title: The Symbiosis-Related ERN Transcription Factors Act in Concert to Coordinate Rhizobial Host Root Infection.
abstract: Legumes improve their mineral nutrition through nitrogen-fixing root nodule symbioses with soil rhizobia. Rhizobial infection of legumes is regulated by a number of transcription factors, including ERF Required for Nodulation1 (ERN1). Medicago truncatula plants defective in ERN1 are unable to nodulate, but still exhibit early symbiotic responses including rhizobial infection. ERN1 has a close homolog, ERN2, which shows partially overlapping expression patterns. Here we show that ern2 mutants exhibit a later nodulation phenotype than ern1, being able to form nodules but with signs of premature senescence. Molecular characterization of the ern2-1 mutation reveals a key role for a conserved threonine for both DNA binding and transcriptional activity. In contrast to either single mutant, the double ern1-1 ern2-1 line is completely unable to initiate infection or nodule development. The strong ern1-1 ern2-1 phenotype demonstrates functional redundancy between these two transcriptional regulators and reveals the essential role of ERN1/ERN2 to coordinately induce rhizobial infection and nodule organogenesis. While ERN1/ERN2 act in concert in the root epidermis, only ERN1 can efficiently allow the development of mature nodules in the cortex, probably through an independent pathway. Together, these findings reveal the key roles that ERN1/ERN2 play at the very earliest stages of root nodule development.
authors.affiliation: Laboratory of Plant-Microbe Interactions (LIPM), Centre National de la Recherche Scientifique (CNRS, UMR 2594), Institut National de la Recherche Agronomique (INRA, UMR 441), F-31326 Castanet-Tolosan, France (M.R.C., L.F., A.K., J.F., M.-C.A., D.G.B., F.d.C.-N.)Department of Cell and Developmental Biology, John Innes Centre, Norwich Research Park, Norwich NR4 7UH, United Kingdom (P.H.M., G.E.O.)The Samuel Roberts Noble Foundation, Ardmore, Oklahoma 73401 (K.S.M., J.W.); andInstitute de Pharmacologie et de Biologie Structurale (IPBS), UMR 5089-205, 31077 Toulouse, France (M.E.).
authors.forename: Marion R
authors.initials: MR
authors.lastname: Cerri
authors.affiliation: Laboratory of Plant-Microbe Interactions (LIPM), Centre National de la Recherche Scientifique (CNRS, UMR 2594), Institut National de la Recherche Agronomique (INRA, UMR 441), F-31326 Castanet-Tolosan, France (M.R.C., L.F., A.K., J.F., M.-C.A., D.G.B., F.d.C.-N.)Department of Cell and Developmental Biology, John Innes Centre, Norwich Research Park, Norwich NR4 7UH, United Kingdom (P.H.M., G.E.O.)The Samuel Roberts Noble Foundation, Ardmore, Oklahoma 73401 (K.S.M., J.W.); andInstitute de Pharmacologie et de Biologie Structurale (IPBS), UMR 5089-205, 31077 Toulouse, France (M.E.).
authors.forename: Lisa
authors.initials: L
authors.lastname: Frances
authors.affiliation: Laboratory of Plant-Microbe Interactions (LIPM), Centre National de la Recherche Scientifique (CNRS, UMR 2594), Institut National de la Recherche Agronomique (INRA, UMR 441), F-31326 Castanet-Tolosan, France (M.R.C., L.F., A.K., J.F., M.-C.A., D.G.B., F.d.C.-N.)Department of Cell and Developmental Biology, John Innes Centre, Norwich Research Park, Norwich NR4 7UH, United Kingdom (P.H.M., G.E.O.)The Samuel Roberts Noble Foundation, Ardmore, Oklahoma 73401 (K.S.M., J.W.); andInstitute de Pharmacologie et de Biologie Structurale (IPBS), UMR 5089-205, 31077 Toulouse, France (M.E.).
authors.forename: Audrey
authors.initials: A
authors.lastname: Kelner
authors.affiliation: Laboratory of Plant-Microbe Interactions (LIPM), Centre National de la Recherche Scientifique (CNRS, UMR 2594), Institut National de la Recherche Agronomique (INRA, UMR 441), F-31326 Castanet-Tolosan, France (M.R.C., L.F., A.K., J.F., M.-C.A., D.G.B., F.d.C.-N.)Department of Cell and Developmental Biology, John Innes Centre, Norwich Research Park, Norwich NR4 7UH, United Kingdom (P.H.M., G.E.O.)The Samuel Roberts Noble Foundation, Ardmore, Oklahoma 73401 (K.S.M., J.W.); andInstitute de Pharmacologie et de Biologie Structurale (IPBS), UMR 5089-205, 31077 Toulouse, France (M.E.).
authors.forename: Joëlle
authors.identifier: 0000-0003-3746-8080
authors.initials: J
authors.lastname: Fournier
authors.affiliation: Laboratory of Plant-Microbe Interactions (LIPM), Centre National de la Recherche Scientifique (CNRS, UMR 2594), Institut National de la Recherche Agronomique (INRA, UMR 441), F-31326 Castanet-Tolosan, France (M.R.C., L.F., A.K., J.F., M.-C.A., D.G.B., F.d.C.-N.)Department of Cell and Developmental Biology, John Innes Centre, Norwich Research Park, Norwich NR4 7UH, United Kingdom (P.H.M., G.E.O.)The Samuel Roberts Noble Foundation, Ardmore, Oklahoma 73401 (K.S.M., J.W.); andInstitute de Pharmacologie et de Biologie Structurale (IPBS), UMR 5089-205, 31077 Toulouse, France (M.E.).
authors.forename: Patrick H
authors.initials: PH
authors.lastname: Middleton
authors.affiliation: Laboratory of Plant-Microbe Interactions (LIPM), Centre National de la Recherche Scientifique (CNRS, UMR 2594), Institut National de la Recherche Agronomique (INRA, UMR 441), F-31326 Castanet-Tolosan, France (M.R.C., L.F., A.K., J.F., M.-C.A., D.G.B., F.d.C.-N.)Department of Cell and Developmental Biology, John Innes Centre, Norwich Research Park, Norwich NR4 7UH, United Kingdom (P.H.M., G.E.O.)The Samuel Roberts Noble Foundation, Ardmore, Oklahoma 73401 (K.S.M., J.W.); andInstitute de Pharmacologie et de Biologie Structurale (IPBS), UMR 5089-205, 31077 Toulouse, France (M.E.).
authors.forename: Marie-Christine
authors.initials: MC
authors.lastname: Auriac
authors.affiliation: Laboratory of Plant-Microbe Interactions (LIPM), Centre National de la Recherche Scientifique (CNRS, UMR 2594), Institut National de la Recherche Agronomique (INRA, UMR 441), F-31326 Castanet-Tolosan, France (M.R.C., L.F., A.K., J.F., M.-C.A., D.G.B., F.d.C.-N.)Department of Cell and Developmental Biology, John Innes Centre, Norwich Research Park, Norwich NR4 7UH, United Kingdom (P.H.M., G.E.O.)The Samuel Roberts Noble Foundation, Ardmore, Oklahoma 73401 (K.S.M., J.W.); andInstitute de Pharmacologie et de Biologie Structurale (IPBS), UMR 5089-205, 31077 Toulouse, France (M.E.).
authors.forename: Kirankumar S
authors.initials: KS
authors.lastname: Mysore
authors.affiliation: Laboratory of Plant-Microbe Interactions (LIPM), Centre National de la Recherche Scientifique (CNRS, UMR 2594), Institut National de la Recherche Agronomique (INRA, UMR 441), F-31326 Castanet-Tolosan, France (M.R.C., L.F., A.K., J.F., M.-C.A., D.G.B., F.d.C.-N.)Department of Cell and Developmental Biology, John Innes Centre, Norwich Research Park, Norwich NR4 7UH, United Kingdom (P.H.M., G.E.O.)The Samuel Roberts Noble Foundation, Ardmore, Oklahoma 73401 (K.S.M., J.W.); andInstitute de Pharmacologie et de Biologie Structurale (IPBS), UMR 5089-205, 31077 Toulouse, France (M.E.).
authors.forename: Jiangqi
authors.identifier: 0000-0001-5113-7750
authors.initials: J
authors.lastname: Wen
authors.affiliation: Laboratory of Plant-Microbe Interactions (LIPM), Centre National de la Recherche Scientifique (CNRS, UMR 2594), Institut National de la Recherche Agronomique (INRA, UMR 441), F-31326 Castanet-Tolosan, France (M.R.C., L.F., A.K., J.F., M.-C.A., D.G.B., F.d.C.-N.)Department of Cell and Developmental Biology, John Innes Centre, Norwich Research Park, Norwich NR4 7UH, United Kingdom (P.H.M., G.E.O.)The Samuel Roberts Noble Foundation, Ardmore, Oklahoma 73401 (K.S.M., J.W.); andInstitute de Pharmacologie et de Biologie Structurale (IPBS), UMR 5089-205, 31077 Toulouse, France (M.E.).
authors.forename: Monique
authors.initials: M
authors.lastname: Erard
authors.affiliation: Laboratory of Plant-Microbe Interactions (LIPM), Centre National de la Recherche Scientifique (CNRS, UMR 2594), Institut National de la Recherche Agronomique (INRA, UMR 441), F-31326 Castanet-Tolosan, France (M.R.C., L.F., A.K., J.F., M.-C.A., D.G.B., F.d.C.-N.)Department of Cell and Developmental Biology, John Innes Centre, Norwich Research Park, Norwich NR4 7UH, United Kingdom (P.H.M., G.E.O.)The Samuel Roberts Noble Foundation, Ardmore, Oklahoma 73401 (K.S.M., J.W.); andInstitute de Pharmacologie et de Biologie Structurale (IPBS), UMR 5089-205, 31077 Toulouse, France (M.E.).
authors.forename: David G
authors.initials: DG
authors.lastname: Barker
authors.affiliation: Laboratory of Plant-Microbe Interactions (LIPM), Centre National de la Recherche Scientifique (CNRS, UMR 2594), Institut National de la Recherche Agronomique (INRA, UMR 441), F-31326 Castanet-Tolosan, France (M.R.C., L.F., A.K., J.F., M.-C.A., D.G.B., F.d.C.-N.)Department of Cell and Developmental Biology, John Innes Centre, Norwich Research Park, Norwich NR4 7UH, United Kingdom (P.H.M., G.E.O.)The Samuel Roberts Noble Foundation, Ardmore, Oklahoma 73401 (K.S.M., J.W.); andInstitute de Pharmacologie et de Biologie Structurale (IPBS), UMR 5089-205, 31077 Toulouse, France (M.E.).
authors.forename: Giles E
authors.identifier: 0000-0002-5245-6355
authors.initials: GE
authors.lastname: Oldroyd
authors.affiliation: Laboratory of Plant-Microbe Interactions (LIPM), Centre National de la Recherche Scientifique (CNRS, UMR 2594), Institut National de la Recherche Agronomique (INRA, UMR 441), F-31326 Castanet-Tolosan, France (M.R.C., L.F., A.K., J.F., M.-C.A., D.G.B., F.d.C.-N.)Department of Cell and Developmental Biology, John Innes Centre, Norwich Research Park, Norwich NR4 7UH, United Kingdom (P.H.M., G.E.O.)The Samuel Roberts Noble Foundation, Ardmore, Oklahoma 73401 (K.S.M., J.W.); andInstitute de Pharmacologie et de Biologie Structurale (IPBS), UMR 5089-205, 31077 Toulouse, France (M.E.) fernanda.de-carvalho-niebel@toulouse.inra.fr.
authors.forename: Fernanda
authors.identifier: 0000-0002-5596-9420
authors.initials: F
authors.lastname: de Carvalho-Niebel
mesh_terms: D000483:Alleles; D000595:Amino Acid Sequence; D001483:Base Sequence; D018506:Gene Expression Regulation, Plant; D046913:Medicago truncatula / Q000235:genetics / Q000378:metabolism* / Q000382:microbiology* / Q000648:ultrastructure; D009154:Mutation / Q000235:genetics; D038821:Mycorrhizae / Q000502:physiology; D009586:Nitrogen Fixation; D038081:Organogenesis / Q000235:genetics; D010935:Plant Diseases / Q000382:microbiology*; D019441:Plant Epidermis / Q000235:genetics / Q000382:microbiology; D010940:Plant Proteins / Q000737:chemistry / Q000235:genetics / Q000378:metabolism*; D018517:Plant Roots / Q000235:genetics / Q000382:microbiology* / Q000648:ultrastructure; D011401:Promoter Regions, Genetic / Q000235:genetics; D011485:Protein Binding; D012231:Rhizobium / Q000502:physiology*; D053204:Root Nodules, Plant / Q000378:metabolism / Q000382:microbiology / Q000648:ultrastructure; D015398:Signal Transduction / Q000235:genetics; D013559:Symbiosis / Q000235:genetics; D014157:Transcription Factors / Q000737:chemistry / Q000378:metabolism*; D014158:Transcription, Genetic
chemical_list: D010940:Plant Proteins; D014157:Transcription Factors