Amino Acid Polymorphisms in the VHIID Conserved Motif of Nodulation Signaling Pathways 2 Distinctly Modulate Symbiotic Signaling and Nodule Morphogenesis in Medicago truncatula

Legumes establish an endosymbiotic association with nitrogen-fixing soil bacteria. Following the mutual recognition of the symbiotic partner, the infection process is controlled by the induction of the signaling pathway and subsequent activation of symbiosis-related host genes. One of the protein co...

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Main Authors: Szilárd Kovacs, Lili Fodor, Agota Domonkos, Ferhan Ayaydin, Krisztián Laczi, Gábor Rákhely, Péter Kalo
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-12-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2021.709857/full
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author Szilárd Kovacs
Lili Fodor
Agota Domonkos
Ferhan Ayaydin
Ferhan Ayaydin
Krisztián Laczi
Krisztián Laczi
Gábor Rákhely
Gábor Rákhely
Péter Kalo
Péter Kalo
author_facet Szilárd Kovacs
Lili Fodor
Agota Domonkos
Ferhan Ayaydin
Ferhan Ayaydin
Krisztián Laczi
Krisztián Laczi
Gábor Rákhely
Gábor Rákhely
Péter Kalo
Péter Kalo
author_sort Szilárd Kovacs
collection DOAJ
description Legumes establish an endosymbiotic association with nitrogen-fixing soil bacteria. Following the mutual recognition of the symbiotic partner, the infection process is controlled by the induction of the signaling pathway and subsequent activation of symbiosis-related host genes. One of the protein complexes regulating nitrogen-fixing root nodule symbiosis is formed by GRAS domain regulatory proteins Nodulation Signaling Pathways 1 and 2 (NSP1 and NSP2) that control the expression of several early nodulation genes. Here, we report on a novel point mutant allele (nsp2-6) affecting the function of the NSP2 gene and compared the mutant with the formerly identified nsp2-3 mutant. Both mutants carry a single amino acid substitution in the VHIID motif of the NSP2 protein. We found that the two mutant alleles show dissimilar root hair response to bacterial infection. Although the nsp2-3 mutant developed aberrant infection threads, rhizobia were able to colonize nodule cells in this mutant. The encoded NSP2 proteins of the nsp2-3 and the novel nsp2 mutants interact with NSP1 diversely and, as a consequence, the activation of early nodulin genes and nodule organogenesis are arrested in the new nsp2 allele. The novel mutant with amino acid substitution D244H in NSP2 shows similar defects in symbiotic responses as a formerly identified nsp2-2 mutant carrying a deletion in the NSP2 gene. Additionally, we found that rhizobial strains induce delayed nodule formation on the roots of the ns2-3 weak allele. Our study highlights the importance of a conserved Asp residue in the VHIID motif of NSP2 that is required for the formation of a functional NSP1-NSP2 signaling module. Furthermore, our results imply the involvement of NSP2 during differentiation of symbiotic nodule cells.
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spelling doaj.art-25374eeca7a646e79ad1f89e9c143a782022-12-21T16:35:06ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2021-12-011210.3389/fpls.2021.709857709857Amino Acid Polymorphisms in the VHIID Conserved Motif of Nodulation Signaling Pathways 2 Distinctly Modulate Symbiotic Signaling and Nodule Morphogenesis in Medicago truncatulaSzilárd Kovacs0Lili Fodor1Agota Domonkos2Ferhan Ayaydin3Ferhan Ayaydin4Krisztián Laczi5Krisztián Laczi6Gábor Rákhely7Gábor Rákhely8Péter Kalo9Péter Kalo10Institute of Plant Biology, Biological Research Center, Eötvös Lóránd Research Network, Szeged, HungaryInstitute of Genetics and Biotechnology, Hungarian University of Agriculture and Life Sciences, Gödöllö, HungaryInstitute of Genetics and Biotechnology, Hungarian University of Agriculture and Life Sciences, Gödöllö, HungaryHungarian Centre of Excellence for Molecular Medicine (HCEMM) Nonprofit Ltd., Szeged, HungaryCellular Imaging Laboratory, Biological Research Center, Eötvös Lóránd Research Network, Szeged, HungaryInstitute of Plant Biology, Biological Research Center, Eötvös Lóránd Research Network, Szeged, HungaryDepartment of Biotechnology, University of Szeged, Szeged, HungaryDepartment of Biotechnology, University of Szeged, Szeged, HungaryInstitute of Biophysics, Biological Research Center, Eötvös Lóránd Research Network, Szeged, HungaryInstitute of Plant Biology, Biological Research Center, Eötvös Lóránd Research Network, Szeged, HungaryInstitute of Genetics and Biotechnology, Hungarian University of Agriculture and Life Sciences, Gödöllö, HungaryLegumes establish an endosymbiotic association with nitrogen-fixing soil bacteria. Following the mutual recognition of the symbiotic partner, the infection process is controlled by the induction of the signaling pathway and subsequent activation of symbiosis-related host genes. One of the protein complexes regulating nitrogen-fixing root nodule symbiosis is formed by GRAS domain regulatory proteins Nodulation Signaling Pathways 1 and 2 (NSP1 and NSP2) that control the expression of several early nodulation genes. Here, we report on a novel point mutant allele (nsp2-6) affecting the function of the NSP2 gene and compared the mutant with the formerly identified nsp2-3 mutant. Both mutants carry a single amino acid substitution in the VHIID motif of the NSP2 protein. We found that the two mutant alleles show dissimilar root hair response to bacterial infection. Although the nsp2-3 mutant developed aberrant infection threads, rhizobia were able to colonize nodule cells in this mutant. The encoded NSP2 proteins of the nsp2-3 and the novel nsp2 mutants interact with NSP1 diversely and, as a consequence, the activation of early nodulin genes and nodule organogenesis are arrested in the new nsp2 allele. The novel mutant with amino acid substitution D244H in NSP2 shows similar defects in symbiotic responses as a formerly identified nsp2-2 mutant carrying a deletion in the NSP2 gene. Additionally, we found that rhizobial strains induce delayed nodule formation on the roots of the ns2-3 weak allele. Our study highlights the importance of a conserved Asp residue in the VHIID motif of NSP2 that is required for the formation of a functional NSP1-NSP2 signaling module. Furthermore, our results imply the involvement of NSP2 during differentiation of symbiotic nodule cells.https://www.frontiersin.org/articles/10.3389/fpls.2021.709857/fullroot nodule symbiosisnitrogen fixationnod-factor signalingMedicagorhizobiaGRAS transcription factors
spellingShingle Szilárd Kovacs
Lili Fodor
Agota Domonkos
Ferhan Ayaydin
Ferhan Ayaydin
Krisztián Laczi
Krisztián Laczi
Gábor Rákhely
Gábor Rákhely
Péter Kalo
Péter Kalo
Amino Acid Polymorphisms in the VHIID Conserved Motif of Nodulation Signaling Pathways 2 Distinctly Modulate Symbiotic Signaling and Nodule Morphogenesis in Medicago truncatula
Frontiers in Plant Science
root nodule symbiosis
nitrogen fixation
nod-factor signaling
Medicago
rhizobia
GRAS transcription factors
title Amino Acid Polymorphisms in the VHIID Conserved Motif of Nodulation Signaling Pathways 2 Distinctly Modulate Symbiotic Signaling and Nodule Morphogenesis in Medicago truncatula
title_full Amino Acid Polymorphisms in the VHIID Conserved Motif of Nodulation Signaling Pathways 2 Distinctly Modulate Symbiotic Signaling and Nodule Morphogenesis in Medicago truncatula
title_fullStr Amino Acid Polymorphisms in the VHIID Conserved Motif of Nodulation Signaling Pathways 2 Distinctly Modulate Symbiotic Signaling and Nodule Morphogenesis in Medicago truncatula
title_full_unstemmed Amino Acid Polymorphisms in the VHIID Conserved Motif of Nodulation Signaling Pathways 2 Distinctly Modulate Symbiotic Signaling and Nodule Morphogenesis in Medicago truncatula
title_short Amino Acid Polymorphisms in the VHIID Conserved Motif of Nodulation Signaling Pathways 2 Distinctly Modulate Symbiotic Signaling and Nodule Morphogenesis in Medicago truncatula
title_sort amino acid polymorphisms in the vhiid conserved motif of nodulation signaling pathways 2 distinctly modulate symbiotic signaling and nodule morphogenesis in medicago truncatula
topic root nodule symbiosis
nitrogen fixation
nod-factor signaling
Medicago
rhizobia
GRAS transcription factors
url https://www.frontiersin.org/articles/10.3389/fpls.2021.709857/full
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