title: PUB1 Interacts with the Receptor Kinase DMI2 and Negatively Regulates Rhizobial and Arbuscular Mycorrhizal Symbioses through Its Ubiquitination Activity in Medicago truncatula.
abstract: PUB1, an E3 ubiquitin ligase, which interacts with and is phosphorylated by the LYK3 symbiotic receptor kinase, negatively regulates rhizobial infection and nodulation during the nitrogen-fixing root nodule symbiosis in Medicago truncatula In this study, we show that PUB1 also interacts with and is phosphorylated by DOES NOT MAKE INFECTIONS 2, the key symbiotic receptor kinase of the common symbiosis signaling pathway, required for both the rhizobial and the arbuscular mycorrhizal (AM) endosymbioses. We also show here that PUB1 expression is activated during successive stages of root colonization by Rhizophagus irregularis that is compatible with its interaction with DOES NOT MAKE INFECTIONS 2. Through characterization of a mutant, pub1-1, affected by the E3 ubiquitin ligase activity of PUB1, we have shown that the ubiquitination activity of PUB1 is required to negatively modulate successive stages of infection and development of rhizobial and AM symbioses. In conclusion, PUB1 represents, to our knowledge, a novel common component of symbiotic signaling integrating signal perception through interaction with and phosphorylation by two key symbiotic receptor kinases, and downstream signaling via its ubiquitination activity to fine-tune both rhizobial and AM root endosymbioses.
authors.affiliation: Institut National de la Recherche Agronomique, Laboratoire des Interactions Plantes-Microorganismes, UMR441, Castanet-Tolosan F-31326, France (T.V., S.C., C.C, C.R., F.D.C.-N., M.M., T.T., V.G., B.L., J.C., C.H.); Centre National de la Recherche Scientifique, Laboratoire des Interactions Plantes-Microorganismes, UMR2594, Castanet-Tolosan F-31326, France (T.V., S.C., C.C, C.R., F.D.C.-N., M.M., T.T., V.G., B.L., J.C., C.H.); and Institut National de la Recherche Agronomique-UMR1347-Agroecologie AgroSup/Institut National de la Recherche Agronomique/uB, Pôle Génétique & Ecophysiologie GEAPSI, 21065 Dijon France (R.T., C.L.).
authors.forename: Tatiana
authors.identifier: 0000-0003-1387-6370
authors.initials: T
authors.lastname: Vernié
authors.affiliation: Institut National de la Recherche Agronomique, Laboratoire des Interactions Plantes-Microorganismes, UMR441, Castanet-Tolosan F-31326, France (T.V., S.C., C.C, C.R., F.D.C.-N., M.M., T.T., V.G., B.L., J.C., C.H.); Centre National de la Recherche Scientifique, Laboratoire des Interactions Plantes-Microorganismes, UMR2594, Castanet-Tolosan F-31326, France (T.V., S.C., C.C, C.R., F.D.C.-N., M.M., T.T., V.G., B.L., J.C., C.H.); and Institut National de la Recherche Agronomique-UMR1347-Agroecologie AgroSup/Institut National de la Recherche Agronomique/uB, Pôle Génétique & Ecophysiologie GEAPSI, 21065 Dijon France (R.T., C.L.).
authors.forename: Sylvie
authors.initials: S
authors.lastname: Camut
authors.affiliation: Institut National de la Recherche Agronomique, Laboratoire des Interactions Plantes-Microorganismes, UMR441, Castanet-Tolosan F-31326, France (T.V., S.C., C.C, C.R., F.D.C.-N., M.M., T.T., V.G., B.L., J.C., C.H.); Centre National de la Recherche Scientifique, Laboratoire des Interactions Plantes-Microorganismes, UMR2594, Castanet-Tolosan F-31326, France (T.V., S.C., C.C, C.R., F.D.C.-N., M.M., T.T., V.G., B.L., J.C., C.H.); and Institut National de la Recherche Agronomique-UMR1347-Agroecologie AgroSup/Institut National de la Recherche Agronomique/uB, Pôle Génétique & Ecophysiologie GEAPSI, 21065 Dijon France (R.T., C.L.).
authors.forename: Céline
authors.initials: C
authors.lastname: Camps
authors.affiliation: Institut National de la Recherche Agronomique, Laboratoire des Interactions Plantes-Microorganismes, UMR441, Castanet-Tolosan F-31326, France (T.V., S.C., C.C, C.R., F.D.C.-N., M.M., T.T., V.G., B.L., J.C., C.H.); Centre National de la Recherche Scientifique, Laboratoire des Interactions Plantes-Microorganismes, UMR2594, Castanet-Tolosan F-31326, France (T.V., S.C., C.C, C.R., F.D.C.-N., M.M., T.T., V.G., B.L., J.C., C.H.); and Institut National de la Recherche Agronomique-UMR1347-Agroecologie AgroSup/Institut National de la Recherche Agronomique/uB, Pôle Génétique & Ecophysiologie GEAPSI, 21065 Dijon France (R.T., C.L.).
authors.forename: Céline
authors.initials: C
authors.lastname: Rembliere
authors.affiliation: Institut National de la Recherche Agronomique, Laboratoire des Interactions Plantes-Microorganismes, UMR441, Castanet-Tolosan F-31326, France (T.V., S.C., C.C, C.R., F.D.C.-N., M.M., T.T., V.G., B.L., J.C., C.H.); Centre National de la Recherche Scientifique, Laboratoire des Interactions Plantes-Microorganismes, UMR2594, Castanet-Tolosan F-31326, France (T.V., S.C., C.C, C.R., F.D.C.-N., M.M., T.T., V.G., B.L., J.C., C.H.); and Institut National de la Recherche Agronomique-UMR1347-Agroecologie AgroSup/Institut National de la Recherche Agronomique/uB, Pôle Génétique & Ecophysiologie GEAPSI, 21065 Dijon France (R.T., C.L.).
authors.forename: Fernanda
authors.initials: F
authors.lastname: de Carvalho-Niebel
authors.affiliation: Institut National de la Recherche Agronomique, Laboratoire des Interactions Plantes-Microorganismes, UMR441, Castanet-Tolosan F-31326, France (T.V., S.C., C.C, C.R., F.D.C.-N., M.M., T.T., V.G., B.L., J.C., C.H.); Centre National de la Recherche Scientifique, Laboratoire des Interactions Plantes-Microorganismes, UMR2594, Castanet-Tolosan F-31326, France (T.V., S.C., C.C, C.R., F.D.C.-N., M.M., T.T., V.G., B.L., J.C., C.H.); and Institut National de la Recherche Agronomique-UMR1347-Agroecologie AgroSup/Institut National de la Recherche Agronomique/uB, Pôle Génétique & Ecophysiologie GEAPSI, 21065 Dijon France (R.T., C.L.).
authors.forename: Malick
authors.identifier: 0000-0002-7723-7757
authors.initials: M
authors.lastname: Mbengue
authors.affiliation: Institut National de la Recherche Agronomique, Laboratoire des Interactions Plantes-Microorganismes, UMR441, Castanet-Tolosan F-31326, France (T.V., S.C., C.C, C.R., F.D.C.-N., M.M., T.T., V.G., B.L., J.C., C.H.); Centre National de la Recherche Scientifique, Laboratoire des Interactions Plantes-Microorganismes, UMR2594, Castanet-Tolosan F-31326, France (T.V., S.C., C.C, C.R., F.D.C.-N., M.M., T.T., V.G., B.L., J.C., C.H.); and Institut National de la Recherche Agronomique-UMR1347-Agroecologie AgroSup/Institut National de la Recherche Agronomique/uB, Pôle Génétique & Ecophysiologie GEAPSI, 21065 Dijon France (R.T., C.L.).
authors.forename: Ton
authors.initials: T
authors.lastname: Timmers
authors.affiliation: Institut National de la Recherche Agronomique, Laboratoire des Interactions Plantes-Microorganismes, UMR441, Castanet-Tolosan F-31326, France (T.V., S.C., C.C, C.R., F.D.C.-N., M.M., T.T., V.G., B.L., J.C., C.H.); Centre National de la Recherche Scientifique, Laboratoire des Interactions Plantes-Microorganismes, UMR2594, Castanet-Tolosan F-31326, France (T.V., S.C., C.C, C.R., F.D.C.-N., M.M., T.T., V.G., B.L., J.C., C.H.); and Institut National de la Recherche Agronomique-UMR1347-Agroecologie AgroSup/Institut National de la Recherche Agronomique/uB, Pôle Génétique & Ecophysiologie GEAPSI, 21065 Dijon France (R.T., C.L.).
authors.forename: Virginie
authors.initials: V
authors.lastname: Gasciolli
authors.affiliation: Institut National de la Recherche Agronomique, Laboratoire des Interactions Plantes-Microorganismes, UMR441, Castanet-Tolosan F-31326, France (T.V., S.C., C.C, C.R., F.D.C.-N., M.M., T.T., V.G., B.L., J.C., C.H.); Centre National de la Recherche Scientifique, Laboratoire des Interactions Plantes-Microorganismes, UMR2594, Castanet-Tolosan F-31326, France (T.V., S.C., C.C, C.R., F.D.C.-N., M.M., T.T., V.G., B.L., J.C., C.H.); and Institut National de la Recherche Agronomique-UMR1347-Agroecologie AgroSup/Institut National de la Recherche Agronomique/uB, Pôle Génétique & Ecophysiologie GEAPSI, 21065 Dijon France (R.T., C.L.).
authors.forename: Richard
authors.initials: R
authors.lastname: Thompson
authors.affiliation: Institut National de la Recherche Agronomique, Laboratoire des Interactions Plantes-Microorganismes, UMR441, Castanet-Tolosan F-31326, France (T.V., S.C., C.C, C.R., F.D.C.-N., M.M., T.T., V.G., B.L., J.C., C.H.); Centre National de la Recherche Scientifique, Laboratoire des Interactions Plantes-Microorganismes, UMR2594, Castanet-Tolosan F-31326, France (T.V., S.C., C.C, C.R., F.D.C.-N., M.M., T.T., V.G., B.L., J.C., C.H.); and Institut National de la Recherche Agronomique-UMR1347-Agroecologie AgroSup/Institut National de la Recherche Agronomique/uB, Pôle Génétique & Ecophysiologie GEAPSI, 21065 Dijon France (R.T., C.L.).
authors.forename: Christine
authors.identifier: 0000-0002-3204-3537
authors.initials: C
authors.lastname: le Signor
authors.affiliation: Institut National de la Recherche Agronomique, Laboratoire des Interactions Plantes-Microorganismes, UMR441, Castanet-Tolosan F-31326, France (T.V., S.C., C.C, C.R., F.D.C.-N., M.M., T.T., V.G., B.L., J.C., C.H.); Centre National de la Recherche Scientifique, Laboratoire des Interactions Plantes-Microorganismes, UMR2594, Castanet-Tolosan F-31326, France (T.V., S.C., C.C, C.R., F.D.C.-N., M.M., T.T., V.G., B.L., J.C., C.H.); and Institut National de la Recherche Agronomique-UMR1347-Agroecologie AgroSup/Institut National de la Recherche Agronomique/uB, Pôle Génétique & Ecophysiologie GEAPSI, 21065 Dijon France (R.T., C.L.).
authors.forename: Benoit
authors.initials: B
authors.lastname: Lefebvre
authors.affiliation: Institut National de la Recherche Agronomique, Laboratoire des Interactions Plantes-Microorganismes, UMR441, Castanet-Tolosan F-31326, France (T.V., S.C., C.C, C.R., F.D.C.-N., M.M., T.T., V.G., B.L., J.C., C.H.); Centre National de la Recherche Scientifique, Laboratoire des Interactions Plantes-Microorganismes, UMR2594, Castanet-Tolosan F-31326, France (T.V., S.C., C.C, C.R., F.D.C.-N., M.M., T.T., V.G., B.L., J.C., C.H.); and Institut National de la Recherche Agronomique-UMR1347-Agroecologie AgroSup/Institut National de la Recherche Agronomique/uB, Pôle Génétique & Ecophysiologie GEAPSI, 21065 Dijon France (R.T., C.L.).
authors.forename: Julie
authors.initials: J
authors.lastname: Cullimore
authors.affiliation: Institut National de la Recherche Agronomique, Laboratoire des Interactions Plantes-Microorganismes, UMR441, Castanet-Tolosan F-31326, France (T.V., S.C., C.C, C.R., F.D.C.-N., M.M., T.T., V.G., B.L., J.C., C.H.); Centre National de la Recherche Scientifique, Laboratoire des Interactions Plantes-Microorganismes, UMR2594, Castanet-Tolosan F-31326, France (T.V., S.C., C.C, C.R., F.D.C.-N., M.M., T.T., V.G., B.L., J.C., C.H.); and Institut National de la Recherche Agronomique-UMR1347-Agroecologie AgroSup/Institut National de la Recherche Agronomique/uB, Pôle Génétique & Ecophysiologie GEAPSI, 21065 Dijon France (R.T., C.L.) christine.herve@toulouse.inra.fr.
authors.forename: Christine
authors.initials: C
authors.lastname: Hervé
mesh_terms: D015169:Colony Count, Microbial; D055137:Glomeromycota / Q000502:physiology; D046913:Medicago truncatula / Q000378:metabolism* / Q000382:microbiology*; D038821:Mycorrhizae / Q000254:growth & development / Q000502:physiology*; D010766:Phosphorylation; D010940:Plant Proteins / Q000737:chemistry / Q000378:metabolism*; D000072417:Protein Domains; D012231:Rhizobium / Q000502:physiology*; D012441:Saccharomyces cerevisiae / Q000378:metabolism; D013559:Symbiosis; D044767:Ubiquitin-Protein Ligases / Q000378:metabolism; D054875:Ubiquitination
chemical_list: D010940:Plant Proteins; D044767:Ubiquitin-Protein Ligases
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