Pseudomonas protegens Pf-5 causes discoloration and pitting of mushroom caps due to the production of antifungal metabolites

Marcella D. Henkels, Teresa A. Kidarsa, Brenda T. Shaffer, Neal C. Goebel, Peter Burlinson, Dmitri V. Mavrodi, Michael A. Bentley, Lorena I. Rangel, Edward W. Davis, Linda S. Thomashow, Mark Zabriskie, Gail M. Preston, Joyce E. Loper

Research output: Contribution to journalArticle

11 Citations (Scopus)

Abstract

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.

Original languageEnglish (US)
Pages (from-to)733-746
Number of pages14
JournalMolecular Plant-Microbe Interactions
Volume27
Issue number7
DOIs
StatePublished - 2014
Externally publishedYes

Fingerprint

Agaricales
discoloration
Pseudomonas
mushrooms
Pseudomonas tolaasii
metabolites
signs and symptoms (plants)
lipopeptides
Lipopeptides
lesions (plant)
mutants
Pseudomonas fluorescens group
Agaricus
Bacteria
Plant Diseases
Pseudomonas fluorescens
Rhizosphere
Agaricus bisporus
bacteria
plant diseases and disorders

ASJC Scopus subject areas

  • Physiology
  • Agronomy and Crop Science

Cite this

Henkels, M. D., Kidarsa, T. A., Shaffer, B. T., Goebel, N. C., Burlinson, P., Mavrodi, D. V., ... Loper, J. E. (2014). Pseudomonas protegens Pf-5 causes discoloration and pitting of mushroom caps due to the production of antifungal metabolites. Molecular Plant-Microbe Interactions, 27(7), 733-746. https://doi.org/10.1094/MPMI-10-13-0311-R

Pseudomonas protegens Pf-5 causes discoloration and pitting of mushroom caps due to the production of antifungal metabolites. / Henkels, Marcella D.; Kidarsa, Teresa A.; Shaffer, Brenda T.; Goebel, Neal C.; Burlinson, Peter; Mavrodi, Dmitri V.; Bentley, Michael A.; Rangel, Lorena I.; Davis, Edward W.; Thomashow, Linda S.; Zabriskie, Mark; Preston, Gail M.; Loper, Joyce E.

In: Molecular Plant-Microbe Interactions, Vol. 27, No. 7, 2014, p. 733-746.

Research output: Contribution to journalArticle

Henkels, MD, Kidarsa, TA, Shaffer, BT, Goebel, NC, Burlinson, P, Mavrodi, DV, Bentley, MA, Rangel, LI, Davis, EW, Thomashow, LS, Zabriskie, M, Preston, GM & Loper, JE 2014, 'Pseudomonas protegens Pf-5 causes discoloration and pitting of mushroom caps due to the production of antifungal metabolites', Molecular Plant-Microbe Interactions, vol. 27, no. 7, pp. 733-746. https://doi.org/10.1094/MPMI-10-13-0311-R
Henkels, Marcella D. ; Kidarsa, Teresa A. ; Shaffer, Brenda T. ; Goebel, Neal C. ; Burlinson, Peter ; Mavrodi, Dmitri V. ; Bentley, Michael A. ; Rangel, Lorena I. ; Davis, Edward W. ; Thomashow, Linda S. ; Zabriskie, Mark ; Preston, Gail M. ; Loper, Joyce E. / Pseudomonas protegens Pf-5 causes discoloration and pitting of mushroom caps due to the production of antifungal metabolites. In: Molecular Plant-Microbe Interactions. 2014 ; Vol. 27, No. 7. pp. 733-746.
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abstract = "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.",
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AU - Henkels, Marcella D.

AU - Kidarsa, Teresa A.

AU - Shaffer, Brenda T.

AU - Goebel, Neal C.

AU - Burlinson, Peter

AU - Mavrodi, Dmitri V.

AU - Bentley, Michael A.

AU - Rangel, Lorena I.

AU - Davis, Edward W.

AU - Thomashow, Linda S.

AU - Zabriskie, Mark

AU - Preston, Gail M.

AU - Loper, Joyce E.

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N2 - 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.

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