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A Laser Dissection-RNAseq Analysis Highlights the Activation of Cytokinin Pathways by Nod Factors in the Medicago truncatula Root Epidermis

Marie-Françoise Jardinaud, Stéphane Boivin, Nathalie Rodde, Olivier Catrice, Anna Kisiala, Agnes Lepage, Sandra Moreau, Brice Roux, Ludovic Cottret, Erika Sallet, Mathias Brault, R.J. Neil Emery, Jérôme Gouzy, Florian Frugier, Pascal Gamas
Marie-Françoise Jardinaud
LIPM, Université de Toulouse, Institut National de la Recherche Agronomique, Centre National de la Recherche Scientifique, 31326 Castanet-Tolosan, France (M.-F.J., N.R., O.C., A.L., S.M., B.R., L.C., E.S., J.G., P.G.);
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Stéphane Boivin
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Nathalie Rodde
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Olivier Catrice
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Anna Kisiala
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Agnes Lepage
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Sandra Moreau
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Brice Roux
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Ludovic Cottret
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Erika Sallet
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Mathias Brault
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R.J. Neil Emery
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Jérôme Gouzy
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Florian Frugier
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Pascal Gamas
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  • For correspondence: pascal.gamas@toulouse.inra.fr

Published July 2016. DOI: https://doi.org/10.1104/pp.16.00711

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  • © 2016 American Society of Plant Biologists. All Rights Reserved.

Abstract

Nod factors (NFs) are lipochitooligosaccharidic signal molecules produced by rhizobia, which play a key role in the rhizobium-legume symbiotic interaction. In this study, we analyzed the gene expression reprogramming induced by purified NF (4 and 24 h of treatment) in the root epidermis of the model legume Medicago truncatula. Tissue-specific transcriptome analysis was achieved by laser-capture microdissection coupled to high-depth RNA sequencing. The expression of 17,191 genes was detected in the epidermis, among which 1,070 were found to be regulated by NF addition, including previously characterized NF-induced marker genes. Many genes exhibited strong levels of transcriptional activation, sometimes only transiently at 4 h, indicating highly dynamic regulation. Expression reprogramming affected a variety of cellular processes, including perception, signaling, regulation of gene expression, as well as cell wall, cytoskeleton, transport, metabolism, and defense, with numerous NF-induced genes never identified before. Strikingly, early epidermal activation of cytokinin (CK) pathways was indicated, based on the induction of CK metabolic and signaling genes, including the CRE1 receptor essential to promote nodulation. These transcriptional activations were independently validated using promoter:β-glucuronidase fusions with the MtCRE1 CK receptor gene and a CK response reporter (TWO COMPONENT SIGNALING SENSOR NEW). A CK pretreatment reduced the NF induction of the EARLY NODULIN11 (ENOD11) symbiotic marker, while a CK-degrading enzyme (CYTOKININ OXIDASE/DEHYDROGENASE3) ectopically expressed in the root epidermis led to increased NF induction of ENOD11 and nodulation. Therefore, CK may play both positive and negative roles in M. truncatula nodulation.

  • Glossary

    RH
    root hair
    LCO
    lipochitooligosaccharide
    NF
    Nod factor
    TF
    transcription factor
    ROS
    reactive oxygen species
    CK
    cytokinin
    RNAseq
    RNA sequencing
    LCM
    laser-capture microdissection
    MtGEA
    M. truncatula Gene Atlas
    H2O2
    hydrogen peroxide
    BAP
    6-benzylaminopurine
    LC-MS/MS
    liquid chromatography-tandem mass spectrometry
    tZNT
    trans-zeatin nucleotide
    iPNT
    isopentenyl adenine nucleotide
    PGDB
    pathway genome database
    • Received May 6, 2016.
    • Accepted May 18, 2016.
    • Published May 23, 2016.

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    A Laser Dissection-RNAseq Analysis Highlights the Activation of Cytokinin Pathways by Nod Factors in the Medicago truncatula Root Epidermis
    Marie-Françoise Jardinaud, Stéphane Boivin, Nathalie Rodde, Olivier Catrice, Anna Kisiala, Agnes Lepage, Sandra Moreau, Brice Roux, Ludovic Cottret, Erika Sallet, Mathias Brault, R.J. Neil Emery, Jérôme Gouzy, Florian Frugier, Pascal Gamas
    Plant Physiology Jul 2016, 171 (3) 2256-2276; DOI: 10.1104/pp.16.00711

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    A Laser Dissection-RNAseq Analysis Highlights the Activation of Cytokinin Pathways by Nod Factors in the Medicago truncatula Root Epidermis
    Marie-Françoise Jardinaud, Stéphane Boivin, Nathalie Rodde, Olivier Catrice, Anna Kisiala, Agnes Lepage, Sandra Moreau, Brice Roux, Ludovic Cottret, Erika Sallet, Mathias Brault, R.J. Neil Emery, Jérôme Gouzy, Florian Frugier, Pascal Gamas
    Plant Physiology Jul 2016, 171 (3) 2256-2276; DOI: 10.1104/pp.16.00711
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