The Coiled-Coil and Nucleotide Binding Domains of BROWN PLANTHOPPER RESISTANCE14 Function in Signaling and Resistance against Planthopper in Rice
BROWN PLANTHOPPER RESISTANCE14 (BPH14), the first planthopper resistance gene isolated via map-based cloning in rice (Oryza sativa), encodes a coiled-coil, nucleotide binding site, leucine-rich repeat (CC-NB-LRR) protein. Several planthopper and aphid resistance genes encoding proteins with similar...
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| Veröffentlicht in: | The Plant cell 2017-12, Vol.29 (12), p.3157-3185 |
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| creator | Hu, Liang Wu, Yan Wu, Di Rao, Weiwei Guo, Jianping Ma, Yinhua Wang, Zhizheng Shangguan, Xinxin Wang, Huiying Xu, Chunxue Huang, Jin Shi, Shaojie Chen, Rongzhi Du, Bo Zhu, Lili He, Guangcun |
| description | BROWN PLANTHOPPER RESISTANCE14 (BPH14), the first planthopper resistance gene isolated via map-based cloning in rice (Oryza sativa), encodes a coiled-coil, nucleotide binding site, leucine-rich repeat (CC-NB-LRR) protein. Several planthopper and aphid resistance genes encoding proteins with similar structures have recently been identified. Here, we analyzed the functions of the domains of BPH14 to identify molecular mechanisms underpinning BPH14-mediated planthopper resistance. The CC or NB domains alone or in combination (CC-NB [CN]) conferred a similar level of brown planthopper resistance to that of full-length (FL) BPH14. Both domains activated the salicylic acid signaling pathway and defense gene expression. In rice protoplasts and Nicotiana benthamiana leaves, these domains increased reactive oxygen species levels without triggering cell death. Additionally, the resistance domains and FL BPH14 protein formed homocomplexes that interacted with transcription factors WRKY46 and WRKY72. In rice protoplasts, the expression of FL BPH14 or its CC, NB, and CN domains increased the accumulation of WRKY46 and WRKY72 as well as WRKY46- and WRKY72-dependent transactivation activity. WRKY46 and WRKY72 bind to the promoters of the receptor-like cytoplasmic kinase gene RLCK281 and the callose synthase gene LOC_Os01g67364.1, whose transactivation activity is dependent on WRKY46 or WRKY72. These findings shed light on this important insect resistance mechanism. |
| doi_str_mv | 10.1105/tpc.17.00263 |
| format | Article |
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Several planthopper and aphid resistance genes encoding proteins with similar structures have recently been identified. Here, we analyzed the functions of the domains of BPH14 to identify molecular mechanisms underpinning BPH14-mediated planthopper resistance. The CC or NB domains alone or in combination (CC-NB [CN]) conferred a similar level of brown planthopper resistance to that of full-length (FL) BPH14. Both domains activated the salicylic acid signaling pathway and defense gene expression. In rice protoplasts and Nicotiana benthamiana leaves, these domains increased reactive oxygen species levels without triggering cell death. Additionally, the resistance domains and FL BPH14 protein formed homocomplexes that interacted with transcription factors WRKY46 and WRKY72. In rice protoplasts, the expression of FL BPH14 or its CC, NB, and CN domains increased the accumulation of WRKY46 and WRKY72 as well as WRKY46- and WRKY72-dependent transactivation activity. WRKY46 and WRKY72 bind to the promoters of the receptor-like cytoplasmic kinase gene RLCK281 and the callose synthase gene LOC_Os01g67364.1, whose transactivation activity is dependent on WRKY46 or WRKY72. These findings shed light on this important insect resistance mechanism.</description><identifier>ISSN: 1040-4651</identifier><identifier>ISSN: 1532-298X</identifier><identifier>EISSN: 1532-298X</identifier><identifier>DOI: 10.1105/tpc.17.00263</identifier><identifier>PMID: 29093216</identifier><language>eng</language><publisher>England: American Society of Plant Biologists</publisher><subject>Animals ; Binding sites ; Cell death ; Cell Death - drug effects ; Cell Nucleus - drug effects ; Cell Nucleus - metabolism ; Cloning ; Coils ; Disease Resistance ; Gene expression ; Hemiptera - physiology ; Kinases ; Leucine ; Magnaporthe - physiology ; Models, Biological ; Molecular modelling ; Oryza - genetics ; Oryza - immunology ; Oryza - metabolism ; Oryza - parasitology ; Oryza sativa ; Plant Diseases - microbiology ; Plant Diseases - parasitology ; Plant Growth Regulators - pharmacology ; Plant Proteins - chemistry ; Plant Proteins - metabolism ; Plants, Genetically Modified ; Protein Binding - drug effects ; Protein Domains ; Protein Stability - drug effects ; Proteins ; Proteolysis - drug effects ; Protoplasts ; Reactive oxygen species ; Rice ; Salicylic acid ; Salicylic Acid - metabolism ; Signal Transduction ; Signaling ; Structure-Activity Relationship ; Transcription factors ; Transcription Factors - metabolism ; Xanthomonas - physiology</subject><ispartof>The Plant cell, 2017-12, Vol.29 (12), p.3157-3185</ispartof><rights>2017 American Society of Plant Biologists</rights><rights>2017 American Society of Plant Biologists. All rights reserved.</rights><rights>Copyright American Society of Plant Biologists Dec 2017</rights><rights>2017 American Society of Plant Biologists. All rights reserved. 2017</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c434t-b2a2f4ec82661b5efb22dd85bfedb2786fb21a023dcc3f734fe7b5c62ddeebc03</citedby><orcidid>0000-0001-6395-4774</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/90017102$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/90017102$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,780,784,803,885,27924,27925,58017,58250</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29093216$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Hu, Liang</creatorcontrib><creatorcontrib>Wu, Yan</creatorcontrib><creatorcontrib>Wu, Di</creatorcontrib><creatorcontrib>Rao, Weiwei</creatorcontrib><creatorcontrib>Guo, Jianping</creatorcontrib><creatorcontrib>Ma, Yinhua</creatorcontrib><creatorcontrib>Wang, Zhizheng</creatorcontrib><creatorcontrib>Shangguan, Xinxin</creatorcontrib><creatorcontrib>Wang, Huiying</creatorcontrib><creatorcontrib>Xu, Chunxue</creatorcontrib><creatorcontrib>Huang, Jin</creatorcontrib><creatorcontrib>Shi, Shaojie</creatorcontrib><creatorcontrib>Chen, Rongzhi</creatorcontrib><creatorcontrib>Du, Bo</creatorcontrib><creatorcontrib>Zhu, Lili</creatorcontrib><creatorcontrib>He, Guangcun</creatorcontrib><title>The Coiled-Coil and Nucleotide Binding Domains of BROWN PLANTHOPPER RESISTANCE14 Function in Signaling and Resistance against Planthopper in Rice</title><title>The Plant cell</title><addtitle>Plant Cell</addtitle><description>BROWN PLANTHOPPER RESISTANCE14 (BPH14), the first planthopper resistance gene isolated via map-based cloning in rice (Oryza sativa), encodes a coiled-coil, nucleotide binding site, leucine-rich repeat (CC-NB-LRR) protein. Several planthopper and aphid resistance genes encoding proteins with similar structures have recently been identified. Here, we analyzed the functions of the domains of BPH14 to identify molecular mechanisms underpinning BPH14-mediated planthopper resistance. The CC or NB domains alone or in combination (CC-NB [CN]) conferred a similar level of brown planthopper resistance to that of full-length (FL) BPH14. Both domains activated the salicylic acid signaling pathway and defense gene expression. In rice protoplasts and Nicotiana benthamiana leaves, these domains increased reactive oxygen species levels without triggering cell death. Additionally, the resistance domains and FL BPH14 protein formed homocomplexes that interacted with transcription factors WRKY46 and WRKY72. In rice protoplasts, the expression of FL BPH14 or its CC, NB, and CN domains increased the accumulation of WRKY46 and WRKY72 as well as WRKY46- and WRKY72-dependent transactivation activity. WRKY46 and WRKY72 bind to the promoters of the receptor-like cytoplasmic kinase gene RLCK281 and the callose synthase gene LOC_Os01g67364.1, whose transactivation activity is dependent on WRKY46 or WRKY72. These findings shed light on this important insect resistance mechanism.</description><subject>Animals</subject><subject>Binding sites</subject><subject>Cell death</subject><subject>Cell Death - drug effects</subject><subject>Cell Nucleus - drug effects</subject><subject>Cell Nucleus - metabolism</subject><subject>Cloning</subject><subject>Coils</subject><subject>Disease Resistance</subject><subject>Gene expression</subject><subject>Hemiptera - physiology</subject><subject>Kinases</subject><subject>Leucine</subject><subject>Magnaporthe - physiology</subject><subject>Models, Biological</subject><subject>Molecular modelling</subject><subject>Oryza - genetics</subject><subject>Oryza - immunology</subject><subject>Oryza - metabolism</subject><subject>Oryza - parasitology</subject><subject>Oryza sativa</subject><subject>Plant Diseases - microbiology</subject><subject>Plant Diseases - parasitology</subject><subject>Plant Growth Regulators - pharmacology</subject><subject>Plant Proteins - chemistry</subject><subject>Plant Proteins - metabolism</subject><subject>Plants, Genetically Modified</subject><subject>Protein Binding - drug effects</subject><subject>Protein Domains</subject><subject>Protein Stability - drug effects</subject><subject>Proteins</subject><subject>Proteolysis - drug effects</subject><subject>Protoplasts</subject><subject>Reactive oxygen species</subject><subject>Rice</subject><subject>Salicylic acid</subject><subject>Salicylic Acid - metabolism</subject><subject>Signal Transduction</subject><subject>Signaling</subject><subject>Structure-Activity Relationship</subject><subject>Transcription factors</subject><subject>Transcription Factors - metabolism</subject><subject>Xanthomonas - physiology</subject><issn>1040-4651</issn><issn>1532-298X</issn><issn>1532-298X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkl9v0zAUxSMEYmPwxivIEi88LMV_4qR5mdSVjk2q2iotgjfLcW5aV6kdYgeJj8E3nrNuFePpWr4_H917jqPoPcEjQjD_4ls1ItkIY5qyF9E54YzGNB__fBnOOMFxknJyFr1xbo8xJhnJX0dnNMc5oyQ9j_5udoCmVjdQxUNB0lRo0asGrNcVoGttKm226Ks9SG0csjW6LpY_Fmg1nyw2t8vValagYra-W28mi-mMJOimN8pra5A2aK23RjbD-0G2AKedl0YBkttBzaNVI43f2baFbuALreBt9KqWjYN3j_Ui-n4z20xv4_ny2910Mo9VwhIfl1TSOgE1pmlKSg51SWlVjXlZQ1XSbJyGCyIxZZVSrM5YUkNWcpUGCKBUmF1EV0fdti8PUCkwvpONaDt9kN0fYaUWzztG78TW_hY84xlNsyDw-VGgs796cF4ctFPQhJXA9k6QnAeTKeM8oJ_-Q_e274I1TlCM0xwnST4IXh4p1VnnOqhPwxAshqxFyFqQTDxkHfCP_y5wgp_CDcCHI7B33nanfv7wDYIz9_-Fr0c</recordid><startdate>20171201</startdate><enddate>20171201</enddate><creator>Hu, Liang</creator><creator>Wu, Yan</creator><creator>Wu, Di</creator><creator>Rao, Weiwei</creator><creator>Guo, Jianping</creator><creator>Ma, Yinhua</creator><creator>Wang, Zhizheng</creator><creator>Shangguan, Xinxin</creator><creator>Wang, Huiying</creator><creator>Xu, Chunxue</creator><creator>Huang, Jin</creator><creator>Shi, Shaojie</creator><creator>Chen, Rongzhi</creator><creator>Du, Bo</creator><creator>Zhu, Lili</creator><creator>He, Guangcun</creator><general>American Society of Plant Biologists</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>4T-</scope><scope>7QO</scope><scope>7TM</scope><scope>8FD</scope><scope>FR3</scope><scope>K9.</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-6395-4774</orcidid></search><sort><creationdate>20171201</creationdate><title>The Coiled-Coil and Nucleotide Binding Domains of BROWN PLANTHOPPER RESISTANCE14 Function in Signaling and Resistance against Planthopper in Rice</title><author>Hu, Liang ; Wu, Yan ; Wu, Di ; Rao, Weiwei ; Guo, Jianping ; Ma, Yinhua ; Wang, Zhizheng ; Shangguan, Xinxin ; Wang, Huiying ; Xu, Chunxue ; Huang, Jin ; Shi, Shaojie ; Chen, Rongzhi ; Du, Bo ; Zhu, Lili ; He, Guangcun</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c434t-b2a2f4ec82661b5efb22dd85bfedb2786fb21a023dcc3f734fe7b5c62ddeebc03</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Animals</topic><topic>Binding sites</topic><topic>Cell death</topic><topic>Cell Death - drug effects</topic><topic>Cell Nucleus - drug effects</topic><topic>Cell Nucleus - metabolism</topic><topic>Cloning</topic><topic>Coils</topic><topic>Disease Resistance</topic><topic>Gene expression</topic><topic>Hemiptera - physiology</topic><topic>Kinases</topic><topic>Leucine</topic><topic>Magnaporthe - physiology</topic><topic>Models, Biological</topic><topic>Molecular modelling</topic><topic>Oryza - genetics</topic><topic>Oryza - immunology</topic><topic>Oryza - metabolism</topic><topic>Oryza - parasitology</topic><topic>Oryza sativa</topic><topic>Plant Diseases - microbiology</topic><topic>Plant Diseases - parasitology</topic><topic>Plant Growth Regulators - pharmacology</topic><topic>Plant Proteins - chemistry</topic><topic>Plant Proteins - metabolism</topic><topic>Plants, Genetically Modified</topic><topic>Protein Binding - drug effects</topic><topic>Protein Domains</topic><topic>Protein Stability - drug effects</topic><topic>Proteins</topic><topic>Proteolysis - drug effects</topic><topic>Protoplasts</topic><topic>Reactive oxygen species</topic><topic>Rice</topic><topic>Salicylic acid</topic><topic>Salicylic Acid - metabolism</topic><topic>Signal Transduction</topic><topic>Signaling</topic><topic>Structure-Activity Relationship</topic><topic>Transcription factors</topic><topic>Transcription Factors - metabolism</topic><topic>Xanthomonas - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Hu, Liang</creatorcontrib><creatorcontrib>Wu, Yan</creatorcontrib><creatorcontrib>Wu, Di</creatorcontrib><creatorcontrib>Rao, Weiwei</creatorcontrib><creatorcontrib>Guo, Jianping</creatorcontrib><creatorcontrib>Ma, Yinhua</creatorcontrib><creatorcontrib>Wang, Zhizheng</creatorcontrib><creatorcontrib>Shangguan, Xinxin</creatorcontrib><creatorcontrib>Wang, Huiying</creatorcontrib><creatorcontrib>Xu, Chunxue</creatorcontrib><creatorcontrib>Huang, Jin</creatorcontrib><creatorcontrib>Shi, Shaojie</creatorcontrib><creatorcontrib>Chen, Rongzhi</creatorcontrib><creatorcontrib>Du, Bo</creatorcontrib><creatorcontrib>Zhu, Lili</creatorcontrib><creatorcontrib>He, Guangcun</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Docstoc</collection><collection>Biotechnology Research Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Plant cell</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Hu, Liang</au><au>Wu, Yan</au><au>Wu, Di</au><au>Rao, Weiwei</au><au>Guo, Jianping</au><au>Ma, Yinhua</au><au>Wang, Zhizheng</au><au>Shangguan, Xinxin</au><au>Wang, Huiying</au><au>Xu, Chunxue</au><au>Huang, Jin</au><au>Shi, Shaojie</au><au>Chen, Rongzhi</au><au>Du, Bo</au><au>Zhu, Lili</au><au>He, Guangcun</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The Coiled-Coil and Nucleotide Binding Domains of BROWN PLANTHOPPER RESISTANCE14 Function in Signaling and Resistance against Planthopper in Rice</atitle><jtitle>The Plant cell</jtitle><addtitle>Plant Cell</addtitle><date>2017-12-01</date><risdate>2017</risdate><volume>29</volume><issue>12</issue><spage>3157</spage><epage>3185</epage><pages>3157-3185</pages><issn>1040-4651</issn><issn>1532-298X</issn><eissn>1532-298X</eissn><abstract>BROWN PLANTHOPPER RESISTANCE14 (BPH14), the first planthopper resistance gene isolated via map-based cloning in rice (Oryza sativa), encodes a coiled-coil, nucleotide binding site, leucine-rich repeat (CC-NB-LRR) protein. Several planthopper and aphid resistance genes encoding proteins with similar structures have recently been identified. Here, we analyzed the functions of the domains of BPH14 to identify molecular mechanisms underpinning BPH14-mediated planthopper resistance. The CC or NB domains alone or in combination (CC-NB [CN]) conferred a similar level of brown planthopper resistance to that of full-length (FL) BPH14. Both domains activated the salicylic acid signaling pathway and defense gene expression. In rice protoplasts and Nicotiana benthamiana leaves, these domains increased reactive oxygen species levels without triggering cell death. Additionally, the resistance domains and FL BPH14 protein formed homocomplexes that interacted with transcription factors WRKY46 and WRKY72. In rice protoplasts, the expression of FL BPH14 or its CC, NB, and CN domains increased the accumulation of WRKY46 and WRKY72 as well as WRKY46- and WRKY72-dependent transactivation activity. WRKY46 and WRKY72 bind to the promoters of the receptor-like cytoplasmic kinase gene RLCK281 and the callose synthase gene LOC_Os01g67364.1, whose transactivation activity is dependent on WRKY46 or WRKY72. These findings shed light on this important insect resistance mechanism.</abstract><cop>England</cop><pub>American Society of Plant Biologists</pub><pmid>29093216</pmid><doi>10.1105/tpc.17.00263</doi><tpages>29</tpages><orcidid>https://orcid.org/0000-0001-6395-4774</orcidid><oa>free_for_read</oa></addata></record> |
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| ispartof | The Plant cell, 2017-12, Vol.29 (12), p.3157-3185 |
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| source | MEDLINE; JSTOR Archive Collection A-Z Listing; Oxford University Press Journals All Titles (1996-Current); EZB-FREE-00999 freely available EZB journals |
| subjects | Animals Binding sites Cell death Cell Death - drug effects Cell Nucleus - drug effects Cell Nucleus - metabolism Cloning Coils Disease Resistance Gene expression Hemiptera - physiology Kinases Leucine Magnaporthe - physiology Models, Biological Molecular modelling Oryza - genetics Oryza - immunology Oryza - metabolism Oryza - parasitology Oryza sativa Plant Diseases - microbiology Plant Diseases - parasitology Plant Growth Regulators - pharmacology Plant Proteins - chemistry Plant Proteins - metabolism Plants, Genetically Modified Protein Binding - drug effects Protein Domains Protein Stability - drug effects Proteins Proteolysis - drug effects Protoplasts Reactive oxygen species Rice Salicylic acid Salicylic Acid - metabolism Signal Transduction Signaling Structure-Activity Relationship Transcription factors Transcription Factors - metabolism Xanthomonas - physiology |
| title | The Coiled-Coil and Nucleotide Binding Domains of BROWN PLANTHOPPER RESISTANCE14 Function in Signaling and Resistance against Planthopper in Rice |
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