The Elicitation of Plant Innate Immunity by Lipooligosaccharide of Xanthomonas campestris

Abstract

Lipopolysaccharides (LPSs) and lipooligosaccharides (LOSs) are major components of the cell surface of Gram-negative bacteria with diverse roles in bacterial pathogenesis of animals and plants that include elicitation of host defenses. Little is known about the mechanisms of perception of these molecules by plants and about the associated signal transduction pathways that trigger plant immunity. Here we address the issue of the molecular basis of elicitation of plant defenses through the structural determination of the LOS of the plant pathogen Xanthomonas campestris pv. campestris strain 8004 and examination of the effects of LOS and fragments obtained by chemical treatments on the immune response in Arabidopsis thaliana. The structure shows a strong accumulation of negatively charged groups in the lipid A-inner core region and has a number of novel features, including a galacturonyl phosphate attached at a 3-deoxy-D-manno-oct-2-ulosonic acid residue and a unique phosphoramide group in the inner core region. Intact LOS and the lipid A and core oligosaccharides derived from it were all able to induce the defense-related genes PR1 and PR2 in Arabidopsis and to prevent the hypersensitive response caused by avirulent bacteria. Although LOS induced defense-related gene transcription in two temporal phases, the core oligosaccharide induced only the earlier phase, and lipid A induced only the later phase. These findings suggest that plant cells can recognize lipid A and core oligosaccharide structures within LOS to trigger defensive cellular responses and that this may occur via two distinct recognition events. Lipopolysaccharides (LPSs)2 are ubiquitous and vital components of the cell surface of Gram-negative bacteria (1, 2). They are amphiphilic macromolecules composed of a hydrophilic heteropolysaccharide (comprising the core oligosaccharide and O-specific polysaccharide or O-chain) covalently linked to a lipophilic moiety termed lipid A, which anchors these macromolecules to the outer membrane. LPSs not possessing the O-chain are termed rough LPSs or lipooligosaccharides (LOSs).In animal and insect cells, innate immune defenses are triggered by the perception of pathogen-associated molecular patterns (PAMPs), conserved and generally indispensable microbial structures including LPSs. The recognition of PAMPs by these cells is often mediated by leucine-rich repeat proteins such as Toll in Drosophila and the Toll-like receptors in mammals (3-6). Recognition of LPSs occurs through the lipid A moiety, which is responsible for most of the biological effects of LPS in animals. Lipid A toxicity in animals strongly depends on its structure and is also influenced by the covalently linked core region, which possesses immunogenic properties (1, 2).LPSs apparently have diverse roles in bacterial pathogenesis of plants. As major components of the outer membrane, LPSs are involved in the protection of bacterial cell, contributing to reduce the membrane permeability and thus allowing growth of bacterium in the unfavorable conditi...

Microarray Analysis of bacterial blight resistance 1 mutant rice infected with Xanthomonas oryzae pv. oryzae

“…4). Among the genes we detected, several were reported to be related to disease resistance, such as F-BOX STRESS INDUCED 2 (Maldonado-Calderon et al 2012), PEN3 (Xin et al 2013), RPM1-INDUCED PROTEIN KINASE (Feng et al 2012), WRKY108 (Higashi et al 2008 and BETA-1,3-GLUCANASE 2 (Silipo et al 2005). This observation supports the hypothesis that AP2 domain containing transcription factors are involved in the regulation of differentially expressed genes in bbr1.…”

Within-Species Flagellin Polymorphism inXanthomonas campestrispvcampestrisand Its Impact on Elicitation ofArabidopsis FLAGELLIN SENSING2–Dependent Defenses

“…This finding regarding flagellin does not imply that Xcc bacteria entirely escape detection by plant basal defense systems. For example, lipopolysaccharides, harpins, and cold shock proteins of X. campestris have been implicated as general elicitors of plant defense responses (Newman et al, 1995;Meyer et al, 2001;Felix and Boller, 2003;Kim et al, 2004;Silipo et al, 2005). Our results reveal that flagellin detection systems are apparently circumvented by Xcc bacteria, but plant-microbe interactions involve multiple layers of defense and counterdefense, and other elicitors of basal defenses remain that may limit plant colonization by Xcc.…”

“…In the xylem, Xcc growth causes darkening of the veins and eventual death of the infected tissue. Many aspects of Arabidopsis-Xcc interactions have been studied (Bent et al, 1992;Lummerzheim et al, 1993;Parker et al, 1993;Buell and Somerville, 1997;Hugouvieux et al, 1998;Godard et al, 2000;Korves and Bergelson, 2003;O'Donnell et al, 2003;Silipo et al, 2005). The extensive progress made by Boller and colleagues concerning Arabidopsis FLS2-mediated flagellin detection Zipfel et al, 2004) motivated our examination of Arabidopsis-Xcc interactions with respect to flagellin detection.…”

Glycan moiety of flagellin inAcidovorax avenaeK1 prevents the recognition by rice that causes the induction of immune responses

“…5,6,7,8 PAMPs include structures characteristic from pathogens such as b-glucan, polysaccharide chitin, ergosterol, lipopolysaccharides (LPS), flagellin and elongation factor-Tu. 9,10,11,12 Among these PAMPs, flagellin, a main component of the bacterial flagellum, has been the most extensively studied in regards to the recognition mechanism and signal transduction. 13,14,15,16 We previously reported that flagellin from the rice avirulent N1141 strain of gram-negative phytopathogenic bacterium, Acidovorax avenae, induces PTI including H 2 O 2 generation, while flagellin from the rice virulent K1 strain of A. avenae does not induce.…”