title: Regulation of Differentiation of Nitrogen-Fixing Bacteria by Microsymbiont Targeting of Plant Thioredoxin s1.
abstract: Legumes associate with rhizobia to form nitrogen (N2)-fixing nodules, which is important for plant fitness [1, 2]. Medicago truncatula controls the terminal differentiation of Sinorhizobium meliloti into N2-fixing bacteroids by producing defensin-like nodule-specific cysteine-rich peptides (NCRs) [3, 4]. The redox state of NCRs influences some biological activities in free-living bacteria, but the relevance of redox regulation of NCRs in planta is unknown [5, 6], although redox regulation plays a crucial role in symbiotic nitrogen fixation [7, 8]. Two thioredoxins (Trx), Trx s1 and s2, define a new type of Trx and are expressed principally in nodules [9]. Here, we show that there are four Trx s genes, two of which, Trx s1 and s3, are induced in the nodule infection zone where bacterial differentiation occurs. Trx s1 is targeted to the symbiosomes, the N2-fixing organelles. Trx s1 interacted with NCR247 and NCR335 and increased the cytotoxic effect of NCR335 in S. meliloti. We show that Trx s silencing impairs bacteroid growth and endoreduplication, two features of terminal bacteroid differentiation, and that the ectopic expression of Trx s1 in S. meliloti partially complements the silencing phenotype. Thus, our findings show that Trx s1 is targeted to the bacterial endosymbiont, where it controls NCR activity and bacteroid terminal differentiation. Similarly, Trxs are critical for the activation of defensins produced against infectious microbes in mammalian hosts. Therefore, our results suggest the Trx-mediated regulation of host peptides as a conserved mechanism among symbiotic and pathogenic interactions.
authors.affiliation: Institut Sophia Agrobiotech, Université de Nice-Sophia Antipolis, 400 Route des Chappes, BP167, 06903 Sophia Antipolis Cedex, France; Institut Sophia Agrobiotech, INRA UMR 1355, 400 Route des Chappes, BP167, 06903 Sophia Antipolis Cedex, France; Institut Sophia Agrobiotech, CNRS UMR 7254, 400 Route des Chappes, BP167, 06903 Sophia Antipolis Cedex, France.
authors.forename: Carolina Werner
authors.initials: CW
authors.lastname: Ribeiro
authors.affiliation: Institut Sophia Agrobiotech, Université de Nice-Sophia Antipolis, 400 Route des Chappes, BP167, 06903 Sophia Antipolis Cedex, France; Institut Sophia Agrobiotech, INRA UMR 1355, 400 Route des Chappes, BP167, 06903 Sophia Antipolis Cedex, France; Institut Sophia Agrobiotech, CNRS UMR 7254, 400 Route des Chappes, BP167, 06903 Sophia Antipolis Cedex, France.
authors.forename: Fabien
authors.initials: F
authors.lastname: Baldacci-Cresp
authors.affiliation: Institut Sophia Agrobiotech, Université de Nice-Sophia Antipolis, 400 Route des Chappes, BP167, 06903 Sophia Antipolis Cedex, France; Institut Sophia Agrobiotech, INRA UMR 1355, 400 Route des Chappes, BP167, 06903 Sophia Antipolis Cedex, France; Institut Sophia Agrobiotech, CNRS UMR 7254, 400 Route des Chappes, BP167, 06903 Sophia Antipolis Cedex, France.
authors.forename: Olivier
authors.initials: O
authors.lastname: Pierre
authors.affiliation: Institut Sophia Agrobiotech, Université de Nice-Sophia Antipolis, 400 Route des Chappes, BP167, 06903 Sophia Antipolis Cedex, France; Institut Sophia Agrobiotech, INRA UMR 1355, 400 Route des Chappes, BP167, 06903 Sophia Antipolis Cedex, France; Institut Sophia Agrobiotech, CNRS UMR 7254, 400 Route des Chappes, BP167, 06903 Sophia Antipolis Cedex, France.
authors.forename: Marie
authors.initials: M
authors.lastname: Larousse
authors.affiliation: Institut Sophia Agrobiotech, Université de Nice-Sophia Antipolis, 400 Route des Chappes, BP167, 06903 Sophia Antipolis Cedex, France; Institut Sophia Agrobiotech, INRA UMR 1355, 400 Route des Chappes, BP167, 06903 Sophia Antipolis Cedex, France; Institut Sophia Agrobiotech, CNRS UMR 7254, 400 Route des Chappes, BP167, 06903 Sophia Antipolis Cedex, France.
authors.forename: Sofiane
authors.initials: S
authors.lastname: Benyamina
authors.affiliation: Institut Sophia Agrobiotech, Université de Nice-Sophia Antipolis, 400 Route des Chappes, BP167, 06903 Sophia Antipolis Cedex, France; Institut Sophia Agrobiotech, INRA UMR 1355, 400 Route des Chappes, BP167, 06903 Sophia Antipolis Cedex, France; Institut Sophia Agrobiotech, CNRS UMR 7254, 400 Route des Chappes, BP167, 06903 Sophia Antipolis Cedex, France.
authors.forename: Annie
authors.initials: A
authors.lastname: Lambert
authors.affiliation: Institut Sophia Agrobiotech, Université de Nice-Sophia Antipolis, 400 Route des Chappes, BP167, 06903 Sophia Antipolis Cedex, France; Institut Sophia Agrobiotech, INRA UMR 1355, 400 Route des Chappes, BP167, 06903 Sophia Antipolis Cedex, France; Institut Sophia Agrobiotech, CNRS UMR 7254, 400 Route des Chappes, BP167, 06903 Sophia Antipolis Cedex, France.
authors.forename: Julie
authors.initials: J
authors.lastname: Hopkins
authors.affiliation: Institut Sophia Agrobiotech, Université de Nice-Sophia Antipolis, 400 Route des Chappes, BP167, 06903 Sophia Antipolis Cedex, France; Institut Sophia Agrobiotech, INRA UMR 1355, 400 Route des Chappes, BP167, 06903 Sophia Antipolis Cedex, France; Institut Sophia Agrobiotech, CNRS UMR 7254, 400 Route des Chappes, BP167, 06903 Sophia Antipolis Cedex, France.
authors.forename: Claude
authors.initials: C
authors.lastname: Castella
authors.affiliation: Institut de Pharmacologie Moléculaire et Cellulaire, CNRS UMR 7275, Université Côte d'Azur, Sophia Antipolis, 660 Route des Lucioles, Valbonne 06560, France.
authors.forename: Julie
authors.initials: J
authors.lastname: Cazareth
authors.affiliation: Institut Sophia Agrobiotech, Université de Nice-Sophia Antipolis, 400 Route des Chappes, BP167, 06903 Sophia Antipolis Cedex, France; Institut Sophia Agrobiotech, INRA UMR 1355, 400 Route des Chappes, BP167, 06903 Sophia Antipolis Cedex, France; Institut Sophia Agrobiotech, CNRS UMR 7254, 400 Route des Chappes, BP167, 06903 Sophia Antipolis Cedex, France.
authors.forename: Geneviève
authors.initials: G
authors.lastname: Alloing
authors.affiliation: Institut Sophia Agrobiotech, Université de Nice-Sophia Antipolis, 400 Route des Chappes, BP167, 06903 Sophia Antipolis Cedex, France; Institut Sophia Agrobiotech, INRA UMR 1355, 400 Route des Chappes, BP167, 06903 Sophia Antipolis Cedex, France; Institut Sophia Agrobiotech, CNRS UMR 7254, 400 Route des Chappes, BP167, 06903 Sophia Antipolis Cedex, France.
authors.forename: Eric
authors.initials: E
authors.lastname: Boncompagni
authors.affiliation: Université de Lorraine, Interactions Arbres-Microorganismes, UMR1136, 54500 Vandoeuvre-lès-Nancy, France; INRA, Interactions Arbres-Microorganismes, UMR1136, 54280 Champenoux, France.
authors.forename: Jérémy
authors.initials: J
authors.lastname: Couturier
authors.affiliation: Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS, University Paris-Sud, Université Paris-Saclay, 91198 Gif-sur-Yvette Cedex, France.
authors.forename: Peter
authors.initials: P
authors.lastname: Mergaert
authors.affiliation: INRA, Laboratoire des Interactions Plantes-Microorganismes (LIPM), UMR441, Castanet-Tolosan 31326, France; CNRS, Laboratoire des Interactions Plantes-Microorganismes (LIPM), UMR2594, Castanet-Tolosan 31326, France.
authors.forename: Pascal
authors.initials: P
authors.lastname: Gamas
authors.affiliation: Université de Lorraine, Interactions Arbres-Microorganismes, UMR1136, 54500 Vandoeuvre-lès-Nancy, France; INRA, Interactions Arbres-Microorganismes, UMR1136, 54280 Champenoux, France.
authors.forename: Nicolas
authors.initials: N
authors.lastname: Rouhier
authors.affiliation: IRHS, INRA, Université d'Angers, AGROCAMPUS-Ouest, SFR 4207 QUASAV, 42 Rue Georges Morel, 49071 Beaucouzé Cedex, France.
authors.forename: Françoise
authors.initials: F
authors.lastname: Montrichard
authors.affiliation: Institut Sophia Agrobiotech, Université de Nice-Sophia Antipolis, 400 Route des Chappes, BP167, 06903 Sophia Antipolis Cedex, France; Institut Sophia Agrobiotech, INRA UMR 1355, 400 Route des Chappes, BP167, 06903 Sophia Antipolis Cedex, France; Institut Sophia Agrobiotech, CNRS UMR 7254, 400 Route des Chappes, BP167, 06903 Sophia Antipolis Cedex, France. Electronic address: frendo@unice.fr.
authors.forename: Pierre
authors.initials: P
authors.lastname: Frendo
mesh_terms: D003545:Cysteine / Q000737:chemistry / Q000235:genetics / Q000378:metabolism; D018506:Gene Expression Regulation, Plant; D046913:Medicago truncatula / Q000254:growth & development* / Q000382:microbiology; D000072738:Nitrogen-Fixing Bacteria / Q000187:drug effects / Q000254:growth & development*; D010446:Peptide Fragments / Q000378:metabolism; D053204:Root Nodules, Plant / Q000254:growth & development* / Q000382:microbiology; D015398:Signal Transduction; D016962:Sinorhizobium meliloti / Q000187:drug effects / Q000254:growth & development*; D013559:Symbiosis; D013879:Thioredoxins / Q000037:antagonists & inhibitors*
chemical_list: D010446:Peptide Fragments; D013879:Thioredoxins; D003545:Cysteine
keywords: Medicago truncatula; Sinorhizobium meliloti; bacteroids; differentiation; disulfide bond reduction; nitrogen-fixing symbiosis; nodule cysteine-rich peptides; redox state; thiol modifications; thioredoxins