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

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.

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.