Two members of a Nodule‐specific Cysteine‐Rich (NCR) peptide gene cluster are required for differentiation of rhizobia in Medicago truncatula nodules
SUMMARY Legumes have evolved a nitrogen‐fixing symbiotic interaction with rhizobia, and this association helps them to cope with the limited nitrogen conditions in soil. The compatible interaction between the host plant and rhizobia leads to the formation of root nodules, wherein internalization and...
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Veröffentlicht in: | The Plant journal : for cell and molecular biology 2024-08, Vol.119 (3), p.1508-1525 |
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creator | Saifi, Farheen Biró, János Barnabás Horváth, Beatrix Vizler, Csaba Laczi, Krisztián Rákhely, Gábor Kovács, Szilárd Kang, Mingming Li, Dengyao Chen, Yuhui Chen, Rujin Domonkos, Ágota Kaló, Péter |
description | SUMMARY
Legumes have evolved a nitrogen‐fixing symbiotic interaction with rhizobia, and this association helps them to cope with the limited nitrogen conditions in soil. The compatible interaction between the host plant and rhizobia leads to the formation of root nodules, wherein internalization and transition of rhizobia into their symbiotic form, termed bacteroids, occur. Rhizobia in the nodules of the Inverted Repeat‐Lacking Clade legumes, including Medicago truncatula, undergo terminal differentiation, resulting in elongated and endoreduplicated bacteroids. This transition of endocytosed rhizobia is mediated by a large gene family of host‐produced nodule‐specific cysteine‐rich (NCR) peptides in M. truncatula. Few NCRs have been recently found to be essential for complete differentiation and persistence of bacteroids. Here, we show that a M. truncatula symbiotic mutant FN9285, defective in the complete transition of rhizobia, is deficient in a cluster of NCR genes. More specifically, we show that the loss of the duplicated genes NCR086 and NCR314 in the A17 genotype, found in a single copy in Medicago littoralis R108, is responsible for the ineffective symbiotic phenotype of FN9285. The NCR086 and NCR314 gene pair encodes the same mature peptide but their transcriptional activity varies considerably. Nevertheless, both genes can restore the effective symbiosis in FN9285 indicating that their complementation ability does not depend on the strength of their expression activity. The identification of the NCR086/NCR314 peptide, essential for complete bacteroid differentiation, has extended the list of peptides, from a gene family of several hundred members, that are essential for effective nitrogen‐fixing symbiosis in M. truncatula.
Significance Statement
Our results demonstrate the requirement of NCR086/NCR314, which are members of the nodule‐specific cysteine‐rich peptide family, for effective symbiotic interaction between Medicago truncatula and the tested rhizobia strains. The NCR086/NCR314 peptides are encoded by a highly similar gene pair in M. truncatula A17 that was duplicated following the separation of lines M. truncatula A17 and Medicago littoralis R108. |
doi_str_mv | 10.1111/tpj.16871 |
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Legumes have evolved a nitrogen‐fixing symbiotic interaction with rhizobia, and this association helps them to cope with the limited nitrogen conditions in soil. The compatible interaction between the host plant and rhizobia leads to the formation of root nodules, wherein internalization and transition of rhizobia into their symbiotic form, termed bacteroids, occur. Rhizobia in the nodules of the Inverted Repeat‐Lacking Clade legumes, including Medicago truncatula, undergo terminal differentiation, resulting in elongated and endoreduplicated bacteroids. This transition of endocytosed rhizobia is mediated by a large gene family of host‐produced nodule‐specific cysteine‐rich (NCR) peptides in M. truncatula. Few NCRs have been recently found to be essential for complete differentiation and persistence of bacteroids. Here, we show that a M. truncatula symbiotic mutant FN9285, defective in the complete transition of rhizobia, is deficient in a cluster of NCR genes. More specifically, we show that the loss of the duplicated genes NCR086 and NCR314 in the A17 genotype, found in a single copy in Medicago littoralis R108, is responsible for the ineffective symbiotic phenotype of FN9285. The NCR086 and NCR314 gene pair encodes the same mature peptide but their transcriptional activity varies considerably. Nevertheless, both genes can restore the effective symbiosis in FN9285 indicating that their complementation ability does not depend on the strength of their expression activity. The identification of the NCR086/NCR314 peptide, essential for complete bacteroid differentiation, has extended the list of peptides, from a gene family of several hundred members, that are essential for effective nitrogen‐fixing symbiosis in M. truncatula.
Significance Statement
Our results demonstrate the requirement of NCR086/NCR314, which are members of the nodule‐specific cysteine‐rich peptide family, for effective symbiotic interaction between Medicago truncatula and the tested rhizobia strains. The NCR086/NCR314 peptides are encoded by a highly similar gene pair in M. truncatula A17 that was duplicated following the separation of lines M. truncatula A17 and Medicago littoralis R108.</description><identifier>ISSN: 0960-7412</identifier><identifier>ISSN: 1365-313X</identifier><identifier>EISSN: 1365-313X</identifier><identifier>DOI: 10.1111/tpj.16871</identifier><identifier>PMID: 38923649</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Alfalfa ; Bacteroids ; Complementation ; Cysteine ; Cysteine - metabolism ; Differentiation ; family ; Fixing ; Gene duplication ; Gene expression ; Gene Expression Regulation, Plant ; Genes ; genotype ; Genotypes ; Host plants ; indeterminate nodule ; Internalization ; Inverted repeat ; Legumes ; Medicago littoralis ; Medicago truncatula ; Medicago truncatula - genetics ; Medicago truncatula - microbiology ; Medicago truncatula - physiology ; Multigene Family ; mutants ; Nitrogen ; nitrogen fixation ; Nitrogen Fixation - genetics ; nitrogen‐fixing symbiosis ; Nodules ; nodule‐specific cysteine‐rich peptides ; Peptides ; Peptides - genetics ; Peptides - metabolism ; phenotype ; Phenotypes ; Plant Proteins - genetics ; Plant Proteins - metabolism ; Rhizobium - genetics ; Rhizobium - physiology ; Root nodules ; Root Nodules, Plant - genetics ; Root Nodules, Plant - microbiology ; Sinorhizobium meliloti - genetics ; Sinorhizobium meliloti - physiology ; soil ; Soil microorganisms ; Symbiosis ; Symbiosis - genetics ; terminal differentiation ; transcription (genetics)</subject><ispartof>The Plant journal : for cell and molecular biology, 2024-08, Vol.119 (3), p.1508-1525</ispartof><rights>2024 The Author(s). published by Society for Experimental Biology and John Wiley & Sons Ltd.</rights><rights>2024 The Author(s). The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd.</rights><rights>2024. This article is published under http://creativecommons.org/licenses/by-nc-nd/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c3111-27aa1c0e59e55274b09d84b6602da4eef1200c846dc10872ae77950d824ca43f3</cites><orcidid>0000-0002-6912-8227 ; 0000-0001-5444-2144 ; 0000-0001-8851-0387 ; 0000-0003-4017-0605 ; 0000-0001-8499-568X ; 0000-0002-0404-8904 ; 0009-0005-2750-8845</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Ftpj.16871$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Ftpj.16871$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>314,776,780,1411,27901,27902,45550,45551</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38923649$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Saifi, Farheen</creatorcontrib><creatorcontrib>Biró, János Barnabás</creatorcontrib><creatorcontrib>Horváth, Beatrix</creatorcontrib><creatorcontrib>Vizler, Csaba</creatorcontrib><creatorcontrib>Laczi, Krisztián</creatorcontrib><creatorcontrib>Rákhely, Gábor</creatorcontrib><creatorcontrib>Kovács, Szilárd</creatorcontrib><creatorcontrib>Kang, Mingming</creatorcontrib><creatorcontrib>Li, Dengyao</creatorcontrib><creatorcontrib>Chen, Yuhui</creatorcontrib><creatorcontrib>Chen, Rujin</creatorcontrib><creatorcontrib>Domonkos, Ágota</creatorcontrib><creatorcontrib>Kaló, Péter</creatorcontrib><title>Two members of a Nodule‐specific Cysteine‐Rich (NCR) peptide gene cluster are required for differentiation of rhizobia in Medicago truncatula nodules</title><title>The Plant journal : for cell and molecular biology</title><addtitle>Plant J</addtitle><description>SUMMARY
Legumes have evolved a nitrogen‐fixing symbiotic interaction with rhizobia, and this association helps them to cope with the limited nitrogen conditions in soil. The compatible interaction between the host plant and rhizobia leads to the formation of root nodules, wherein internalization and transition of rhizobia into their symbiotic form, termed bacteroids, occur. Rhizobia in the nodules of the Inverted Repeat‐Lacking Clade legumes, including Medicago truncatula, undergo terminal differentiation, resulting in elongated and endoreduplicated bacteroids. This transition of endocytosed rhizobia is mediated by a large gene family of host‐produced nodule‐specific cysteine‐rich (NCR) peptides in M. truncatula. Few NCRs have been recently found to be essential for complete differentiation and persistence of bacteroids. Here, we show that a M. truncatula symbiotic mutant FN9285, defective in the complete transition of rhizobia, is deficient in a cluster of NCR genes. More specifically, we show that the loss of the duplicated genes NCR086 and NCR314 in the A17 genotype, found in a single copy in Medicago littoralis R108, is responsible for the ineffective symbiotic phenotype of FN9285. The NCR086 and NCR314 gene pair encodes the same mature peptide but their transcriptional activity varies considerably. Nevertheless, both genes can restore the effective symbiosis in FN9285 indicating that their complementation ability does not depend on the strength of their expression activity. The identification of the NCR086/NCR314 peptide, essential for complete bacteroid differentiation, has extended the list of peptides, from a gene family of several hundred members, that are essential for effective nitrogen‐fixing symbiosis in M. truncatula.
Significance Statement
Our results demonstrate the requirement of NCR086/NCR314, which are members of the nodule‐specific cysteine‐rich peptide family, for effective symbiotic interaction between Medicago truncatula and the tested rhizobia strains. The NCR086/NCR314 peptides are encoded by a highly similar gene pair in M. truncatula A17 that was duplicated following the separation of lines M. truncatula A17 and Medicago littoralis R108.</description><subject>Alfalfa</subject><subject>Bacteroids</subject><subject>Complementation</subject><subject>Cysteine</subject><subject>Cysteine - metabolism</subject><subject>Differentiation</subject><subject>family</subject><subject>Fixing</subject><subject>Gene duplication</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Plant</subject><subject>Genes</subject><subject>genotype</subject><subject>Genotypes</subject><subject>Host plants</subject><subject>indeterminate nodule</subject><subject>Internalization</subject><subject>Inverted repeat</subject><subject>Legumes</subject><subject>Medicago littoralis</subject><subject>Medicago truncatula</subject><subject>Medicago truncatula - genetics</subject><subject>Medicago truncatula - microbiology</subject><subject>Medicago truncatula - physiology</subject><subject>Multigene Family</subject><subject>mutants</subject><subject>Nitrogen</subject><subject>nitrogen fixation</subject><subject>Nitrogen Fixation - genetics</subject><subject>nitrogen‐fixing symbiosis</subject><subject>Nodules</subject><subject>nodule‐specific cysteine‐rich peptides</subject><subject>Peptides</subject><subject>Peptides - genetics</subject><subject>Peptides - metabolism</subject><subject>phenotype</subject><subject>Phenotypes</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - metabolism</subject><subject>Rhizobium - genetics</subject><subject>Rhizobium - physiology</subject><subject>Root nodules</subject><subject>Root Nodules, Plant - genetics</subject><subject>Root Nodules, Plant - microbiology</subject><subject>Sinorhizobium meliloti - genetics</subject><subject>Sinorhizobium meliloti - physiology</subject><subject>soil</subject><subject>Soil microorganisms</subject><subject>Symbiosis</subject><subject>Symbiosis - genetics</subject><subject>terminal differentiation</subject><subject>transcription (genetics)</subject><issn>0960-7412</issn><issn>1365-313X</issn><issn>1365-313X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>EIF</sourceid><recordid>eNqFkctq3DAUhkVpaKZpF32BIugmWTjRxbbsZRnSG0lawhS6M7J0lGiwJUeyCNNVH6Hbvl6fpJpMkkWh9IA4Qnx8R4cfoVeUHNNcJ_O0PqZ1I-gTtKC8rgpO-benaEHamhSipGwfPY9xTQgVvC6foX3etCzf2gX6tbr1eISxhxCxN1jiC6_TAL9__IwTKGuswstNnMG67dulVdf48GJ5eYQnmGarAV-BA6yGlJmAZQAc4CbZABobH7C2xkAAN1s5W--2I8K1_e57K7F1-By0VfLK4zkkp-ScBond3QfiC7Rn5BDh5X0_QF_fna6WH4qzz-8_Lt-eFYrn3QsmpKSKQNVCVTFR9qTVTdnXNWFalgCGMkJUU9ZaUdIIJkGItiK6YaWSJTf8AB3uvFPwNwni3I02KhgG6cCn2HFacUE4zee_KBFMtA1ty4y--Qtd-xRcXiRTTc2auqJb4dGOUsHHGMB0U7CjDJuOkm4bbZej7e6izezre2PqR9CP5EOWGTjZAbd2gM2_Td3qy6ed8g_Vaq_l</recordid><startdate>202408</startdate><enddate>202408</enddate><creator>Saifi, Farheen</creator><creator>Biró, János Barnabás</creator><creator>Horváth, Beatrix</creator><creator>Vizler, Csaba</creator><creator>Laczi, Krisztián</creator><creator>Rákhely, Gábor</creator><creator>Kovács, Szilárd</creator><creator>Kang, Mingming</creator><creator>Li, Dengyao</creator><creator>Chen, Yuhui</creator><creator>Chen, Rujin</creator><creator>Domonkos, Ágota</creator><creator>Kaló, Péter</creator><general>Blackwell Publishing Ltd</general><scope>24P</scope><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>7QO</scope><scope>7QP</scope><scope>7QR</scope><scope>7TM</scope><scope>8FD</scope><scope>FR3</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope><orcidid>https://orcid.org/0000-0002-6912-8227</orcidid><orcidid>https://orcid.org/0000-0001-5444-2144</orcidid><orcidid>https://orcid.org/0000-0001-8851-0387</orcidid><orcidid>https://orcid.org/0000-0003-4017-0605</orcidid><orcidid>https://orcid.org/0000-0001-8499-568X</orcidid><orcidid>https://orcid.org/0000-0002-0404-8904</orcidid><orcidid>https://orcid.org/0009-0005-2750-8845</orcidid></search><sort><creationdate>202408</creationdate><title>Two members of a Nodule‐specific Cysteine‐Rich (NCR) peptide gene cluster are required for differentiation of rhizobia in Medicago truncatula nodules</title><author>Saifi, Farheen ; Biró, János Barnabás ; Horváth, Beatrix ; Vizler, Csaba ; Laczi, Krisztián ; Rákhely, Gábor ; Kovács, Szilárd ; Kang, Mingming ; Li, Dengyao ; Chen, Yuhui ; Chen, Rujin ; Domonkos, Ágota ; Kaló, Péter</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3111-27aa1c0e59e55274b09d84b6602da4eef1200c846dc10872ae77950d824ca43f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Alfalfa</topic><topic>Bacteroids</topic><topic>Complementation</topic><topic>Cysteine</topic><topic>Cysteine - metabolism</topic><topic>Differentiation</topic><topic>family</topic><topic>Fixing</topic><topic>Gene duplication</topic><topic>Gene expression</topic><topic>Gene Expression Regulation, Plant</topic><topic>Genes</topic><topic>genotype</topic><topic>Genotypes</topic><topic>Host plants</topic><topic>indeterminate nodule</topic><topic>Internalization</topic><topic>Inverted repeat</topic><topic>Legumes</topic><topic>Medicago littoralis</topic><topic>Medicago truncatula</topic><topic>Medicago truncatula - genetics</topic><topic>Medicago truncatula - microbiology</topic><topic>Medicago truncatula - physiology</topic><topic>Multigene Family</topic><topic>mutants</topic><topic>Nitrogen</topic><topic>nitrogen fixation</topic><topic>Nitrogen Fixation - genetics</topic><topic>nitrogen‐fixing symbiosis</topic><topic>Nodules</topic><topic>nodule‐specific cysteine‐rich peptides</topic><topic>Peptides</topic><topic>Peptides - genetics</topic><topic>Peptides - metabolism</topic><topic>phenotype</topic><topic>Phenotypes</topic><topic>Plant Proteins - genetics</topic><topic>Plant Proteins - metabolism</topic><topic>Rhizobium - genetics</topic><topic>Rhizobium - physiology</topic><topic>Root nodules</topic><topic>Root Nodules, Plant - genetics</topic><topic>Root Nodules, Plant - microbiology</topic><topic>Sinorhizobium meliloti - genetics</topic><topic>Sinorhizobium meliloti - physiology</topic><topic>soil</topic><topic>Soil microorganisms</topic><topic>Symbiosis</topic><topic>Symbiosis - genetics</topic><topic>terminal differentiation</topic><topic>transcription (genetics)</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Saifi, Farheen</creatorcontrib><creatorcontrib>Biró, János Barnabás</creatorcontrib><creatorcontrib>Horváth, Beatrix</creatorcontrib><creatorcontrib>Vizler, Csaba</creatorcontrib><creatorcontrib>Laczi, Krisztián</creatorcontrib><creatorcontrib>Rákhely, Gábor</creatorcontrib><creatorcontrib>Kovács, Szilárd</creatorcontrib><creatorcontrib>Kang, Mingming</creatorcontrib><creatorcontrib>Li, Dengyao</creatorcontrib><creatorcontrib>Chen, Yuhui</creatorcontrib><creatorcontrib>Chen, Rujin</creatorcontrib><creatorcontrib>Domonkos, Ágota</creatorcontrib><creatorcontrib>Kaló, Péter</creatorcontrib><collection>Wiley Online Library Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Biotechnology Research Abstracts</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><jtitle>The Plant journal : for cell and molecular biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Saifi, Farheen</au><au>Biró, János Barnabás</au><au>Horváth, Beatrix</au><au>Vizler, Csaba</au><au>Laczi, Krisztián</au><au>Rákhely, Gábor</au><au>Kovács, Szilárd</au><au>Kang, Mingming</au><au>Li, Dengyao</au><au>Chen, Yuhui</au><au>Chen, Rujin</au><au>Domonkos, Ágota</au><au>Kaló, Péter</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Two members of a Nodule‐specific Cysteine‐Rich (NCR) peptide gene cluster are required for differentiation of rhizobia in Medicago truncatula nodules</atitle><jtitle>The Plant journal : for cell and molecular biology</jtitle><addtitle>Plant J</addtitle><date>2024-08</date><risdate>2024</risdate><volume>119</volume><issue>3</issue><spage>1508</spage><epage>1525</epage><pages>1508-1525</pages><issn>0960-7412</issn><issn>1365-313X</issn><eissn>1365-313X</eissn><abstract>SUMMARY
Legumes have evolved a nitrogen‐fixing symbiotic interaction with rhizobia, and this association helps them to cope with the limited nitrogen conditions in soil. The compatible interaction between the host plant and rhizobia leads to the formation of root nodules, wherein internalization and transition of rhizobia into their symbiotic form, termed bacteroids, occur. Rhizobia in the nodules of the Inverted Repeat‐Lacking Clade legumes, including Medicago truncatula, undergo terminal differentiation, resulting in elongated and endoreduplicated bacteroids. This transition of endocytosed rhizobia is mediated by a large gene family of host‐produced nodule‐specific cysteine‐rich (NCR) peptides in M. truncatula. Few NCRs have been recently found to be essential for complete differentiation and persistence of bacteroids. Here, we show that a M. truncatula symbiotic mutant FN9285, defective in the complete transition of rhizobia, is deficient in a cluster of NCR genes. More specifically, we show that the loss of the duplicated genes NCR086 and NCR314 in the A17 genotype, found in a single copy in Medicago littoralis R108, is responsible for the ineffective symbiotic phenotype of FN9285. The NCR086 and NCR314 gene pair encodes the same mature peptide but their transcriptional activity varies considerably. Nevertheless, both genes can restore the effective symbiosis in FN9285 indicating that their complementation ability does not depend on the strength of their expression activity. The identification of the NCR086/NCR314 peptide, essential for complete bacteroid differentiation, has extended the list of peptides, from a gene family of several hundred members, that are essential for effective nitrogen‐fixing symbiosis in M. truncatula.
Significance Statement
Our results demonstrate the requirement of NCR086/NCR314, which are members of the nodule‐specific cysteine‐rich peptide family, for effective symbiotic interaction between Medicago truncatula and the tested rhizobia strains. The NCR086/NCR314 peptides are encoded by a highly similar gene pair in M. truncatula A17 that was duplicated following the separation of lines M. truncatula A17 and Medicago littoralis R108.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>38923649</pmid><doi>10.1111/tpj.16871</doi><tpages>18</tpages><orcidid>https://orcid.org/0000-0002-6912-8227</orcidid><orcidid>https://orcid.org/0000-0001-5444-2144</orcidid><orcidid>https://orcid.org/0000-0001-8851-0387</orcidid><orcidid>https://orcid.org/0000-0003-4017-0605</orcidid><orcidid>https://orcid.org/0000-0001-8499-568X</orcidid><orcidid>https://orcid.org/0000-0002-0404-8904</orcidid><orcidid>https://orcid.org/0009-0005-2750-8845</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Alfalfa Bacteroids Complementation Cysteine Cysteine - metabolism Differentiation family Fixing Gene duplication Gene expression Gene Expression Regulation, Plant Genes genotype Genotypes Host plants indeterminate nodule Internalization Inverted repeat Legumes Medicago littoralis Medicago truncatula Medicago truncatula - genetics Medicago truncatula - microbiology Medicago truncatula - physiology Multigene Family mutants Nitrogen nitrogen fixation Nitrogen Fixation - genetics nitrogen‐fixing symbiosis Nodules nodule‐specific cysteine‐rich peptides Peptides Peptides - genetics Peptides - metabolism phenotype Phenotypes Plant Proteins - genetics Plant Proteins - metabolism Rhizobium - genetics Rhizobium - physiology Root nodules Root Nodules, Plant - genetics Root Nodules, Plant - microbiology Sinorhizobium meliloti - genetics Sinorhizobium meliloti - physiology soil Soil microorganisms Symbiosis Symbiosis - genetics terminal differentiation transcription (genetics) |
title | Two members of a Nodule‐specific Cysteine‐Rich (NCR) peptide gene cluster are required for differentiation of rhizobia in Medicago truncatula nodules |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-28T15%3A44%3A53IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_cross&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Two%20members%20of%20a%20Nodule%E2%80%90specific%20Cysteine%E2%80%90Rich%20(NCR)%20peptide%20gene%20cluster%20are%20required%20for%20differentiation%20of%20rhizobia%20in%20Medicago%20truncatula%20nodules&rft.jtitle=The%20Plant%20journal%20:%20for%20cell%20and%20molecular%20biology&rft.au=Saifi,%20Farheen&rft.date=2024-08&rft.volume=119&rft.issue=3&rft.spage=1508&rft.epage=1525&rft.pages=1508-1525&rft.issn=0960-7412&rft.eissn=1365-313X&rft_id=info:doi/10.1111/tpj.16871&rft_dat=%3Cproquest_cross%3E3072798194%3C/proquest_cross%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=3086286510&rft_id=info:pmid/38923649&rfr_iscdi=true |