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Photosynthetic Bradyrhizobium Sp. Strain ORS285 Synthesizes 2- O

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Photosynthetic Bradyrhizobium Sp. Strain ORS285 Synthesizes 2- O Photosynthetic Bradyrhizobium Sp. Strain ORS285 Synthesizes 2- O -Methylfucosylated Lipochitooligosaccharides for nod Gene–Dependent Interaction with Aeschynomene Plants Adeline Renier, Fabienne Maillet, Joël Fardoux, Verena Poinsot, Eric Giraud, Nico Nouwen To cite this version: Adeline Renier, Fabienne Maillet, Joël Fardoux, Verena Poinsot, Eric Giraud, et al.. Photosynthetic Bradyrhizobium Sp. Strain ORS285 Synthesizes 2- O -Methylfucosylated Lipochitooligosaccharides for nod Gene–Dependent Interaction with Aeschynomene Plants. Molecular Plant-Microbe Interactions, American Phytopathological Society, 2011, 24 (12), pp.1440-1447. 10.1094/MPMI-05-11-0104. hal- 02437955 HAL Id: hal-02437955 https://hal.archives-ouvertes.fr/hal-02437955 Submitted on 29 May 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. MPMI Vol. 24, No. 12, 2011, pp. 1440–1447. doi:10.1094 / MPMI -05-11-0104. e-Xtra* Photosynthetic Bradyrhizobium Sp. Strain ORS285 Synthesizes 2-O-Methylfucosylated Lipochitooligosaccharides for nod Gene–Dependent Interaction with Aeschynomene Plants Adeline Renier,1 Fabienne Maillet,2 Joel Fardoux,1 Véréna Poinsot,3 Eric Giraud,1 and Nico Nouwen1 1Laboratoire des Symbioses Tropicales et Méditerranéennes, UMR113 IRD, Laboratoire des Symbioses Tropicales et Méditerranéennes, UMR IRD/SupAgro/INRA/UM2/CIRAD, F-34398 Montpellier, France; 2Laboratoire des Interactions plantes/microorganismes LIPM, UMR441/2594 INRA/CNRS 441/2594, 24 chemin de Borde Rouge, 31326 Castanet- Tolosan, France; 3Laboratoire des Interactions Moléculaires et Réactivité Chimique et Photochimique, UMR 5623 CNRS/Université Paul Sabatier, 118 Route de Narbonne, F-31062 Toulouse, France Submitted 3 May 2011. Accepted 15 August 2011. Bradyrhizobium sp. strain ORS285 is a photosynthetic bac- cules produced by both bacteria and plants (Spaink 1992). Le- terium that forms nitrogen-fixing nodules on the roots and guminous plants synthesize and exude a diverse array of stems of tropical aquatic legumes of the Aeschynomene ge- phenolic compounds such as flavonoids into the rhizosphere. nus. The symbiotic interaction of Bradyrhizobium sp. strain These compounds serve as chemoatractants for rhizobia, influ- ORS285 with certain Aeschynomene spp. depends on the ence bacterial growth, and selectively induce the expression of presence of nodulation (nod) genes whereas the interaction bacterial nodulation (nod) genes, leading to the biosynthesis of with other species is nod gene independent. To study the the bacterial signal molecules, the Nod factors (NF) (Caetano- nod gene-dependent molecular dialogue between Bradyrhi- Anolles et al. 1988; Dharmatilake and Bauer 1992). NF are zobium sp. strain ORS285 and Aeschynomene spp., we used composed of three to five 1-4 -linked N-acetyl glucasamine a nodB-lacZ reporter strain to monitor the nod gene ex- units (GlcNac) with the N-acetyl group of the terminal nonre- pression with various flavonoids. The flavanones liquiriti- ducing sugar replaced by an acyl chain with 16 or 18 carbons genin and naringenin were found to be the strongest induc- and with varying degrees of saturation. Various modifications ers of nod gene expression. Chemical analysis of the culture at both reducing and nonreducing termini of the chitin back- supernatant of cells grown in the presence of naringenin bone are possible, such as methylation, acetylation, carbamoy- showed that the major Nod factor produced by Bradyrhizo- lation, fycosylation, or sulfation (D’Haeze and Holsters 2002; bium sp. strain ORS285 is a modified chitin pentasaccha- Perret et al. 2000). The structure of the fatty acyl chain, the ride molecule with a terminal N-C18:1-glucosamine and number of GlcNac residues, and the presence of extra substitu- with a 2-O-methyl fucose linked to C-6 of the reducing glu- ents determine the host specificity of the bacterium (Denarie et cosamine. In this respect, the Bradyrhizobium sp. strain al. 1996). Thus, it is not surprising that broad host range sym- ORS285 Nod factor is the same as the major Nod factor bionts such as Rhizobium sp. strain NGR234, Rhizobium produced by the nonphotosynthetic Bradyrhizobium japoni- fredii, R. tropici, and certain Bradyrhizobium spp. produce a cum USDA110 that nodulates the roots of soybean. This range of NF (Bec-Ferte et al. 1996; Carlson et al. 1993; Poupot suggests a classic nod gene-dependent molecular dialogue et al. 1993; Price et al. 1992). between Bradyrhizobium sp. strain ORS285 and certain Photosynthetic Bradyrhizobium spp. establish a symbiotic Aeschynomene spp. This is supported by the fact that B. ja- interaction with tropical aquatic legumes of the Aeschynomene ponicum USDA110 is able to form N2-fixing nodules on genus (Giraud and Fleischman 2004). In addition to being both the roots and stems of Aeschynomene afraspera. photosynthetic, these bacteria and the interaction with Aes- chynomene have other atypical characteristics compared with the classical and well-studied rhizobia–legume interaction. Rhizobia have the ability to establish a symbiotic relation- First, photosynthetic Bradyrhizobium spp. are able to fix nitro- ship with leguminous plants. In this association, the bacteria gen in the free living state (Alazard 1990). Second, in addition induce the plant to develop a new organ, the nodule, in which to nodulating roots, photosynthetic Bradyrhizobium spp. are the symbiont resides and fixes atmospheric nitrogen. This com- also able to nodulate the stems of Aeschynomene plants plex interorganismal relationship is mediated by signal mole- (Alazard 1985). Third, the infection process of the plant does not involve root hair curling but bacteria enter the plant via epidermal fissures (“cracks”) generated by the emergence of Corresponding author: N. Nouwen; E-mail: [email protected] lateral or adventive roots (Sprent 2008). Fourth, certain photo- synthetic Bradyrhizobium spp. (ORS278 and BTAi1) lack the *The e-Xtra logo stands for “electronic extra” and indicates that one sup- genes that encode the enzymes that synthesize the core struc- plementary figure is published online and Figure 5 appears in color online. ture of NF (nodABC) (Giraud et al. 2007). This indicates that some photosynthetic Bradyrhizobium spp. likely use a novel This article is in the public domain and not copyrightable. It may be freely reprinted with customary crediting of the source. The American Phyto- mechanism, independent of the long-time considered universal pathological Society, 2011. NF to interact with their legume hosts. 1440 / Molecular Plant-Microbe Interactions Photosynthetic Bradyrhizobium sp. strain ORS285 has a porter strain in the presence of flavonoids of different func- broad host range and interacts with many plants in the Aes- tional classes (Fig. 1) showed that the flavanones liquiriti- chynomene genus (Molouba et al. 1999). In contrast to the re- genin and naringenin result in the highest induction of - cently (completely) sequenced photosynthetic Bradyrhizobium galactosidase activity (Table 1). Because both activities were sp. strains ORS278 and BTAi1 (Giraud et al. 2007), strain not significantly different, C5 hydroxylation (as found in nar- ORS285 contains the nodABC genes (Chaintreuil et al. 2001). ingenin) seems not to be very important for inducing capac- However, whereas a deletion of the nodBC genes in Bradyrhi- ity. C3 hydroxylation of flavanones leads to a twofold reduc- zobium sp. strain ORS285 results in the inhibition of nodula- tion in -galactosidase activity, whereas flavanones with a tion of certain plants in the Aeschynomene genus, the mutant methoxy or glucoside at the C7 position (naringenin-7-O- was still able to interact with a subgroup of plants that are glucoside, sakuranetin, and sakuranin) are inactive. Flavones nodulated by photosynthetic Bradyrhizobium spp. that do not are approximately twofold less active in induction of nodB- contain nodABC genes (Giraud et al. 2007). This indicates that lacZ expression compared with flavanones. As with flavan- Bradyrhizobium sp. strain ORS285 interacts with certain Aes- ones, attachment of a glucoside at the C7 position (apigenin- chynomene plants in a nod gene-dependent manner whereas, 7-O-glucoside and luteolin-7-O-glucoside) results in a com- with others, it is using (or can use) a nod gene-independent mechanism. In many aspects, the interaction between photosynthetic Bradyrhizobium spp. and Aeschynomene spp. is different from the classical rhizobia–legume interaction; therefore, the aim of this study was to determine which signal molecules are in- volved in the nod gene-dependent molecular dialogue between photosynthetic Bradyrhizobium sp. strain ORS285 and Aeschy- nomene spp. (i.e., the flavonoids that induce the expression of the nodABC operon and the determination of the NF structures produced by the bacterium). RESULTS The flavanones liquiritigenin and naringenin are strong inducers of nodB expression. The photosynthetic Bradyrhizobium sp. strain ORS285 con- tains an operon containing the common nod genes (nodABC) (Chaintreuil et al. 2001) that
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