A new adenylyl cyclase, putative disease-resistance RPP13-like protein 3, participates in abscisic acid-mediated resistance to heat stress in maize
ZmRPP13-LK3 is a newly identified adenylyl cyclase in maize that participates in ABA-mediated resistance to heat stress. Abstract In plants, 3´,5´-cyclic adenosine monophosphate (cAMP) is an important second messenger with varied functions; however, only a few adenylyl cyclases (ACs) that synthesiz...
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Veröffentlicht in: | Journal of experimental botany 2021-02, Vol.72 (2), p.283-301 |
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creator | Yang, Hao Zhao, Yulong Chen, Ning Liu, Yanpei Yang, Shaoyu Du, Hanwei Wang, Wei Wu, Jianyu Tai, Fuju Chen, Feng Hu, Xiuli |
description | ZmRPP13-LK3 is a newly identified adenylyl cyclase in maize that participates in ABA-mediated resistance to heat stress.
Abstract
In plants, 3´,5´-cyclic adenosine monophosphate (cAMP) is an important second messenger with varied functions; however, only a few adenylyl cyclases (ACs) that synthesize cAMP have been identified. Moreover, the biological roles of ACs/cAMP in response to stress remain largely unclear. In this study, we used quantitative proteomics techniques to identify a maize heat-induced putative disease-resistance RPP13-like protein 3 (ZmRPP13-LK3), which has three conserved catalytic AC centres. The AC activity of ZmRPP13-LK3 was confirmed by in vitro enzyme activity analysis, in vivo RNAi experiments, and functional complementation in the E. coli cyaA mutant. ZmRPP13-LK3 is located in the mitochondria. The results of in vitro and in vivo experiments indicated that ZmRPP13-LK3 interacts with ZmABC2, a possible cAMP exporter. Under heat stress, the concentrations of ZmRPP13-LK3 and cAMP in the ABA-deficient mutant vp5 were significantly less than those in the wild-type, and treatment with ABA and an ABA inhibitor affected ZmRPP13-LK3 expression in the wild-type. Application of 8-Br-cAMP, a cAMP analogue, increased heat-induced expression of heat-shock proteins in wild-type plants and alleviated heat-activated oxidative stress. Taken together, our results indicate that ZmRPP13-LK3, a new AC, can catalyse ATP for the production of cAMP and may be involved in ABA-regulated heat resistance. |
doi_str_mv | 10.1093/jxb/eraa431 |
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Abstract
In plants, 3´,5´-cyclic adenosine monophosphate (cAMP) is an important second messenger with varied functions; however, only a few adenylyl cyclases (ACs) that synthesize cAMP have been identified. Moreover, the biological roles of ACs/cAMP in response to stress remain largely unclear. In this study, we used quantitative proteomics techniques to identify a maize heat-induced putative disease-resistance RPP13-like protein 3 (ZmRPP13-LK3), which has three conserved catalytic AC centres. The AC activity of ZmRPP13-LK3 was confirmed by in vitro enzyme activity analysis, in vivo RNAi experiments, and functional complementation in the E. coli cyaA mutant. ZmRPP13-LK3 is located in the mitochondria. The results of in vitro and in vivo experiments indicated that ZmRPP13-LK3 interacts with ZmABC2, a possible cAMP exporter. Under heat stress, the concentrations of ZmRPP13-LK3 and cAMP in the ABA-deficient mutant vp5 were significantly less than those in the wild-type, and treatment with ABA and an ABA inhibitor affected ZmRPP13-LK3 expression in the wild-type. Application of 8-Br-cAMP, a cAMP analogue, increased heat-induced expression of heat-shock proteins in wild-type plants and alleviated heat-activated oxidative stress. Taken together, our results indicate that ZmRPP13-LK3, a new AC, can catalyse ATP for the production of cAMP and may be involved in ABA-regulated heat resistance.</description><identifier>ISSN: 0022-0957</identifier><identifier>EISSN: 1460-2431</identifier><identifier>DOI: 10.1093/jxb/eraa431</identifier><identifier>PMID: 32936902</identifier><language>eng</language><publisher>UK: Oxford University Press</publisher><ispartof>Journal of experimental botany, 2021-02, Vol.72 (2), p.283-301</ispartof><rights>The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved. For permissions, please email: journals.permissions@oup.com 2020</rights><rights>The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved. For permissions, please email: journals.permissions@oup.com.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c320t-c786d0570141ec0bb951b532fe57293a8b2606c0dc5f4d69b756ff32bb514ea3</citedby><cites>FETCH-LOGICAL-c320t-c786d0570141ec0bb951b532fe57293a8b2606c0dc5f4d69b756ff32bb514ea3</cites><orcidid>0000-0002-3711-5181</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,776,780,27903,27904</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32936902$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Zhang, Jianhua</contributor><creatorcontrib>Yang, Hao</creatorcontrib><creatorcontrib>Zhao, Yulong</creatorcontrib><creatorcontrib>Chen, Ning</creatorcontrib><creatorcontrib>Liu, Yanpei</creatorcontrib><creatorcontrib>Yang, Shaoyu</creatorcontrib><creatorcontrib>Du, Hanwei</creatorcontrib><creatorcontrib>Wang, Wei</creatorcontrib><creatorcontrib>Wu, Jianyu</creatorcontrib><creatorcontrib>Tai, Fuju</creatorcontrib><creatorcontrib>Chen, Feng</creatorcontrib><creatorcontrib>Hu, Xiuli</creatorcontrib><title>A new adenylyl cyclase, putative disease-resistance RPP13-like protein 3, participates in abscisic acid-mediated resistance to heat stress in maize</title><title>Journal of experimental botany</title><addtitle>J Exp Bot</addtitle><description>ZmRPP13-LK3 is a newly identified adenylyl cyclase in maize that participates in ABA-mediated resistance to heat stress.
Abstract
In plants, 3´,5´-cyclic adenosine monophosphate (cAMP) is an important second messenger with varied functions; however, only a few adenylyl cyclases (ACs) that synthesize cAMP have been identified. Moreover, the biological roles of ACs/cAMP in response to stress remain largely unclear. In this study, we used quantitative proteomics techniques to identify a maize heat-induced putative disease-resistance RPP13-like protein 3 (ZmRPP13-LK3), which has three conserved catalytic AC centres. The AC activity of ZmRPP13-LK3 was confirmed by in vitro enzyme activity analysis, in vivo RNAi experiments, and functional complementation in the E. coli cyaA mutant. ZmRPP13-LK3 is located in the mitochondria. The results of in vitro and in vivo experiments indicated that ZmRPP13-LK3 interacts with ZmABC2, a possible cAMP exporter. Under heat stress, the concentrations of ZmRPP13-LK3 and cAMP in the ABA-deficient mutant vp5 were significantly less than those in the wild-type, and treatment with ABA and an ABA inhibitor affected ZmRPP13-LK3 expression in the wild-type. Application of 8-Br-cAMP, a cAMP analogue, increased heat-induced expression of heat-shock proteins in wild-type plants and alleviated heat-activated oxidative stress. Taken together, our results indicate that ZmRPP13-LK3, a new AC, can catalyse ATP for the production of cAMP and may be involved in ABA-regulated heat resistance.</description><issn>0022-0957</issn><issn>1460-2431</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><recordid>eNp9kU9P3DAQxa0K1N1ue-KOfEJINDC24_w5rlbQVloJVHGPxs5ENWSTEDuU5Wv0C-N2F9QTpxk9_-ZJz4-xIwHnAkp1cfdkLmhETJX4wOYizSCRcT9gcwApEyh1PmOfvL8DAA1af2QzJUuVlSDn7M-Sd_SbY03dtt223G5ti56-8mEKGNwj8dp5ikoyknc-YGeJ_7y5ESpp3T3xYewDuY6reIFjcNYNGMjzKKHx1nlnOVpXJxuqXXyp-X8-oee_CAP3IYr_bjbonukzO2yw9fRlPxfs9urydvU9WV9_-7FarhOrJITE5kVWg85BpIIsGFNqYbSSDek85sPCyAwyC7XVTVpnpcl11jRKGqNFSqgW7HRnGzM8TORDtXHeUttiR_3kK5mmqihEUaYRPduhduy9H6mphtFtcNxWAqq_JVSxhGpfQqSP98aTibHf2Ndfj8DJDuin4V2nF0CgklU</recordid><startdate>20210202</startdate><enddate>20210202</enddate><creator>Yang, Hao</creator><creator>Zhao, Yulong</creator><creator>Chen, Ning</creator><creator>Liu, Yanpei</creator><creator>Yang, Shaoyu</creator><creator>Du, Hanwei</creator><creator>Wang, Wei</creator><creator>Wu, Jianyu</creator><creator>Tai, Fuju</creator><creator>Chen, Feng</creator><creator>Hu, Xiuli</creator><general>Oxford University Press</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-3711-5181</orcidid></search><sort><creationdate>20210202</creationdate><title>A new adenylyl cyclase, putative disease-resistance RPP13-like protein 3, participates in abscisic acid-mediated resistance to heat stress in maize</title><author>Yang, Hao ; Zhao, Yulong ; Chen, Ning ; Liu, Yanpei ; Yang, Shaoyu ; Du, Hanwei ; Wang, Wei ; Wu, Jianyu ; Tai, Fuju ; Chen, Feng ; Hu, Xiuli</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c320t-c786d0570141ec0bb951b532fe57293a8b2606c0dc5f4d69b756ff32bb514ea3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Yang, Hao</creatorcontrib><creatorcontrib>Zhao, Yulong</creatorcontrib><creatorcontrib>Chen, Ning</creatorcontrib><creatorcontrib>Liu, Yanpei</creatorcontrib><creatorcontrib>Yang, Shaoyu</creatorcontrib><creatorcontrib>Du, Hanwei</creatorcontrib><creatorcontrib>Wang, Wei</creatorcontrib><creatorcontrib>Wu, Jianyu</creatorcontrib><creatorcontrib>Tai, Fuju</creatorcontrib><creatorcontrib>Chen, Feng</creatorcontrib><creatorcontrib>Hu, Xiuli</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Journal of experimental botany</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Yang, Hao</au><au>Zhao, Yulong</au><au>Chen, Ning</au><au>Liu, Yanpei</au><au>Yang, Shaoyu</au><au>Du, Hanwei</au><au>Wang, Wei</au><au>Wu, Jianyu</au><au>Tai, Fuju</au><au>Chen, Feng</au><au>Hu, Xiuli</au><au>Zhang, Jianhua</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A new adenylyl cyclase, putative disease-resistance RPP13-like protein 3, participates in abscisic acid-mediated resistance to heat stress in maize</atitle><jtitle>Journal of experimental botany</jtitle><addtitle>J Exp Bot</addtitle><date>2021-02-02</date><risdate>2021</risdate><volume>72</volume><issue>2</issue><spage>283</spage><epage>301</epage><pages>283-301</pages><issn>0022-0957</issn><eissn>1460-2431</eissn><abstract>ZmRPP13-LK3 is a newly identified adenylyl cyclase in maize that participates in ABA-mediated resistance to heat stress.
Abstract
In plants, 3´,5´-cyclic adenosine monophosphate (cAMP) is an important second messenger with varied functions; however, only a few adenylyl cyclases (ACs) that synthesize cAMP have been identified. Moreover, the biological roles of ACs/cAMP in response to stress remain largely unclear. In this study, we used quantitative proteomics techniques to identify a maize heat-induced putative disease-resistance RPP13-like protein 3 (ZmRPP13-LK3), which has three conserved catalytic AC centres. The AC activity of ZmRPP13-LK3 was confirmed by in vitro enzyme activity analysis, in vivo RNAi experiments, and functional complementation in the E. coli cyaA mutant. ZmRPP13-LK3 is located in the mitochondria. The results of in vitro and in vivo experiments indicated that ZmRPP13-LK3 interacts with ZmABC2, a possible cAMP exporter. Under heat stress, the concentrations of ZmRPP13-LK3 and cAMP in the ABA-deficient mutant vp5 were significantly less than those in the wild-type, and treatment with ABA and an ABA inhibitor affected ZmRPP13-LK3 expression in the wild-type. Application of 8-Br-cAMP, a cAMP analogue, increased heat-induced expression of heat-shock proteins in wild-type plants and alleviated heat-activated oxidative stress. Taken together, our results indicate that ZmRPP13-LK3, a new AC, can catalyse ATP for the production of cAMP and may be involved in ABA-regulated heat resistance.</abstract><cop>UK</cop><pub>Oxford University Press</pub><pmid>32936902</pmid><doi>10.1093/jxb/eraa431</doi><tpages>19</tpages><orcidid>https://orcid.org/0000-0002-3711-5181</orcidid></addata></record> |
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title | A new adenylyl cyclase, putative disease-resistance RPP13-like protein 3, participates in abscisic acid-mediated resistance to heat stress in maize |
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