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J. Biol. Chem., Vol. 280, Issue 39, 33660-33668, September 30, 2005

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The Elicitation of Plant Innate Immunity by Lipooligosaccharide of Xanthomonas campestris^*

Alba Silipo, Antonio Molinaro1, Luisa Sturiale, J. Maxwell Dow¶, Gitte Erbs||, Rosa Lanzetta, Mari-Anne Newman||, and Michelangelo Parrilli

From the Dipartimento di Chimica Organica e Biochimica, Università di Napoli Federico II, Complesso Universitario Monte Sant' Angelo, Via Cintia 4, 80126 Napoli, Italy, and Istituto per la Chimica e la Tecnologia dei Materiali Polimerici, ICTMP, CNR, 95123 Catania, Italy, ^¶BIOMERIT Research Centre, Department of Microbiology, BioSciences Institute, National University of Ireland, Cork, Ireland, and the ^||Section for Plant Pathology, Royal Veterinary and Agricultural University, 1871 Copenhagen, Denmark

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.

Received for publication, June 8, 2005 , and in revised form, July 21, 2005.

^* The work at Università di Napoli was supported by a grant from MIUR, Rome (Progetti di Ricerca di Interesse Nazionale, 2004) (to M. P.). The work at the Biomerit Research Centre was supported by the Science Foundation of Ireland through Investigator Award 03/IN3/B373. The work at the Royal Veterinary and Agricultural University was supported by the Danish Agricultural and Veterinary Research Council. This work was also supported by Carlsbergfondet (Copenhagen, Denmark). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains supplemental Figs. 1 and 2.

¹ To whom correspondence should be addressed. Tel.: 39-081-674123; Fax: 39-081-674393; E-mail: molinaro{at}unina.it.

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