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Nonhost Resistance of Arabidopsis thaliana Against Alternaria alternata Involves both Pre- and Postinvasive Defenses but Is Collapsed by AAL-Toxin in the Absence of LOH2

First and fifth authors: Laboratory of Plant Pathology, and second and third authors: Laboratory of Plant Molecular Biology, Faculty of Agriculture, Tottori University, 4-101 Koyama-Minami, Tottori 680-8553, Japan; and fourth author: Department of Plant-Microbe Interactions, Graduate School of Agriculture, Kyoto University, Kyoto 606-8502, Japan.

The tomato pathotype of Alternaria alternata causes Alternaria stem canker on tomato depending upon the production of the host-specific AAL-toxin. Host defense mechanisms to A. alternata, however, are largely unknown. Here, we elucidate some of the mechanisms of nonhost resistance to A. alternata using Arabidopsis mutants. Wild-type Arabidopsis showed either no symptoms or a hypersensitive reaction (HR) when inoculated with both strains of AAL-toxin-producing and non-producing A. alternata. Yet, when these Arabidopsis penetration (pen) mutants, pen2 and pen3, were challenged with both strains of A. alternata, fungal penetration was possible. However, further fungal development and conidiation were limited on these pen mutants by postinvasion defense with HR-like cell death. Meanwhile, only AAL-toxin-producing A. alternata could invade lag one homologue (loh)2 mutants, which have a defect in the AAL-toxin resistance gene, subsequently allowing the fungus to complete its life cycle. Thus, the nonhost resistance of Arabidopsis thaliana to A. alternata consists of multilayered defense systems that include pre-invasion resistance via PEN2 and PEN3 and postinvasion resistance. However, our study also indicates that the pathogen is able to completely overcome the multilayered nonhost resistance if the plant is sensitive to the AAL-toxin, which is an effector of the toxin-dependent necrotrophic pathogen A. alternata.