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Bacterial Molecular Signals in the Sinorhizobium Fredii-Soybean Symbiosis

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Bacterial Molecular Signals in the Sinorhizobium Fredii-Soybean Symbiosis International Journal of Molecular Sciences Article Bacterial Molecular Signals in the Sinorhizobium fredii-Soybean Symbiosis Francisco J. López-Baena 1,*, José E. Ruiz-Sainz 1, Miguel A. Rodríguez-Carvajal 2 and José M. Vinardell 1 1 Departamento de Microbiología, Facultad de Biología, Universidad de Sevilla, Avenida de Reina Mercedes, 6, 41012 Sevilla, Spain; [email protected] (J.E.R.-S.); [email protected] (J.M.V.) 2 Departamento de Química Orgánica, Facultad de Química, Universidad de Sevilla, Profesor García González, 1, 41012 Sevilla, Spain; [email protected] * Correspondence: [email protected]; Tel.: +34-954-554-330; Fax: +34-954-557-830 Academic Editors: Peter M. Gresshoff and Brett Ferguson Received: 23 March 2016; Accepted: 5 May 2016; Published: 18 May 2016 Abstract: Sinorhizobium (Ensifer) fredii (S. fredii) is a rhizobial species exhibiting a remarkably broad nodulation host-range. Thus, S. fredii is able to effectively nodulate dozens of different legumes, including plants forming determinate nodules, such as the important crops soybean and cowpea, and plants forming indeterminate nodules, such as Glycyrrhiza uralensis and pigeon-pea. This capacity of adaptation to different symbioses makes the study of the molecular signals produced by S. fredii strains of increasing interest since it allows the analysis of their symbiotic role in different types of nodule. In this review, we analyze in depth different S. fredii molecules that act as signals in symbiosis, including nodulation factors, different surface polysaccharides (exopolysaccharides, lipopolysaccharides, cyclic glucans, and K-antigen capsular polysaccharides), and effectors delivered to the interior of the host cells through a symbiotic type 3 secretion system. Keywords: soybean; Sinorhizobium fredii; Bradyrhizobium; Nod factors; type 3 secretion system; effector; exopolysaccharide; lipopolysaccharide; cyclic glucans; K-antigen polysaccharide 1. Introduction Rhizobia are soil bacteria able to establish a symbiotic association with legumes in which a complex interchange of molecular signals is necessary for a successful infection. This molecular dialogue culminates in the formation of specialized plant structures, called nodules, on the roots and stems of the host plant. Within these structures, rhizobia differentiate into bacteroids able to fix atmospheric nitrogen into ammonia, which is used by the plant. In exchange, the legume provides an appropriate environment for bacterial growth. Legume roots exude flavonoids responsible for the induction of genes dedicated to the synthesis and secretion of specific signal molecules called Nod factors (NF), which are responsible for nodule initiation and development. In addition to NF, there are other molecules such as surface polysaccharides and proteins secreted by bacterial secretion systems that also seem to play a very important role in the establishment of an efficient symbiosis with the host plant [1]. Soybean-nodulating rhizobia are alfaproteobacteria belonging to the genera Bradyrhizobium, Mesorhizobium, Rhizobium and Sinorhizobium (Ensifer)[2,3]. Taxonomic studies have shown that Sinorhizobium (Ensifer) fredii (S. fredii) is closely related to the alfalfa microsymbiont Sinorhizobium meliloti, although their host-ranges are remarkably different. Soybean is a crop plant of enormous economic and agronomic interest [4]. S. fredii strains are potentially valuable for their use as soybean inoculants since they are able to grow much faster than Int. J. Mol. Sci. 2016, 17, 755; doi:10.3390/ijms17050755 www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2016, 17, 755 2 of 22 bradyrhizobia. In addition to marked soybean cultivar specificity (discussed later), S. fredii strains showInt. a remarkableJ. Mol. Sci. 2016, broad17, 755 host-range, being able to nodulate at least 79 different genera of legumes2 of 22 [5]. 2. Nodshow Factors a remarkable and Nodulation broad host-range, Genes being able to nodulate at least 79 different genera of legumes [5]. One of the first steps in the molecular dialog established between rhizobia and their legume host is the2. secretionNod Factors of phenolicand Nodulation compounds, Genes mainly flavonoids and isoflavonoids, by legume roots [6]. The mostOne abundant of the first flavonoids steps in the produced molecular by dialog soybean established roots are between the isoflavones rhizobia and daidzein, their legume genistein, host and coumestrolis the secretion [7,8]. These of phenolic plant signals compounds, are able mainly to diffuse flavonoids across and bacterial isoflavonoids, membranes by legume and are roots recognized [6]. by theThe bacterial most abundant protein flavonoids NodD, a positive produced transcriptional by soybean roots regulator are the that,isoflavones once activated daidzein, bygenistein, flavonoids, inducesand thecoumestrol expression [7,8]. of These bacterial plant nodulation signals are genesable to (noddiffusegenes) across by bacterial binding membranes to conserved and bacterial are promotersrecognized called by nodthe bacterialboxes [9 protein]. Bacterial NodD,nod a positivegenes code transcriptional for enzymes regulator involved that, inonce the activated synthesis by and secretionflavonoids, of lipochitooligosaccharidic induces the expression of signalbacterial molecules nodulation called genes LCOs(nod genes) or Nod by binding factors to (NF), conserved which in turnbacterial are recognized promoters by plantcalled LysM nod boxes receptor-like [9]. Bacterial kinases, nod inducing genes code different for enzymes responses involved required in the for the nodulationsynthesis process and secretion such as of root lipochitooligosaccharidic hair curling and nodule signal meristem molecules initiation called [LCOs10]. or Nod factors (NF), which in turn are recognized by plant LysM receptor-like kinases, inducing different responses NF usually contain four or five β-(1Ñ4)-linked N-acetyl-glucosamine (GlcNAc) residues and can required for the nodulation process such as root hair curling and nodule meristem initiation [10]. harbor different decorations such as acetyl, sulfate, carbamoyl, arabinose, fucose, methylfucose. Each NF usually contain four or five β-(1→4)-linked N-acetyl-glucosamine (GlcNAc) residues and can rhizobialharbor strain different produces decorations not only such oneas acetyl, but a sulfate, set of differentcarbamoyl, NF, arabinose, which arefucose, important methylfucose. for host-range Each determinationrhizobial strain [1,11 produces]. Among not theonlyS. one fredii but strains,a set of different there is NF, complete which are information important for about host-range the LCOs produceddetermination by the S. [1,11]. fredii Amongstrains NGR234,the S. fredii USDA257 strains, there and is HH103 complete (hereafter information NGR234, about USDA257 the LCOs and HH103)produced [5,12– by14 ].the The S. fredii sets ofstrains NF produced NGR234, USDA257 by HH103 and and HH103 USDA257, (hereafter which NGR234, induce USDA257 the formation and of nitrogen-fixingHH103) [5,12–14]. nodules The in sets soybeans, of NF produced are less by diverse HH103 than and thatUSDA257, of NGR234, which induce which the is Nodformation´, with of this legumenitrogen-fixing (Figure1). Thus,nodules HH103 in soybeans, and USDA257 are less diverse LCOs than are oligomersthat of NGR234, of three which to fiveis Nodβ−-(1, withÑ4)-linked this N-acetyl-glucosaminelegume (Figure 1). Thus, (GlcNAc) HH103 residues and USDA25 bearing7 LCOs an amideare oligomers bound of fatty three acyl to five residue β-(1→ (C164)-linked or C18), saturatedN-acetyl-glucosamine or unsaturated, (GlcNAc) on the non-reducing residues bearing terminal an amide GlcNAc bound residue, fatty andacyl aresidue fucose (C16 or methylfucose or C18), saturated or unsaturated, on the non-reducing terminal GlcNAc residue, and a fucose or modification at the C6 position of the reducing GlcNAc residue. In contrast, NGR234 NF are decorated methylfucose modification at the C6 position of the reducing GlcNAc residue. In contrast, NGR234 not only with (methyl-)fucose but also with acetyl, carbamoyl, N-methyl, and sulfate groups. This NF are decorated not only with (methyl-)fucose but also with acetyl, carbamoyl, N-methyl, and highsulfate diversity groups. of Nod This factors high diversity is most probablyof Nod factors one ofis most the factors probably that one accounts of the factors for the that extraordinarily accounts broadfor host the rangeextraordinarily exhibited broad by NGR234 host range [5 ].exhibited by NGR234 [5]. Figure 1. (A) Structure of nodulation factors produced by Sinorhizobium fredii HH103, USDA257, and Figure 1. (A) Structure of nodulation factors produced by Sinorhizobium fredii HH103, USDA257, and NGR234 and Nod proteins involved in their decoration. Proteins marked in blue are only found in NGR234 and Nod proteins involved in their decoration. Proteins marked in blue are only found in strain strain NGR234. Abbreviations of substituents are as follows: Ac, acetyl; Cb, carbamoyl; Me, methyl; NGR234. Abbreviations of substituents are as follows: Ac, acetyl; Cb, carbamoyl; Me, methyl; S, sulfate; S, sulfate; and (B) Comparison of Nod factors produced by different S. fredii strains, Bradyrhizobium and (japonicumB) Comparison USDA110, of Nodand Bradyrhizobium factors produced elkanii by USDA61. different S. fredii strains, Bradyrhizobium japonicum USDA110, and Bradyrhizobium elkanii USDA61. Int. J. Mol. Sci. 2016, 17, 755 3 of 22 HH103, as well as USDA257, harbors in its symbiotic plasmid two different clusters involved
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