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Plant Microbiology

An Interspecies Signaling System Mediated by Fusaric Acid Has Parallel Effects on Antifungal Metabolite Production by Pseudomonas protegens Strain Pf-5 and Antibiosis of Fusarium spp.

Maria Carolina Quecine, Teresa A. Kidarsa, Neal C. Goebel, Brenda T. Shaffer, Marcella D. Henkels, T. Mark Zabriskie, Joyce E. Loper
J. L. Schottel, Editor
Maria Carolina Quecine
aDepartment of Genetics, College of Agriculture Luiz de Queiroz, ESALQ, University of São Paulo, Piracicaba, São Paulo, Brazil
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Teresa A. Kidarsa
bAgricultural Research Service, U.S. Department of Agriculture, Corvallis, Oregon, USA
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Neal C. Goebel
cDepartment of Pharmaceutical Sciences, Oregon State University, Corvallis, Oregon, USA
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Brenda T. Shaffer
bAgricultural Research Service, U.S. Department of Agriculture, Corvallis, Oregon, USA
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Marcella D. Henkels
bAgricultural Research Service, U.S. Department of Agriculture, Corvallis, Oregon, USA
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T. Mark Zabriskie
cDepartment of Pharmaceutical Sciences, Oregon State University, Corvallis, Oregon, USA
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Joyce E. Loper
bAgricultural Research Service, U.S. Department of Agriculture, Corvallis, Oregon, USA
dDepartment of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon, USA
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J. L. Schottel
University of Minnesota
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DOI: 10.1128/AEM.02574-15
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ABSTRACT

Pseudomonas protegens strain Pf-5 is a rhizosphere bacterium that suppresses soilborne plant diseases and produces at least seven different secondary metabolites with antifungal properties. We derived mutants of Pf-5 with single and multiple mutations in biosynthesis genes for seven antifungal metabolites: 2,4-diacetylphoroglucinol (DAPG), pyrrolnitrin, pyoluteorin, hydrogen cyanide, rhizoxin, orfamide A, and toxoflavin. These mutants were tested for inhibition of the pathogens Fusarium verticillioides and Fusarium oxysporum f. sp. pisi. Rhizoxin, pyrrolnitrin, and DAPG were found to be primarily responsible for fungal antagonism by Pf-5. Previously, other workers showed that the mycotoxin fusaric acid, which is produced by many Fusarium species, including F. verticillioides, inhibited the production of DAPG by Pseudomonas spp. In this study, amendment of culture media with fusaric acid decreased DAPG production, increased pyoluteorin production, and had no consistent influence on pyrrolnitrin or orfamide A production by Pf-5. Fusaric acid also altered the transcription of biosynthetic genes, indicating that the mycotoxin influenced antibiotic production by Pf-5 at the transcriptional level. Addition of fusaric acid to the culture medium reduced antibiosis of F. verticillioides by Pf-5 and derivative strains that produce DAPG but had no effect on antibiosis by Pf-5 derivatives that suppressed F. verticillioides due to pyrrolnitrin or rhizoxin production. Our results demonstrated the importance of three compounds, rhizoxin, pyrrolnitrin, and DAPG, in suppression of Fusarium spp. by Pf-5 and confirmed that an interspecies signaling system mediated by fusaric acid had parallel effects on antifungal metabolite production and antibiosis by the bacterial biological control organism.

We dedicate this article to the late Aline A. Pizzirani-Kleiner, without whom this study could not have been done.

FOOTNOTES

    • Received 7 August 2015.
    • Accepted 3 December 2015.
    • Accepted manuscript posted online 11 December 2015.
  • Supplemental material for this article may be found at http://dx.doi.org/10.1128/AEM.02574-15.

  • Copyright © 2016, American Society for Microbiology. All Rights Reserved.
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An Interspecies Signaling System Mediated by Fusaric Acid Has Parallel Effects on Antifungal Metabolite Production by Pseudomonas protegens Strain Pf-5 and Antibiosis of Fusarium spp.
Maria Carolina Quecine, Teresa A. Kidarsa, Neal C. Goebel, Brenda T. Shaffer, Marcella D. Henkels, T. Mark Zabriskie, Joyce E. Loper
Applied and Environmental Microbiology Feb 2016, 82 (5) 1372-1382; DOI: 10.1128/AEM.02574-15

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An Interspecies Signaling System Mediated by Fusaric Acid Has Parallel Effects on Antifungal Metabolite Production by Pseudomonas protegens Strain Pf-5 and Antibiosis of Fusarium spp.
Maria Carolina Quecine, Teresa A. Kidarsa, Neal C. Goebel, Brenda T. Shaffer, Marcella D. Henkels, T. Mark Zabriskie, Joyce E. Loper
Applied and Environmental Microbiology Feb 2016, 82 (5) 1372-1382; DOI: 10.1128/AEM.02574-15
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