Bacterial Cyclic β-(1,2)-Glucan Acts in Systemic Suppression of Plant Immune Responses

Abstract

Although cyclic glucans have been shown to be important for a number of symbiotic and pathogenic bacterium–plant interactions, their precise roles are unclear. Here, we examined the role of cyclic β-(1,2)-glucan in the virulence of the black rot pathogen Xanthomonas campestris pv campestris (Xcc). Disruption of the Xcc nodule development B (ndvB) gene, which encodes a glycosyltransferase required for cyclic glucan synthesis, generated a mutant that failed to synthesize extracellular cyclic β-(1,2)-glucan and was compromised in virulence in the model plants Arabidopsis thaliana and Nicotiana benthamiana. Infection of the mutant bacterium in N. benthamiana was associated with enhanced callose deposition and earlier expression of the PATHOGENESIS-RELATED1 (PR-1) gene. Application of purified cyclic β-(1,2)-glucan prior to inoculation of the ndvB mutant suppressed the accumulation of callose deposition and the expression of PR-1 in N. benthamiana and restored virulence in both N. benthamiana and Arabidopsis plants. These effects were seen when cyclic glucan and bacteria were applied either to the same or to different leaves. Cyclic β-(1,2)-glucan–induced systemic suppression was associated with the transport of the molecule throughout the plant. Systemic suppression is a novel counterdefensive strategy that may facilitate pathogen spread in plants and may have important implications for the understanding of plant–pathogen coevolution and for the development of phytoprotection measures.

Loss of Cellulose Synthase-Like F6 Function Affects Mixed-Linkage Glucan Deposition, Cell Wall Mechanical Properties, and Defense Responses in Vegetative Tissues of Rice

“…The actual mechanism that activates these defenses in cslf6 remains to be elucidated. It is possible that MLG oligosaccharides can function as signaling molecules to repress defense responses in wild-type plants, analogous to bacterial cyclic b-(1,2)-glucans that have been shown to suppress the plant's defense response (Rigano et al, 2007).…”

Sinorhizobium fredii HH103 cgs Mutants Are Unable to Nodulate Determinate- and Indeterminate Nodule–Forming Legumes and Overproduce an Altered EPS

“…Nevertheless, the recent finding that the application of purified X. campestris CG to Nicotiana benthamiana leaves provokes the suppression of different plant defense mechanisms (Rigano et al 2007) clearly indicates that CG, by themselves, play an important role in plant-microbe interactions.…”

“…Frequently, mutants of phytopathogenic bacterial strains (such as Agrobacterium tumefaciens and Xanthomonas campestris) unable to produce CG are also impaired in their capacity to develop plant diseases Miller 1994, 1998;Rigano et al 2007). The requirement for CG for bacterial pathogenic capacity has also been demonstrated in Brucella abortus, a cattle pathogen that can also infect humans (Arellano-Reynoso et al 2005;Ugalde 1999).…”

Botrytis cinerea Manipulates the Antagonistic Effects between Immune Pathways to Promote Disease Development in Tomato

“…Many pathogens inject a set of effector proteins into host cells through the type III secretion system to interfere with host innate immunity (Hann et al, 2010). These effectors and other virulence factors, including exopolysaccharides, have several targets for suppression, including the hypersensitive response, expression of defense-related genes, cell wall-based defenses, the plant proteasome system, stomatal closure, and the PAMP receptor (Bouarab et al, 2002;Abramovitch and Martin, 2005;Chisholm et al, 2006;Janjusevic et al, 2006;Nomura, 2006;Yun et al, 2006;Rigano et al, 2007;Hann et al, 2010). P. syringae manipulates the antagonistic effect between SA and JA to cause disease by producing an analog of JA (Brooks et al, 2005;Cui et al, 2005;Laurie-Berry et al, 2006).…”