Two CCAAT-box-binding transcription factors redundantly regulate early steps of the legume-rhizobia endosymbiosis

Authors

  • Tom Laloum,

    1. Laboratoire des Interactions Plantes-Microorganismes (LIPM), INRA, UMR441, Castanet-Tolosan, France
    2. Laboratoire des Interactions Plantes-Microorganismes (LIPM), CNRS, UMR2594, Castanet-Tolosan, France
    Current affiliation:
    1. Faculty of Biology, Technion, Haifa, Israel
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    • These authors contributed equally to this work.
  • Maël Baudin,

    1. Laboratoire des Interactions Plantes-Microorganismes (LIPM), INRA, UMR441, Castanet-Tolosan, France
    2. Laboratoire des Interactions Plantes-Microorganismes (LIPM), CNRS, UMR2594, Castanet-Tolosan, France
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    • These authors contributed equally to this work.
  • Lisa Frances,

    1. Laboratoire des Interactions Plantes-Microorganismes (LIPM), INRA, UMR441, Castanet-Tolosan, France
    2. Laboratoire des Interactions Plantes-Microorganismes (LIPM), CNRS, UMR2594, Castanet-Tolosan, France
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  • Agnes Lepage,

    1. Laboratoire des Interactions Plantes-Microorganismes (LIPM), INRA, UMR441, Castanet-Tolosan, France
    2. Laboratoire des Interactions Plantes-Microorganismes (LIPM), CNRS, UMR2594, Castanet-Tolosan, France
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  • Benjamin Billault-Penneteau,

    1. Laboratoire des Interactions Plantes-Microorganismes (LIPM), INRA, UMR441, Castanet-Tolosan, France
    2. Laboratoire des Interactions Plantes-Microorganismes (LIPM), CNRS, UMR2594, Castanet-Tolosan, France
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  • Marion R. Cerri,

    1. Laboratoire des Interactions Plantes-Microorganismes (LIPM), INRA, UMR441, Castanet-Tolosan, France
    2. Laboratoire des Interactions Plantes-Microorganismes (LIPM), CNRS, UMR2594, Castanet-Tolosan, France
    Current affiliation:
    1. Faculty of Biology, Genetics, University of Munich (LMU), Martinsried, Germany
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  • Federico Ariel,

    1. Centre National de la Recherche Scientifique, Institut des Sciences du Végétal, Gif-sur-Yvette Cedex, France
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  • Marie-Françoise Jardinaud,

    1. Laboratoire des Interactions Plantes-Microorganismes (LIPM), INRA, UMR441, Castanet-Tolosan, France
    2. Laboratoire des Interactions Plantes-Microorganismes (LIPM), CNRS, UMR2594, Castanet-Tolosan, France
    3. ENSAT, INPT-Université de Toulouse, Auzeville-Tolosane, Castanet-Tolosan, France
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  • Pascal Gamas,

    1. Laboratoire des Interactions Plantes-Microorganismes (LIPM), INRA, UMR441, Castanet-Tolosan, France
    2. Laboratoire des Interactions Plantes-Microorganismes (LIPM), CNRS, UMR2594, Castanet-Tolosan, France
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  • Fernanda de Carvalho-Niebel,

    1. Laboratoire des Interactions Plantes-Microorganismes (LIPM), INRA, UMR441, Castanet-Tolosan, France
    2. Laboratoire des Interactions Plantes-Microorganismes (LIPM), CNRS, UMR2594, Castanet-Tolosan, France
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  • Andreas Niebel

    Corresponding author
    1. Laboratoire des Interactions Plantes-Microorganismes (LIPM), INRA, UMR441, Castanet-Tolosan, France
    2. Laboratoire des Interactions Plantes-Microorganismes (LIPM), CNRS, UMR2594, Castanet-Tolosan, France
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Summary

During endosymbiotic interactions between legume plants and nitrogen-fixing rhizobia, successful root infection by bacteria and nodule organogenesis requires the perception and transduction of bacterial lipo-chitooligosaccharidic signal called Nod factor (NF). NF perception in legume roots leads to the activation of an early signaling pathway and of a set of symbiotic genes which is controlled by specific early transcription factors (TFs) including CYCLOPS/IPD3, NSP1, NSP2, ERN1 and NIN. In this study, we bring convincing evidence that the Medicago truncatula CCAAT-box-binding NF-YA1 TF, previously associated with later stages of rhizobial infection and nodule meristem formation is, together with its closest homolog NF-YA2, also an essential positive regulator of the NF-signaling pathway. Here we show that NF-YA1 and NF-YA2 are both expressed in epidermal cells responding to NFs and their knock-down by reverse genetic approaches severely affects the NF-induced expression of symbiotic genes and rhizobial infection. Further over-expression, transactivation and ChIP-PCR approaches indicate that NF-YA1 and NF-YA2 function, at least in part, via the direct activation of ERN1. We thus propose a model in which NF-YA1 and NF-YA2 appear as early symbiotic regulators acting downstream of DMI3 and NIN and possibly within the same regulatory complexes as NSP1/2 to directly activate the expression of ERN1.

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