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The hnRNP-Q protein LIF2 participates in the plant immune response
Eukaryotes have evolved complex defense pathways to combat invading pathogens. Here, we investigated the role of the Arabidopsis thaliana heterogeneous nuclear ribonucleoprotein (hnRNP-Q) LIF2 in the plant innate immune response. We show that LIF2 loss-of-function in A. thaliana leads to changes in...
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Published in: | PloS one 2014-06, Vol.9 (6), p.e99343-e99343 |
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description | Eukaryotes have evolved complex defense pathways to combat invading pathogens. Here, we investigated the role of the Arabidopsis thaliana heterogeneous nuclear ribonucleoprotein (hnRNP-Q) LIF2 in the plant innate immune response. We show that LIF2 loss-of-function in A. thaliana leads to changes in the basal expression of the salicylic acid (SA)- and jasmonic acid (JA)- dependent defense marker genes PR1 and PDF1.2, respectively. Whereas the expression of genes involved in SA and JA biosynthesis and signaling was also affected in the lif2-1 mutant, no change in SA and JA hormonal contents was detected. In addition, the composition of glucosinolates, a class of defense-related secondary metabolites, was altered in the lif2-1 mutant in the absence of pathogen challenge. The lif2-1 mutant exhibited reduced susceptibility to the hemi-biotrophic pathogen Pseudomonas syringae and the necrotrophic ascomycete Botrytis cinerea. Furthermore, the lif2-1 sid2-2 double mutant was less susceptible than the wild type to P. syringae infection, suggesting that the lif2 response to pathogens was independent of SA accumulation. Together, our data suggest that lif2-1 exhibits a basal primed defense state, resulting from complex deregulation of gene expression, which leads to increased resistance to pathogens with various infection strategies. Therefore, LIF2 may function as a suppressor of cell-autonomous immunity. Similar to its human homolog, NSAP1/SYNCRIP, a trans-acting factor involved in both cellular processes and the viral life cycle, LIF2 may regulate the conflicting aspects of development and defense programs, suggesting that a conserved evolutionary trade-off between growth and defense pathways exists in eukaryotes. |
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Here, we investigated the role of the Arabidopsis thaliana heterogeneous nuclear ribonucleoprotein (hnRNP-Q) LIF2 in the plant innate immune response. We show that LIF2 loss-of-function in A. thaliana leads to changes in the basal expression of the salicylic acid (SA)- and jasmonic acid (JA)- dependent defense marker genes PR1 and PDF1.2, respectively. Whereas the expression of genes involved in SA and JA biosynthesis and signaling was also affected in the lif2-1 mutant, no change in SA and JA hormonal contents was detected. In addition, the composition of glucosinolates, a class of defense-related secondary metabolites, was altered in the lif2-1 mutant in the absence of pathogen challenge. The lif2-1 mutant exhibited reduced susceptibility to the hemi-biotrophic pathogen Pseudomonas syringae and the necrotrophic ascomycete Botrytis cinerea. Furthermore, the lif2-1 sid2-2 double mutant was less susceptible than the wild type to P. syringae infection, suggesting that the lif2 response to pathogens was independent of SA accumulation. Together, our data suggest that lif2-1 exhibits a basal primed defense state, resulting from complex deregulation of gene expression, which leads to increased resistance to pathogens with various infection strategies. Therefore, LIF2 may function as a suppressor of cell-autonomous immunity. Similar to its human homolog, NSAP1/SYNCRIP, a trans-acting factor involved in both cellular processes and the viral life cycle, LIF2 may regulate the conflicting aspects of development and defense programs, suggesting that a conserved evolutionary trade-off between growth and defense pathways exists in eukaryotes.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0099343</identifier><identifier>PMID: 24914891</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Acids ; Arabidopsis ; Arabidopsis - genetics ; Arabidopsis - immunology ; Arabidopsis - metabolism ; Arabidopsis - microbiology ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; Arabidopsis thaliana ; Biology and Life Sciences ; Biosynthesis ; Botrytis ; Botrytis cinerea ; Cyclopentanes - metabolism ; Defense programs ; Deregulation ; Epigenetics ; Eukaryotes ; Gene expression ; Gene Expression Regulation, Plant ; Gene Ontology ; Genes ; Glucosinolates ; Glucosinolates - metabolism ; Health aspects ; Heterogeneous-Nuclear Ribonucleoproteins - genetics ; Heterogeneous-Nuclear Ribonucleoproteins - metabolism ; Homology ; Immune response ; Immune system ; Immunity ; Infections ; Innate immunity ; Jasmonic acid ; Life cycle engineering ; Life cycles ; Life Sciences ; Metabolites ; Models, Biological ; Mutants ; Mutation ; Mutation - genetics ; Oxylipins - metabolism ; Pathogens ; Pathways ; Physiological aspects ; Plant Diseases - genetics ; Plant Diseases - microbiology ; Plant immunity ; Plant Immunity - genetics ; Proteins ; Pseudomonas syringae ; Pseudomonas syringae - physiology ; RNA-Binding Proteins - genetics ; RNA-Binding Proteins - metabolism ; Salicylic acid ; Salicylic Acid - metabolism ; Secondary metabolites ; Signal Transduction - genetics ; Signaling ; Stress response ; Stress, Physiological - genetics ; Studies ; Transcriptome - genetics</subject><ispartof>PloS one, 2014-06, Vol.9 (6), p.e99343-e99343</ispartof><rights>COPYRIGHT 2014 Public Library of Science</rights><rights>2014 Le Roux et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><rights>2014 Le Roux et al 2014 Le Roux et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c726t-59eaf8d6de2f60ec5c0a93d658c4048b4741405a0aa13ad3ff8a1c791b52c0753</citedby><cites>FETCH-LOGICAL-c726t-59eaf8d6de2f60ec5c0a93d658c4048b4741405a0aa13ad3ff8a1c791b52c0753</cites><orcidid>0000-0001-7452-6337 ; 0000-0002-1356-5567 ; 0000-0001-7873-9866</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/1534520888/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/1534520888?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25753,27924,27925,37012,37013,44590,53791,53793,75126</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24914891$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-01204050$$DView record in HAL$$Hfree_for_read</backlink></links><search><contributor>Zhang, Xiaoyu</contributor><creatorcontrib>Le Roux, Clémentine</creatorcontrib><creatorcontrib>Del Prete, Stefania</creatorcontrib><creatorcontrib>Boutet-Mercey, Stéphanie</creatorcontrib><creatorcontrib>Perreau, François</creatorcontrib><creatorcontrib>Balagué, Claudine</creatorcontrib><creatorcontrib>Roby, Dominique</creatorcontrib><creatorcontrib>Fagard, Mathilde</creatorcontrib><creatorcontrib>Gaudin, Valérie</creatorcontrib><title>The hnRNP-Q protein LIF2 participates in the plant immune response</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Eukaryotes have evolved complex defense pathways to combat invading pathogens. Here, we investigated the role of the Arabidopsis thaliana heterogeneous nuclear ribonucleoprotein (hnRNP-Q) LIF2 in the plant innate immune response. We show that LIF2 loss-of-function in A. thaliana leads to changes in the basal expression of the salicylic acid (SA)- and jasmonic acid (JA)- dependent defense marker genes PR1 and PDF1.2, respectively. Whereas the expression of genes involved in SA and JA biosynthesis and signaling was also affected in the lif2-1 mutant, no change in SA and JA hormonal contents was detected. In addition, the composition of glucosinolates, a class of defense-related secondary metabolites, was altered in the lif2-1 mutant in the absence of pathogen challenge. The lif2-1 mutant exhibited reduced susceptibility to the hemi-biotrophic pathogen Pseudomonas syringae and the necrotrophic ascomycete Botrytis cinerea. Furthermore, the lif2-1 sid2-2 double mutant was less susceptible than the wild type to P. syringae infection, suggesting that the lif2 response to pathogens was independent of SA accumulation. Together, our data suggest that lif2-1 exhibits a basal primed defense state, resulting from complex deregulation of gene expression, which leads to increased resistance to pathogens with various infection strategies. Therefore, LIF2 may function as a suppressor of cell-autonomous immunity. Similar to its human homolog, NSAP1/SYNCRIP, a trans-acting factor involved in both cellular processes and the viral life cycle, LIF2 may regulate the conflicting aspects of development and defense programs, suggesting that a conserved evolutionary trade-off between growth and defense pathways exists in eukaryotes.</description><subject>Acids</subject><subject>Arabidopsis</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - immunology</subject><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis - microbiology</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Arabidopsis thaliana</subject><subject>Biology and Life Sciences</subject><subject>Biosynthesis</subject><subject>Botrytis</subject><subject>Botrytis cinerea</subject><subject>Cyclopentanes - metabolism</subject><subject>Defense programs</subject><subject>Deregulation</subject><subject>Epigenetics</subject><subject>Eukaryotes</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Plant</subject><subject>Gene Ontology</subject><subject>Genes</subject><subject>Glucosinolates</subject><subject>Glucosinolates - metabolism</subject><subject>Health aspects</subject><subject>Heterogeneous-Nuclear Ribonucleoproteins - genetics</subject><subject>Heterogeneous-Nuclear Ribonucleoproteins - metabolism</subject><subject>Homology</subject><subject>Immune response</subject><subject>Immune system</subject><subject>Immunity</subject><subject>Infections</subject><subject>Innate immunity</subject><subject>Jasmonic acid</subject><subject>Life cycle engineering</subject><subject>Life cycles</subject><subject>Life Sciences</subject><subject>Metabolites</subject><subject>Models, Biological</subject><subject>Mutants</subject><subject>Mutation</subject><subject>Mutation - genetics</subject><subject>Oxylipins - metabolism</subject><subject>Pathogens</subject><subject>Pathways</subject><subject>Physiological aspects</subject><subject>Plant Diseases - genetics</subject><subject>Plant Diseases - microbiology</subject><subject>Plant immunity</subject><subject>Plant Immunity - genetics</subject><subject>Proteins</subject><subject>Pseudomonas syringae</subject><subject>Pseudomonas syringae - physiology</subject><subject>RNA-Binding Proteins - genetics</subject><subject>RNA-Binding Proteins - metabolism</subject><subject>Salicylic acid</subject><subject>Salicylic Acid - metabolism</subject><subject>Secondary metabolites</subject><subject>Signal Transduction - genetics</subject><subject>Signaling</subject><subject>Stress response</subject><subject>Stress, Physiological - genetics</subject><subject>Studies</subject><subject>Transcriptome - genetics</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNqNk11v0zAUhiMEYmPwDxBEQkLsIsXfcW4mlYmxShWDMbi1XMdpXCVxsJ0J_j1um03NtAuUi0THz_uej_gkyWsIZhDn8OPGDq6Tzay3nZ4BUBSY4CfJMSwwyhgC-OnB91HywvsNABRzxp4nR4gUkPACHiefbmqd1t3112_Z97R3NmjTpcvFBUp76YJRppdB-zQGQwT7RnYhNW07dDp12sfcXr9MnlWy8frV-D5Jfl58vjm_zJZXXxbn82WmcsRCRgstK16yUqOKAa2oArLAJaNcEUD4iuQEEkAlkBJiWeKq4hKqvIArihTIKT5J3u59-8Z6MbbvBaSYUAQ455FY7InSyo3onWml-yusNGIXsG4tdk01WjBQlpDTUhaAklhYTEUQpKykQHKWg-h1NmYbVq0ule6Ck83EdHrSmVqs7a2IPUC2K_d0b1A_kF3Ol2IbAxCBCINbGNkPYzJnfw_aB9Ear3QTx63tsOuRMkQhIhF99wB9fBIjtZaxWdNVNtaotqZiTiBnmEYoUrNHqPiUujUq3qvKxPhEcDoRRCboP2EtB-_F4sf1_7NXv6bs-wO21rIJtbfNEEy8YFOQ7EHlrPdOV_eThUBs1-JuGmK7FmJciyh7c_gz70V3e4D_AcrXBFM</recordid><startdate>20140610</startdate><enddate>20140610</enddate><creator>Le Roux, Clémentine</creator><creator>Del Prete, Stefania</creator><creator>Boutet-Mercey, Stéphanie</creator><creator>Perreau, François</creator><creator>Balagué, Claudine</creator><creator>Roby, Dominique</creator><creator>Fagard, Mathilde</creator><creator>Gaudin, Valérie</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>1XC</scope><scope>VOOES</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0001-7452-6337</orcidid><orcidid>https://orcid.org/0000-0002-1356-5567</orcidid><orcidid>https://orcid.org/0000-0001-7873-9866</orcidid></search><sort><creationdate>20140610</creationdate><title>The hnRNP-Q protein LIF2 participates in the plant immune response</title><author>Le Roux, Clémentine ; Del Prete, Stefania ; Boutet-Mercey, Stéphanie ; Perreau, François ; Balagué, Claudine ; Roby, Dominique ; Fagard, Mathilde ; Gaudin, Valérie</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c726t-59eaf8d6de2f60ec5c0a93d658c4048b4741405a0aa13ad3ff8a1c791b52c0753</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Acids</topic><topic>Arabidopsis</topic><topic>Arabidopsis - 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Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Le Roux, Clémentine</au><au>Del Prete, Stefania</au><au>Boutet-Mercey, Stéphanie</au><au>Perreau, François</au><au>Balagué, Claudine</au><au>Roby, Dominique</au><au>Fagard, Mathilde</au><au>Gaudin, Valérie</au><au>Zhang, Xiaoyu</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The hnRNP-Q protein LIF2 participates in the plant immune response</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2014-06-10</date><risdate>2014</risdate><volume>9</volume><issue>6</issue><spage>e99343</spage><epage>e99343</epage><pages>e99343-e99343</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Eukaryotes have evolved complex defense pathways to combat invading pathogens. Here, we investigated the role of the Arabidopsis thaliana heterogeneous nuclear ribonucleoprotein (hnRNP-Q) LIF2 in the plant innate immune response. We show that LIF2 loss-of-function in A. thaliana leads to changes in the basal expression of the salicylic acid (SA)- and jasmonic acid (JA)- dependent defense marker genes PR1 and PDF1.2, respectively. Whereas the expression of genes involved in SA and JA biosynthesis and signaling was also affected in the lif2-1 mutant, no change in SA and JA hormonal contents was detected. In addition, the composition of glucosinolates, a class of defense-related secondary metabolites, was altered in the lif2-1 mutant in the absence of pathogen challenge. The lif2-1 mutant exhibited reduced susceptibility to the hemi-biotrophic pathogen Pseudomonas syringae and the necrotrophic ascomycete Botrytis cinerea. Furthermore, the lif2-1 sid2-2 double mutant was less susceptible than the wild type to P. syringae infection, suggesting that the lif2 response to pathogens was independent of SA accumulation. Together, our data suggest that lif2-1 exhibits a basal primed defense state, resulting from complex deregulation of gene expression, which leads to increased resistance to pathogens with various infection strategies. Therefore, LIF2 may function as a suppressor of cell-autonomous immunity. Similar to its human homolog, NSAP1/SYNCRIP, a trans-acting factor involved in both cellular processes and the viral life cycle, LIF2 may regulate the conflicting aspects of development and defense programs, suggesting that a conserved evolutionary trade-off between growth and defense pathways exists in eukaryotes.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>24914891</pmid><doi>10.1371/journal.pone.0099343</doi><orcidid>https://orcid.org/0000-0001-7452-6337</orcidid><orcidid>https://orcid.org/0000-0002-1356-5567</orcidid><orcidid>https://orcid.org/0000-0001-7873-9866</orcidid><oa>free_for_read</oa></addata></record> |
fulltext | fulltext |
identifier | ISSN: 1932-6203 |
ispartof | PloS one, 2014-06, Vol.9 (6), p.e99343-e99343 |
issn | 1932-6203 1932-6203 |
language | eng |
recordid | cdi_plos_journals_1534520888 |
source | Publicly Available Content Database; PubMed Central |
subjects | Acids Arabidopsis Arabidopsis - genetics Arabidopsis - immunology Arabidopsis - metabolism Arabidopsis - microbiology Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism Arabidopsis thaliana Biology and Life Sciences Biosynthesis Botrytis Botrytis cinerea Cyclopentanes - metabolism Defense programs Deregulation Epigenetics Eukaryotes Gene expression Gene Expression Regulation, Plant Gene Ontology Genes Glucosinolates Glucosinolates - metabolism Health aspects Heterogeneous-Nuclear Ribonucleoproteins - genetics Heterogeneous-Nuclear Ribonucleoproteins - metabolism Homology Immune response Immune system Immunity Infections Innate immunity Jasmonic acid Life cycle engineering Life cycles Life Sciences Metabolites Models, Biological Mutants Mutation Mutation - genetics Oxylipins - metabolism Pathogens Pathways Physiological aspects Plant Diseases - genetics Plant Diseases - microbiology Plant immunity Plant Immunity - genetics Proteins Pseudomonas syringae Pseudomonas syringae - physiology RNA-Binding Proteins - genetics RNA-Binding Proteins - metabolism Salicylic acid Salicylic Acid - metabolism Secondary metabolites Signal Transduction - genetics Signaling Stress response Stress, Physiological - genetics Studies Transcriptome - genetics |
title | The hnRNP-Q protein LIF2 participates in the plant immune response |
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