Laccase GhLac1 Modulates Broad-Spectrum Biotic Stress Tolerance via Manipulating Phenylpropanoid Pathway and Jasmonic Acid Synthesis
Plants are constantly challenged by a multitude of pathogens and pests, which causes massive yield and quality losses annually. A promising approach to reduce such losses is to enhance the immune system of plants through genetic engineering. Previous work has shown that laccases (p-diphenol:dioxygen...
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Veröffentlicht in: | Plant physiology (Bethesda) 2018-02, Vol.176 (2), p.1808-1823 |
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creator | Hu, Qin Min, Ling Yang, Xiyan Jin, Shuangxia Zhang, Lin Li, Yaoyao Ma, Yizan Qi, Xuewei Li, Dongqin Liu, Hongbo Lindsey, Keith Zhu, Longfu Zhang, Xianlong |
description | Plants are constantly challenged by a multitude of pathogens and pests, which causes massive yield and quality losses annually. A promising approach to reduce such losses is to enhance the immune system of plants through genetic engineering. Previous work has shown that laccases (p-diphenol:dioxygen oxidoreductase, EC 1.10.3.2) function as lignin polymerization enzymes. Here we demonstrate that transgenic manipulation of the expression of the laccase gene GhLac1 in cotton (Gossypium hirsutum) can confer an enhanced defense response to both pathogens and pests. Overexpression of GhLac1 leads to increased lignification, associated with increased tolerance to the fungal pathogen Verticillium dahliae and to the insect pests cotton bollworm (Helicoverpa armigera) and cotton aphid (Aphis gosypii). Suppression of GhLac1 expression leads to a redirection of metabolic flux in the phenylpropanoid pathway, causing the accumulation of JA and secondary metabolites that confer resistance to V. dahliae and cotton bollworm; it also leads to increased susceptibility to cotton aphid. Plant laccases therefore provide a new molecular tool to engineer pest and pathogen resistance in crops. |
doi_str_mv | 10.1104/pp.17.01628 |
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A promising approach to reduce such losses is to enhance the immune system of plants through genetic engineering. Previous work has shown that laccases (p-diphenol:dioxygen oxidoreductase, EC 1.10.3.2) function as lignin polymerization enzymes. Here we demonstrate that transgenic manipulation of the expression of the laccase gene GhLac1 in cotton (Gossypium hirsutum) can confer an enhanced defense response to both pathogens and pests. Overexpression of GhLac1 leads to increased lignification, associated with increased tolerance to the fungal pathogen Verticillium dahliae and to the insect pests cotton bollworm (Helicoverpa armigera) and cotton aphid (Aphis gosypii). Suppression of GhLac1 expression leads to a redirection of metabolic flux in the phenylpropanoid pathway, causing the accumulation of JA and secondary metabolites that confer resistance to V. dahliae and cotton bollworm; it also leads to increased susceptibility to cotton aphid. Plant laccases therefore provide a new molecular tool to engineer pest and pathogen resistance in crops.</description><identifier>ISSN: 0032-0889</identifier><identifier>EISSN: 1532-2548</identifier><identifier>DOI: 10.1104/pp.17.01628</identifier><identifier>PMID: 29229698</identifier><language>eng</language><publisher>United States: American Society of Plant Biologists</publisher><subject>Animals ; Aphids - physiology ; Cyclopentanes - metabolism ; Disease Resistance ; Gene Expression Regulation, Plant ; Gossypium - enzymology ; Gossypium - genetics ; Gossypium - immunology ; Laccase - genetics ; Laccase - metabolism ; Lepidoptera - physiology ; Lignin - metabolism ; Oxylipins - metabolism ; Plant Diseases - immunology ; Plant Diseases - microbiology ; Plant Diseases - parasitology ; Plant Proteins - genetics ; Plant Proteins - metabolism ; Propanols - metabolism ; SIGNALING AND RESPONSE ; Verticillium - physiology</subject><ispartof>Plant physiology (Bethesda), 2018-02, Vol.176 (2), p.1808-1823</ispartof><rights>2018 American Society of Plant Biologists</rights><rights>2018 American Society of Plant Biologists. All Rights Reserved.</rights><rights>2018 American Society of Plant Biologists. All Rights Reserved. 2018</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c403t-f879c1309cb4c8d3ae18ac0b82f1335e496fdd199e448a3cbdf960ae25af22683</citedby><orcidid>0000-0002-7703-524X ; 0000-0003-3890-135X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/26377868$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/26377868$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,780,784,803,885,27923,27924,58016,58249</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29229698$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Hu, Qin</creatorcontrib><creatorcontrib>Min, Ling</creatorcontrib><creatorcontrib>Yang, Xiyan</creatorcontrib><creatorcontrib>Jin, Shuangxia</creatorcontrib><creatorcontrib>Zhang, Lin</creatorcontrib><creatorcontrib>Li, Yaoyao</creatorcontrib><creatorcontrib>Ma, Yizan</creatorcontrib><creatorcontrib>Qi, Xuewei</creatorcontrib><creatorcontrib>Li, Dongqin</creatorcontrib><creatorcontrib>Liu, Hongbo</creatorcontrib><creatorcontrib>Lindsey, Keith</creatorcontrib><creatorcontrib>Zhu, Longfu</creatorcontrib><creatorcontrib>Zhang, Xianlong</creatorcontrib><title>Laccase GhLac1 Modulates Broad-Spectrum Biotic Stress Tolerance via Manipulating Phenylpropanoid Pathway and Jasmonic Acid Synthesis</title><title>Plant physiology (Bethesda)</title><addtitle>Plant Physiol</addtitle><description>Plants are constantly challenged by a multitude of pathogens and pests, which causes massive yield and quality losses annually. A promising approach to reduce such losses is to enhance the immune system of plants through genetic engineering. Previous work has shown that laccases (p-diphenol:dioxygen oxidoreductase, EC 1.10.3.2) function as lignin polymerization enzymes. Here we demonstrate that transgenic manipulation of the expression of the laccase gene GhLac1 in cotton (Gossypium hirsutum) can confer an enhanced defense response to both pathogens and pests. Overexpression of GhLac1 leads to increased lignification, associated with increased tolerance to the fungal pathogen Verticillium dahliae and to the insect pests cotton bollworm (Helicoverpa armigera) and cotton aphid (Aphis gosypii). Suppression of GhLac1 expression leads to a redirection of metabolic flux in the phenylpropanoid pathway, causing the accumulation of JA and secondary metabolites that confer resistance to V. dahliae and cotton bollworm; it also leads to increased susceptibility to cotton aphid. Plant laccases therefore provide a new molecular tool to engineer pest and pathogen resistance in crops.</description><subject>Animals</subject><subject>Aphids - physiology</subject><subject>Cyclopentanes - metabolism</subject><subject>Disease Resistance</subject><subject>Gene Expression Regulation, Plant</subject><subject>Gossypium - enzymology</subject><subject>Gossypium - genetics</subject><subject>Gossypium - immunology</subject><subject>Laccase - genetics</subject><subject>Laccase - metabolism</subject><subject>Lepidoptera - physiology</subject><subject>Lignin - metabolism</subject><subject>Oxylipins - metabolism</subject><subject>Plant Diseases - immunology</subject><subject>Plant Diseases - microbiology</subject><subject>Plant Diseases - parasitology</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - metabolism</subject><subject>Propanols - metabolism</subject><subject>SIGNALING AND RESPONSE</subject><subject>Verticillium - physiology</subject><issn>0032-0889</issn><issn>1532-2548</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVkc1v1DAQxS0EokvhxBnkIxLK4q8k9gWpraCAtqLSlrM16ziNq8Q2tlO0d_5wUrYUOM1I7zdvZvQQeknJmlIi3sW4pu2a0IbJR2hFa84qVgv5GK0IWXoipTpCz3K-IYRQTsVTdMQUY6pRcoV-bsAYyBafD0tH8UXo5hGKzfg0BeiqbbSmpHnCpy4UZ_C2JJszvgqjTeCNxbcO8AV4F-_GnL_Gl4P1-zGmEMEH1-FLKMMP2GPwHf4CeQp-sTkxi7Ld-zLY7PJz9KSHMdsX9_UYffv44ersU7X5ev757GRTGUF4qXrZKkM5UWYnjOw4WCrBkJ1kPeW8tkI1fddRpawQErjZdb1qCFhWQ89YI_kxen_wjfNusp2xviQYdUxugrTXAZz-X_Fu0NfhVteS8rquF4M39wYpfJ9tLnpy2dhxBG_DnDVVbUNIK4hY0LcH1KSQc7L9wxpK9F1uOkZNW_07t4V-_e9lD-yfoBbg1QG4ySWkv3rD21Yur_0CKBmgbQ</recordid><startdate>20180201</startdate><enddate>20180201</enddate><creator>Hu, Qin</creator><creator>Min, Ling</creator><creator>Yang, Xiyan</creator><creator>Jin, Shuangxia</creator><creator>Zhang, Lin</creator><creator>Li, Yaoyao</creator><creator>Ma, Yizan</creator><creator>Qi, Xuewei</creator><creator>Li, Dongqin</creator><creator>Liu, Hongbo</creator><creator>Lindsey, Keith</creator><creator>Zhu, Longfu</creator><creator>Zhang, Xianlong</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>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-7703-524X</orcidid><orcidid>https://orcid.org/0000-0003-3890-135X</orcidid></search><sort><creationdate>20180201</creationdate><title>Laccase GhLac1 Modulates Broad-Spectrum Biotic Stress Tolerance via Manipulating Phenylpropanoid Pathway and Jasmonic Acid Synthesis</title><author>Hu, Qin ; Min, Ling ; Yang, Xiyan ; Jin, Shuangxia ; Zhang, Lin ; Li, Yaoyao ; Ma, Yizan ; Qi, Xuewei ; Li, Dongqin ; Liu, Hongbo ; Lindsey, Keith ; Zhu, Longfu ; Zhang, Xianlong</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c403t-f879c1309cb4c8d3ae18ac0b82f1335e496fdd199e448a3cbdf960ae25af22683</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Animals</topic><topic>Aphids - physiology</topic><topic>Cyclopentanes - metabolism</topic><topic>Disease Resistance</topic><topic>Gene Expression Regulation, Plant</topic><topic>Gossypium - enzymology</topic><topic>Gossypium - genetics</topic><topic>Gossypium - immunology</topic><topic>Laccase - genetics</topic><topic>Laccase - metabolism</topic><topic>Lepidoptera - physiology</topic><topic>Lignin - metabolism</topic><topic>Oxylipins - metabolism</topic><topic>Plant Diseases - immunology</topic><topic>Plant Diseases - microbiology</topic><topic>Plant Diseases - parasitology</topic><topic>Plant Proteins - genetics</topic><topic>Plant Proteins - metabolism</topic><topic>Propanols - metabolism</topic><topic>SIGNALING AND RESPONSE</topic><topic>Verticillium - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Hu, Qin</creatorcontrib><creatorcontrib>Min, Ling</creatorcontrib><creatorcontrib>Yang, Xiyan</creatorcontrib><creatorcontrib>Jin, Shuangxia</creatorcontrib><creatorcontrib>Zhang, Lin</creatorcontrib><creatorcontrib>Li, Yaoyao</creatorcontrib><creatorcontrib>Ma, Yizan</creatorcontrib><creatorcontrib>Qi, Xuewei</creatorcontrib><creatorcontrib>Li, Dongqin</creatorcontrib><creatorcontrib>Liu, Hongbo</creatorcontrib><creatorcontrib>Lindsey, Keith</creatorcontrib><creatorcontrib>Zhu, Longfu</creatorcontrib><creatorcontrib>Zhang, Xianlong</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>PubMed Central (Full Participant titles)</collection><jtitle>Plant physiology (Bethesda)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Hu, Qin</au><au>Min, Ling</au><au>Yang, Xiyan</au><au>Jin, Shuangxia</au><au>Zhang, Lin</au><au>Li, Yaoyao</au><au>Ma, Yizan</au><au>Qi, Xuewei</au><au>Li, Dongqin</au><au>Liu, Hongbo</au><au>Lindsey, Keith</au><au>Zhu, Longfu</au><au>Zhang, Xianlong</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Laccase GhLac1 Modulates Broad-Spectrum Biotic Stress Tolerance via Manipulating Phenylpropanoid Pathway and Jasmonic Acid Synthesis</atitle><jtitle>Plant physiology (Bethesda)</jtitle><addtitle>Plant Physiol</addtitle><date>2018-02-01</date><risdate>2018</risdate><volume>176</volume><issue>2</issue><spage>1808</spage><epage>1823</epage><pages>1808-1823</pages><issn>0032-0889</issn><eissn>1532-2548</eissn><abstract>Plants are constantly challenged by a multitude of pathogens and pests, which causes massive yield and quality losses annually. A promising approach to reduce such losses is to enhance the immune system of plants through genetic engineering. Previous work has shown that laccases (p-diphenol:dioxygen oxidoreductase, EC 1.10.3.2) function as lignin polymerization enzymes. Here we demonstrate that transgenic manipulation of the expression of the laccase gene GhLac1 in cotton (Gossypium hirsutum) can confer an enhanced defense response to both pathogens and pests. Overexpression of GhLac1 leads to increased lignification, associated with increased tolerance to the fungal pathogen Verticillium dahliae and to the insect pests cotton bollworm (Helicoverpa armigera) and cotton aphid (Aphis gosypii). Suppression of GhLac1 expression leads to a redirection of metabolic flux in the phenylpropanoid pathway, causing the accumulation of JA and secondary metabolites that confer resistance to V. dahliae and cotton bollworm; it also leads to increased susceptibility to cotton aphid. Plant laccases therefore provide a new molecular tool to engineer pest and pathogen resistance in crops.</abstract><cop>United States</cop><pub>American Society of Plant Biologists</pub><pmid>29229698</pmid><doi>10.1104/pp.17.01628</doi><tpages>16</tpages><orcidid>https://orcid.org/0000-0002-7703-524X</orcidid><orcidid>https://orcid.org/0000-0003-3890-135X</orcidid><oa>free_for_read</oa></addata></record> |
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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 Aphids - physiology Cyclopentanes - metabolism Disease Resistance Gene Expression Regulation, Plant Gossypium - enzymology Gossypium - genetics Gossypium - immunology Laccase - genetics Laccase - metabolism Lepidoptera - physiology Lignin - metabolism Oxylipins - metabolism Plant Diseases - immunology Plant Diseases - microbiology Plant Diseases - parasitology Plant Proteins - genetics Plant Proteins - metabolism Propanols - metabolism SIGNALING AND RESPONSE Verticillium - physiology |
title | Laccase GhLac1 Modulates Broad-Spectrum Biotic Stress Tolerance via Manipulating Phenylpropanoid Pathway and Jasmonic Acid Synthesis |
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