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Microsymbiont discrimination mediated by a host-secreted peptide in Medicago truncatula
The legume–rhizobial symbiosis results in the formation of root nodules that provide an ecological niche for nitrogen-fixing bacteria. However, plant–bacteria genotypic interactions can lead to wide variation in nitrogen fixation efficiency, and it is not uncommon that a bacterial strain forms funct...
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Published in: | Proceedings of the National Academy of Sciences - PNAS 2017-06, Vol.114 (26), p.6848-6853 |
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creator | Yang, Shengming Wang, Qi Fedorova, Elena Liu, Jinge Qin, Qiulin Zheng, Qiaolin Price, Paul A. Pan, Huairong Wang, Dong Griffitts, Joel S. Bisseling, Ton Zhu, Hongyan |
description | The legume–rhizobial symbiosis results in the formation of root nodules that provide an ecological niche for nitrogen-fixing bacteria. However, plant–bacteria genotypic interactions can lead to wide variation in nitrogen fixation efficiency, and it is not uncommon that a bacterial strain forms functional (Fix⁺) nodules on one plant genotype but nonfunctional (Fix⁻) nodules on another. Host genetic control of this specificity is unknown. We herein report the cloning of the Medicago truncatula NFS1 gene that regulates the fixation-level incompatibility with the microsymbiont Sinorhizobium meliloti Rm41. We show that NFS1 encodes a nodulespecific cysteine-rich (NCR) peptide. In contrast to the known role of NCR peptides as effectors of endosymbionts’ differentiation to nitrogen-fixing bacteroids, we demonstrate that specific NCRs control discrimination against incompatible microsymbionts. NFS1 provokes bacterial cell death and early nodule senescence in an allele-specific and rhizobial strain-specific manner, and its function is dependent on host genetic background. |
doi_str_mv | 10.1073/pnas.1700460114 |
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However, plant–bacteria genotypic interactions can lead to wide variation in nitrogen fixation efficiency, and it is not uncommon that a bacterial strain forms functional (Fix⁺) nodules on one plant genotype but nonfunctional (Fix⁻) nodules on another. Host genetic control of this specificity is unknown. We herein report the cloning of the Medicago truncatula NFS1 gene that regulates the fixation-level incompatibility with the microsymbiont Sinorhizobium meliloti Rm41. We show that NFS1 encodes a nodulespecific cysteine-rich (NCR) peptide. In contrast to the known role of NCR peptides as effectors of endosymbionts’ differentiation to nitrogen-fixing bacteroids, we demonstrate that specific NCRs control discrimination against incompatible microsymbionts. NFS1 provokes bacterial cell death and early nodule senescence in an allele-specific and rhizobial strain-specific manner, and its function is dependent on host genetic background.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.1700460114</identifier><identifier>PMID: 28607056</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Alfalfa ; Apoptosis ; Bacteria ; Bacteroids ; Biological Sciences ; Cell death ; Cloning ; Differentiation ; Discrimination ; Ecological effects ; Ecological niches ; Endosymbionts ; EPS ; Genetic control ; Host plants ; Incompatibility ; Laboratorium voor Moleculaire biologie ; Laboratory of Molecular Biology ; Legumes ; Medicago truncatula ; Nitrogen ; Nitrogen fixation ; Nitrogen-fixing bacteria ; Nodules ; Peptides ; Root nodules ; Senescence ; Sinorhizobium meliloti ; Symbiosis</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2017-06, Vol.114 (26), p.6848-6853</ispartof><rights>Volumes 1–89 and 106–114, copyright as a collective work only; author(s) retains copyright to individual articles</rights><rights>Copyright National Academy of Sciences Jun 27, 2017</rights><rights>Wageningen University & Research</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c494t-120b93b191103867410e13401104870b7b4cca3f1a5a0510b6f4c3493e8bdbd23</citedby><cites>FETCH-LOGICAL-c494t-120b93b191103867410e13401104870b7b4cca3f1a5a0510b6f4c3493e8bdbd23</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/26484997$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/26484997$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793,58238,58471</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28607056$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Yang, Shengming</creatorcontrib><creatorcontrib>Wang, Qi</creatorcontrib><creatorcontrib>Fedorova, Elena</creatorcontrib><creatorcontrib>Liu, Jinge</creatorcontrib><creatorcontrib>Qin, Qiulin</creatorcontrib><creatorcontrib>Zheng, Qiaolin</creatorcontrib><creatorcontrib>Price, Paul A.</creatorcontrib><creatorcontrib>Pan, Huairong</creatorcontrib><creatorcontrib>Wang, Dong</creatorcontrib><creatorcontrib>Griffitts, Joel S.</creatorcontrib><creatorcontrib>Bisseling, Ton</creatorcontrib><creatorcontrib>Zhu, Hongyan</creatorcontrib><title>Microsymbiont discrimination mediated by a host-secreted peptide in Medicago truncatula</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>The legume–rhizobial symbiosis results in the formation of root nodules that provide an ecological niche for nitrogen-fixing bacteria. However, plant–bacteria genotypic interactions can lead to wide variation in nitrogen fixation efficiency, and it is not uncommon that a bacterial strain forms functional (Fix⁺) nodules on one plant genotype but nonfunctional (Fix⁻) nodules on another. Host genetic control of this specificity is unknown. We herein report the cloning of the Medicago truncatula NFS1 gene that regulates the fixation-level incompatibility with the microsymbiont Sinorhizobium meliloti Rm41. We show that NFS1 encodes a nodulespecific cysteine-rich (NCR) peptide. In contrast to the known role of NCR peptides as effectors of endosymbionts’ differentiation to nitrogen-fixing bacteroids, we demonstrate that specific NCRs control discrimination against incompatible microsymbionts. NFS1 provokes bacterial cell death and early nodule senescence in an allele-specific and rhizobial strain-specific manner, and its function is dependent on host genetic background.</description><subject>Alfalfa</subject><subject>Apoptosis</subject><subject>Bacteria</subject><subject>Bacteroids</subject><subject>Biological Sciences</subject><subject>Cell death</subject><subject>Cloning</subject><subject>Differentiation</subject><subject>Discrimination</subject><subject>Ecological effects</subject><subject>Ecological niches</subject><subject>Endosymbionts</subject><subject>EPS</subject><subject>Genetic control</subject><subject>Host plants</subject><subject>Incompatibility</subject><subject>Laboratorium voor Moleculaire biologie</subject><subject>Laboratory of Molecular Biology</subject><subject>Legumes</subject><subject>Medicago truncatula</subject><subject>Nitrogen</subject><subject>Nitrogen fixation</subject><subject>Nitrogen-fixing bacteria</subject><subject>Nodules</subject><subject>Peptides</subject><subject>Root nodules</subject><subject>Senescence</subject><subject>Sinorhizobium meliloti</subject><subject>Symbiosis</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><recordid>eNpdkU1v1DAQhi0EokvhzAkUiQuXtON44sQcKqGKj0qteiniaNmOd-tV1g62Q7X_HkdbWsrFI4-feT0zLyFvKZxQ6Njp5FU6oR0AcqAUn5EVBUFrjgKekxVA09U9NnhEXqW0BQDR9vCSHDU9hw5aviI_r5yJIe132gWfq8ElE93OeZXLvdrZwalsh0rvK1XdhpTrZE20S2qyU3aDrZyvrgpm1CZUOc7eqDyP6jV5sVZjsm_u4zH58fXLzfn3-vL628X558vaoMBc0wa0YJoKSoH1vEMKljIsswD2HehOozGKralqFbQUNF-jYSiY7fWgh4Ydk08H3Tu1sd75ckivonFJBuXk6HRUcS_v5ij9uIRp1km2DRMgSvHZobgky6jG-hzVKKeygaVoEXj64t2t3ITfskXRNghF4OO9QAy_Zpuy3JUF2nFU3oY5SVp-KRxveUE__Iduwxx92U2hkCMVLV86Oj1Qiykp2vVDMxTk4rhcHJePjpeK9__O8MD_tbgA7w7ANuUQH9859ihEx_4AYLazHw</recordid><startdate>20170627</startdate><enddate>20170627</enddate><creator>Yang, Shengming</creator><creator>Wang, Qi</creator><creator>Fedorova, Elena</creator><creator>Liu, Jinge</creator><creator>Qin, Qiulin</creator><creator>Zheng, Qiaolin</creator><creator>Price, Paul A.</creator><creator>Pan, Huairong</creator><creator>Wang, Dong</creator><creator>Griffitts, Joel S.</creator><creator>Bisseling, Ton</creator><creator>Zhu, Hongyan</creator><general>National Academy of Sciences</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>QVL</scope></search><sort><creationdate>20170627</creationdate><title>Microsymbiont discrimination mediated by a host-secreted peptide in Medicago truncatula</title><author>Yang, Shengming ; 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However, plant–bacteria genotypic interactions can lead to wide variation in nitrogen fixation efficiency, and it is not uncommon that a bacterial strain forms functional (Fix⁺) nodules on one plant genotype but nonfunctional (Fix⁻) nodules on another. Host genetic control of this specificity is unknown. We herein report the cloning of the Medicago truncatula NFS1 gene that regulates the fixation-level incompatibility with the microsymbiont Sinorhizobium meliloti Rm41. We show that NFS1 encodes a nodulespecific cysteine-rich (NCR) peptide. In contrast to the known role of NCR peptides as effectors of endosymbionts’ differentiation to nitrogen-fixing bacteroids, we demonstrate that specific NCRs control discrimination against incompatible microsymbionts. NFS1 provokes bacterial cell death and early nodule senescence in an allele-specific and rhizobial strain-specific manner, and its function is dependent on host genetic background.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>28607056</pmid><doi>10.1073/pnas.1700460114</doi><tpages>6</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Alfalfa Apoptosis Bacteria Bacteroids Biological Sciences Cell death Cloning Differentiation Discrimination Ecological effects Ecological niches Endosymbionts EPS Genetic control Host plants Incompatibility Laboratorium voor Moleculaire biologie Laboratory of Molecular Biology Legumes Medicago truncatula Nitrogen Nitrogen fixation Nitrogen-fixing bacteria Nodules Peptides Root nodules Senescence Sinorhizobium meliloti Symbiosis |
title | Microsymbiont discrimination mediated by a host-secreted peptide in Medicago truncatula |
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