator Liu, Yi
Wang, Kunru
Cheng, Qiang
Kong, Danyu
Zhang, Xunzhong
Wang, Zhibo
Wang, Qian
Xie, Qi
Yan, Jijun
Chu, Jinfang
Ling, Hong-Qing
Li, Qi
Miao, Jiamin
Zhao, Bingyu
description Abstract Plants can be simultaneously exposed to multiple stresses. The interplay of abiotic and biotic stresses may result in synergistic or antagonistic effects on plant development and health. Temporary drought stress can stimulate plant immunity; however, the molecular mechanism of drought-induced immunity is largely unknown. In this study, we demonstrate that cysteine protease RD21A is required for drought-induced immunity. Temporarily drought-treated wild-type Arabidopsis plants became more sensitive to the bacterial pathogen-associated molecular pattern flg22, triggering stomatal closure, which resulted in increased resistance to Pseudomonas syringae pv. tomato DC3000 (Pst-DC3000). Knocking out rd21a inhibited flg22-triggered stomatal closure and compromised the drought-induced immunity. Ubiquitin E3 ligase SINAT4 interacted with RD21A and promoted its degradation in vivo. The overexpression of SINAT4 also consistently compromised the drought-induced immunity to Pst-DC3000. A bacterial type III effector, AvrRxo1, interacted with both SINAT4 and RD21A, enhancing SINAT4 activity and promoting the degradation of RD21A in vivo. Therefore, RD21A could be a positive regulator of drought-induced immunity, which could be targeted by pathogen virulence effectors during pathogenesis.
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The interplay of abiotic and biotic stresses may result in synergistic or antagonistic effects on plant development and health. Temporary drought stress can stimulate plant immunity; however, the molecular mechanism of drought-induced immunity is largely unknown. In this study, we demonstrate that cysteine protease RD21A is required for drought-induced immunity. Temporarily drought-treated wild-type Arabidopsis plants became more sensitive to the bacterial pathogen-associated molecular pattern flg22, triggering stomatal closure, which resulted in increased resistance to Pseudomonas syringae pv. tomato DC3000 (Pst-DC3000). Knocking out rd21a inhibited flg22-triggered stomatal closure and compromised the drought-induced immunity. Ubiquitin E3 ligase SINAT4 interacted with RD21A and promoted its degradation in vivo. The overexpression of SINAT4 also consistently compromised the drought-induced immunity to Pst-DC3000. A bacterial type III effector, AvrRxo1, interacted with both SINAT4 and RD21A, enhancing SINAT4 activity and promoting the degradation of RD21A in vivo. Therefore, RD21A could be a positive regulator of drought-induced immunity, which could be targeted by pathogen virulence effectors during pathogenesis.</description><identifier>ISSN: 0022-0957</identifier><identifier>EISSN: 1460-2431</identifier><identifier>DOI: 10.1093/jxb/eraa255</identifier><identifier>PMID: 32453812</identifier><language>eng</language><publisher>UK: Oxford University Press</publisher><subject>Arabidopsis - genetics ; Arabidopsis - metabolism ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; Cysteine Proteases - genetics ; Droughts ; Gene Expression Regulation, Plant ; Plant Diseases ; Pseudomonas syringae - metabolism ; Ubiquitin-Protein Ligases - genetics</subject><ispartof>Journal of experimental botany, 2020-09, Vol.71 (18), p.5562-5576</ispartof><rights>Published by Oxford University Press on behalf of the Society for Experimental Biology 2020. 2020</rights><rights>Published by Oxford University Press on behalf of the Society for Experimental Biology 2020.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c357t-4aa3eddb98a0e131e0cfc924efb04365daf5e84ceda4531c87c2ca1e2abe4ab53</citedby><cites>FETCH-LOGICAL-c357t-4aa3eddb98a0e131e0cfc924efb04365daf5e84ceda4531c87c2ca1e2abe4ab53</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,776,780,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32453812$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Liu, Yi</creatorcontrib><creatorcontrib>Wang, Kunru</creatorcontrib><creatorcontrib>Cheng, Qiang</creatorcontrib><creatorcontrib>Kong, Danyu</creatorcontrib><creatorcontrib>Zhang, Xunzhong</creatorcontrib><creatorcontrib>Wang, Zhibo</creatorcontrib><creatorcontrib>Wang, Qian</creatorcontrib><creatorcontrib>Xie, Qi</creatorcontrib><creatorcontrib>Yan, Jijun</creatorcontrib><creatorcontrib>Chu, Jinfang</creatorcontrib><creatorcontrib>Ling, Hong-Qing</creatorcontrib><creatorcontrib>Li, Qi</creatorcontrib><creatorcontrib>Miao, Jiamin</creatorcontrib><creatorcontrib>Zhao, Bingyu</creatorcontrib><title>Cysteine protease RD21A regulated by E3 ligase SINAT4 is required for drought-induced resistance to Pseudomonas syringae in Arabidopsis</title><title>Journal of experimental botany</title><addtitle>J Exp Bot</addtitle><description>Abstract Plants can be simultaneously exposed to multiple stresses. The interplay of abiotic and biotic stresses may result in synergistic or antagonistic effects on plant development and health. Temporary drought stress can stimulate plant immunity; however, the molecular mechanism of drought-induced immunity is largely unknown. In this study, we demonstrate that cysteine protease RD21A is required for drought-induced immunity. Temporarily drought-treated wild-type Arabidopsis plants became more sensitive to the bacterial pathogen-associated molecular pattern flg22, triggering stomatal closure, which resulted in increased resistance to Pseudomonas syringae pv. tomato DC3000 (Pst-DC3000). Knocking out rd21a inhibited flg22-triggered stomatal closure and compromised the drought-induced immunity. Ubiquitin E3 ligase SINAT4 interacted with RD21A and promoted its degradation in vivo. The overexpression of SINAT4 also consistently compromised the drought-induced immunity to Pst-DC3000. A bacterial type III effector, AvrRxo1, interacted with both SINAT4 and RD21A, enhancing SINAT4 activity and promoting the degradation of RD21A in vivo. Therefore, RD21A could be a positive regulator of drought-induced immunity, which could be targeted by pathogen virulence effectors during pathogenesis.</description><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Cysteine Proteases - genetics</subject><subject>Droughts</subject><subject>Gene Expression Regulation, Plant</subject><subject>Plant Diseases</subject><subject>Pseudomonas syringae - metabolism</subject><subject>Ubiquitin-Protein Ligases - genetics</subject><issn>0022-0957</issn><issn>1460-2431</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kMtOwzAQRS0EgvJYsUdesUEBP2mzrEqBShUgHutoYk-CURsHO5HIF_DbGBVYshpp7tHVzCHkmLNzznJ58fZRXmAAEFpvkRFXlywTSvJtMmJMiIzlerxH9mN8Y4xppvUu2ZNCaTnhYkQ-Z0Ps0DVI2-A7hIj08UrwKQ1Y9yvo0NJyoHNJV67-Dp8Wd9NnRV1MwHvvQsorH6gNvq9fu8w1tjdpFzC62EFjkHaePkTsrV_7BiKNQ3BNDUhdQ6cBSmd9m9hDslPBKuLRzzwgL9fz59lttry_Wcymy8xIPe4yBSDR2jKfAEMuOTJTmVworEqm5KW2UGmcqHQCpA-5mYyNMMBRQIkKSi0PyNmm1wQfY8CqaINbQxgKzopvnUXSWfzoTPTJhm77co32j_31l4DTDeD79t-mL5gVgcU</recordid><startdate>20200919</startdate><enddate>20200919</enddate><creator>Liu, Yi</creator><creator>Wang, Kunru</creator><creator>Cheng, Qiang</creator><creator>Kong, Danyu</creator><creator>Zhang, Xunzhong</creator><creator>Wang, Zhibo</creator><creator>Wang, Qian</creator><creator>Xie, Qi</creator><creator>Yan, Jijun</creator><creator>Chu, Jinfang</creator><creator>Ling, Hong-Qing</creator><creator>Li, Qi</creator><creator>Miao, Jiamin</creator><creator>Zhao, Bingyu</creator><general>Oxford University Press</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></search><sort><creationdate>20200919</creationdate><title>Cysteine protease RD21A regulated by E3 ligase SINAT4 is required for drought-induced resistance to Pseudomonas syringae in Arabidopsis</title><author>Liu, Yi ; Wang, Kunru ; Cheng, Qiang ; Kong, Danyu ; Zhang, Xunzhong ; Wang, Zhibo ; Wang, Qian ; Xie, Qi ; Yan, Jijun ; Chu, Jinfang ; Ling, Hong-Qing ; Li, Qi ; Miao, Jiamin ; Zhao, Bingyu</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c357t-4aa3eddb98a0e131e0cfc924efb04365daf5e84ceda4531c87c2ca1e2abe4ab53</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Arabidopsis - genetics</topic><topic>Arabidopsis - metabolism</topic><topic>Arabidopsis Proteins - genetics</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>Cysteine Proteases - genetics</topic><topic>Droughts</topic><topic>Gene Expression Regulation, Plant</topic><topic>Plant Diseases</topic><topic>Pseudomonas syringae - metabolism</topic><topic>Ubiquitin-Protein Ligases - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Liu, Yi</creatorcontrib><creatorcontrib>Wang, Kunru</creatorcontrib><creatorcontrib>Cheng, Qiang</creatorcontrib><creatorcontrib>Kong, Danyu</creatorcontrib><creatorcontrib>Zhang, Xunzhong</creatorcontrib><creatorcontrib>Wang, Zhibo</creatorcontrib><creatorcontrib>Wang, Qian</creatorcontrib><creatorcontrib>Xie, Qi</creatorcontrib><creatorcontrib>Yan, Jijun</creatorcontrib><creatorcontrib>Chu, Jinfang</creatorcontrib><creatorcontrib>Ling, Hong-Qing</creatorcontrib><creatorcontrib>Li, Qi</creatorcontrib><creatorcontrib>Miao, Jiamin</creatorcontrib><creatorcontrib>Zhao, Bingyu</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><jtitle>Journal of experimental botany</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Liu, Yi</au><au>Wang, Kunru</au><au>Cheng, Qiang</au><au>Kong, Danyu</au><au>Zhang, Xunzhong</au><au>Wang, Zhibo</au><au>Wang, Qian</au><au>Xie, Qi</au><au>Yan, Jijun</au><au>Chu, Jinfang</au><au>Ling, Hong-Qing</au><au>Li, Qi</au><au>Miao, Jiamin</au><au>Zhao, Bingyu</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Cysteine protease RD21A regulated by E3 ligase SINAT4 is required for drought-induced resistance to Pseudomonas syringae in Arabidopsis</atitle><jtitle>Journal of experimental botany</jtitle><addtitle>J Exp Bot</addtitle><date>2020-09-19</date><risdate>2020</risdate><volume>71</volume><issue>18</issue><spage>5562</spage><epage>5576</epage><pages>5562-5576</pages><issn>0022-0957</issn><eissn>1460-2431</eissn><abstract>Abstract Plants can be simultaneously exposed to multiple stresses. The interplay of abiotic and biotic stresses may result in synergistic or antagonistic effects on plant development and health. Temporary drought stress can stimulate plant immunity; however, the molecular mechanism of drought-induced immunity is largely unknown. In this study, we demonstrate that cysteine protease RD21A is required for drought-induced immunity. Temporarily drought-treated wild-type Arabidopsis plants became more sensitive to the bacterial pathogen-associated molecular pattern flg22, triggering stomatal closure, which resulted in increased resistance to Pseudomonas syringae pv. tomato DC3000 (Pst-DC3000). Knocking out rd21a inhibited flg22-triggered stomatal closure and compromised the drought-induced immunity. Ubiquitin E3 ligase SINAT4 interacted with RD21A and promoted its degradation in vivo. The overexpression of SINAT4 also consistently compromised the drought-induced immunity to Pst-DC3000. A bacterial type III effector, AvrRxo1, interacted with both SINAT4 and RD21A, enhancing SINAT4 activity and promoting the degradation of RD21A in vivo. Therefore, RD21A could be a positive regulator of drought-induced immunity, which could be targeted by pathogen virulence effectors during pathogenesis.</abstract><cop>UK</cop><pub>Oxford University Press</pub><pmid>32453812</pmid><doi>10.1093/jxb/eraa255</doi><tpages>15</tpages><oa>free_for_read</oa></addata></record>
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subjects Arabidopsis - genetics
Arabidopsis - metabolism
Arabidopsis Proteins - genetics
Arabidopsis Proteins - metabolism
Cysteine Proteases - genetics
Droughts
Gene Expression Regulation, Plant
Plant Diseases
Pseudomonas syringae - metabolism
Ubiquitin-Protein Ligases - genetics
title Cysteine protease RD21A regulated by E3 ligase SINAT4 is required for drought-induced resistance to Pseudomonas syringae in Arabidopsis
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