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
Hauptverfasser: 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
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container_issue 3
container_start_page 1508
container_title The Plant journal : for cell and molecular biology
container_volume 119
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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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. 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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. 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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 &amp; 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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. 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source MEDLINE; Wiley Online Library Journals Frontfile Complete
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
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