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Impairment of Cellulose Synthases Required for Arabidopsis Secondary Cell Wall Formation Enhances Disease Resistance^[W]

^a Centro de Biotecnología y Genómica de Plantas, Departamento de Biotecnología, Universidad Politécnica de Madrid, Escuela Técnica Superior Ingenieros Agrónomos, E-28040 Madrid, Spain
^b Laboratoire de Interactions Plantes-Microorganismes, Centre National de la Recherche Scientifique–Institut National de la Recherche Agronomique, Chemin de Borde Rouge, 31326 Castanet Tolosan Toulouse, France
^c Department of Plant Biology, Carnegie Institution, Stanford, California 94305
^d Unité Mixte de Recherche–Interactions Plantes-Microorganismes et Sante Vegetale, Centre National de la Recherche Scientifique–Institut National de la Recherche Agronomique, 06903 Sophia Antipolis Cedex, France
^e Developmental, Cell, and Molecular Biology Group, Department of Biology, Duke University, Durham, North Carolina 27708-1000

⁵ To whom correspondence should be addressed. E-mail yves.marco{at}inra.toulouse.fr or antonio.molina{at}upm.es; fax 33-61285509 or 34-913365695.

Cellulose is synthesized by cellulose synthases (CESAs) contained in plasma membrane–localized complexes. In Arabidopsis thaliana, three types of CESA subunits (CESA4/IRREGULAR XYLEM5 [IRX5], CESA7/IRX3, and CESA8/IRX1) are required for secondary cell wall formation. We report that mutations in these proteins conferred enhanced resistance to the soil-borne bacterium Ralstonia solanacearum and the necrotrophic fungus Plectosphaerella cucumerina. By contrast, susceptibility to these pathogens was not altered in cell wall mutants of primary wall CESA subunits (CESA1, CESA3/ISOXABEN RESISTANT1 [IXR1], and CESA6/IXR2) or POWDERY MILDEW–RESISTANT5 (PMR5) and PMR6 genes. Double mutants indicated that irx-mediated resistance was independent of salicylic acid, ethylene, and jasmonate signaling. Comparative transcriptomic analyses identified a set of common irx upregulated genes, including a number of abscisic acid (ABA)–responsive, defense-related genes encoding antibiotic peptides and enzymes involved in the synthesis and activation of antimicrobial secondary metabolites. These data as well as the increased susceptibility of ABA mutants (abi1-1, abi2-1, and aba1-6) to R. solanacearum support a direct role of ABA in resistance to this pathogen. Our results also indicate that alteration of secondary cell wall integrity by inhibiting cellulose synthesis leads to specific activation of novel defense pathways that contribute to the generation of an antimicrobial-enriched environment hostile to pathogens.

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