Received October 6, 2006
Returned for revision May 29, 2007
Accepted June 6, 2007
Bacterial Cyclic
-(1,2)-Glucan Acts in Systemic Suppression of Plant Immune Responses
Luciano Ariel Rigano 1, Caroline Payette 2, Geneviève Brouillard 2, Maria Rosa Marano 3, Laura Abramowicz 1, Pablo Sebastián Torres 1, Maximina Yun 1, Atilio Pedro Castagnaro 4, Mohamed El Oirdi 2, Vanessa Dufour 2, Florencia Malamud 1, John Maxwell Dow 5, Kamal Bouarab 2*, and Adrian Alberto Vojnov 1
1 Fundación Pablo Cassará, Centro de Ciencia y Tecnología Dr. Cesar Milstein, Consejo Nacional de Investigaciones Científicas y Técnicas, Saladillo 2468 C1440FFX, Ciudad de Buenos Aires, Argentina
2 Centre de Recherche en Amélioration Végétale, Département de Biologie, Faculté des Sciences, Université de Sherbrooke, Sherbrooke, Québec J1K2R1, Canada
3 Instituto de Biología Molecular de Rosario, Departamento de Microbiología, Facultad de Ciencias, Bioquímicas y Farmacéuticas, Universidad Nacional de Rosario, S2002LRK Rosario, Argentina
4 Estación Experimental Agroindustrial Obispo Colombres, Consejo Nacional de Investigaciones Científicas y Técnicas, Universidad Nacional de Tucumán, T4101XAC Las Talitas, Tucumán, Argentina
5 BIOMERIT Research Centre, Department of Microbiology, National University of Ireland, Cork, Ireland
* To whom correspondence should be addressed. E-mail: kamal.bouarab{at}usherbrooke.ca.
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
-(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
-(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
-(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
-(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.