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Pseudomonas protegens Pf-5 Causes Discoloration and Pitting of Mushroom Caps Due to the Production of Antifungal Metabolites

July 2014 , Volume 27 , Number  7
Pages  733 - 746

Marcella D. Henkels,1,2 Teresa A. Kidarsa,2 Brenda T. Shaffer,2 Neal C. Goebel,3 Peter Burlinson,4 Dmitri V. Mavrodi,5 Michael A. Bentley,4 Lorena I. Rangel,1 Edward W. Davis II,1,2 Linda S. Thomashow,6 T. Mark Zabriskie,3 Gail M. Preston,4 and Joyce E. Loper1,2

1Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR 97331, U.S.A.; 2Agricultural Research Service, U.S. Department of Agriculture, 3420 N.W. Orchard Ave., Corvallis, OR 97330, U.S.A.; 3Department of Pharmaceutical Sciences, Oregon State University; 4Department of Plant Sciences, University of Oxford, South Parks Road, Oxford, OX1 3RB, U.K.; 5Department of Biological Sciences, University of Southern Mississippi, Hattiesburg, MS 39406, U.S.A.; 6Agricultural Research Service, U.S. Department of Agriculture, Department of Plant Pathology, Washington State University, Pullman, WA 99164, U.S.A.

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Accepted 10 March 2014.

Bacteria in the diverse Pseudomonas fluorescens group include rhizosphere inhabitants known for their antifungal metabolite production and biological control of plant disease, such as Pseudomonas protegens Pf-5, and mushroom pathogens, such as Pseudomonas tolaasii. Here, we report that strain Pf-5 causes brown, sunken lesions on peeled caps of the button mushroom (Agaricus bisporus) that resemble brown blotch symptoms caused by P. tolaasii. Strain Pf-5 produces six known antifungal metabolites under the control of the GacS/GacA signal transduction system. A gacA mutant produces none of these metabolites and did not cause lesions on mushroom caps. Mutants deficient in the biosynthesis of the antifungal metabolites 2,4-diacetylphloroglucinol and pyoluteorin caused less-severe symptoms than wild-type Pf-5 on peeled mushroom caps, whereas mutants deficient in the production of lipopeptide orfamide A caused similar symptoms to wild-type Pf-5. Purified pyoluteorin and 2,4-diacetylphloroglucinol mimicked the symptoms caused by Pf-5. Both compounds were isolated from mushroom tissue inoculated with Pf-5, providing direct evidence for their in situ production by the bacterium. Although the lipopeptide tolaasin is responsible for brown blotch of mushroom caused by P. tolaasii, P. protegens Pf-5 caused brown blotch–like symptoms on peeled mushroom caps through a lipopeptide-independent mechanism involving the production of 2,4-diacetylphloroglucinol and pyoluteorin.

This article is in the public domain and not copyrightable. It may be freely reprinted with customary crediting of the source. The American Phytopathological Society, 2014.