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Biological control of soil-borne pathogens by fluorescent pseudomonads

Key Points

  • In suppressive soils, crop plants are protected from soil-borne root pathogens (mostly fungi). Disease suppression depends on the prevailing environmental conditions in the soil and, moreover, has a strong biological component, which consists of root-colonizing plant-beneficial bacteria and fungi. Among these plant-beneficial 'probiotic' microorganisms, selected strains of fluorescent pseudomonads have been studied extensively for biocontrol mechanisms using both biochemical and molecular genetic approaches.

  • Many biocontrol strains of fluorescent pseudomonads produce extracellular secondary metabolites that inhibit the growth of fungal pathogens and account for part of the disease-suppressive activity. Siderophores (iron chelators) are occasionally involved in biocontrol but do not seem to have the crucial role that was once attributed to them.

  • Induced systemic resistance in the host plant is a second important mechanism that is involved in the biocontrol of root pathogens. Although it remains unclear which bacterial signals are most apt to elicit resistance, the jasmonate- and ethylene-responsive defence pathways seem to be most important in the host plant, as judged from experiments with mutants of Arabidopsis thaliana.

  • Subtle interactions between a pathogen and a biocontrol agent can tip the balance in favour of plant disease or health. The evidence for such direct and specific interactions is still fragmentary, and is limited to few well-studied cases.

  • Progress has been made recently in the understanding of the molecular mechanisms that regulate the expression of biocontrol factors in fluorescent pseudomonads. At the transcriptional level, several secondary metabolites positively regulate the expression of their own biosynthetic genes. At a post-transcriptional level, small noncoding RNAs that are controlled by the GacS/GacA two-component system can relieve the repressive action that RNA-binding proteins exert on the expression of target mRNAs. These small RNAs therefore determine the expression of biocontrol factors.

  • The soil, the plant, the pathogen and the biocontrol agent interact with each other through both biotic and abiotic signals, many of which remain unknown. A better understanding of these signals and their mode of action might facilitate the practical application of biocontrol microorganisms in the future.

Abstract

Particular bacterial strains in certain natural environments prevent infectious diseases of plant roots. How these bacteria achieve this protection from pathogenic fungi has been analysed in detail in biocontrol strains of fluorescent pseudomonads. During root colonization, these bacteria produce antifungal antibiotics, elicit induced systemic resistance in the host plant or interfere specifically with fungal pathogenicity factors. Before engaging in these activities, biocontrol bacteria go through several regulatory processes at the transcriptional and post-transcriptional levels.

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Figure 1: Interactions between biocontrol plant growth-promoting rhizobacteria (PGPR), plants, pathogens and soil.
Figure 2: The antibiotic compounds produced by fluorescent pseudomonads that are relevant for biocontrol.
Figure 3: Root colonization by fluorescent pseudomonads.
Figure 4: Protection of wheat from Pythium ultimum by Pseudomonas fluorescens.
Figure 5: Model of the GacS/GacA signal-transduction pathway in Pseudomonas fluorescens strain CHA0.

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Acknowledgements

We thank R. Wittek, C. Reimmann and L. Tomashow for critically reading the manuscript, and C. Keel for providing Fig. 4. D.H. thanks P. Rainey and J. Kistler for their hospitality during the time when this review was written. Support from the Swiss National Science Foundation is gratefully acknowledged.

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Glossary

SUPPRESSIVE SOIL

A soil in which plants do not suffer from certain diseases or where disease severity is reduced, although a pathogen might be present, and the host plant is susceptible to the disease; the opposite of a conducive soil. Suppressive soils occur worldwide.

CONDUCIVE SOIL

A soil that allows the development of disease; the opposite of a suppressive soil.

RHIZOSPHERE

A nutrient-rich zone near (that is, a few millimetres from) the roots, where microbial growth is stimulated by root exudates (the rhizosphere effect).

ANTIBIOSIS

A condition in which one or several metabolites that are excreted by an organism have a harmful effect on other organisms. There is no evidence to indicate that antibiotic compounds that are produced in nature result in substantial killing of susceptible organisms.

MICROCOSM

A closed system that contains all the biotic and abiotic components of interest, and mimics environmental conditions in the laboratory.

AXENIC SYSTEM

Conditions in which the biological components to be studied, but no foreign organisms, are present.

PROBIOTICS

Microorganisms that have beneficial effects on their host. This term is commonly used for microorganisms that survive passage through the gastrointestinal tract and might prevent, or even cure, diarrhoea.

ANR

A transcription factor in the FNR family, responsive to low oxygen concentrations.

GACS/GACA

A two-component system controlling the global activation of exoproduct (for example, antibiotics and cyanide) synthesis. GacS/GacA is found in many Gram-negative bacteria.

VERMICULITE CLAY

A hydrous aluminium silicate clay mineral that is rich in magnesium and iron.

ILLITE CLAY

A hydrous aluminium silicate clay mineral that is rich in potassium.

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Haas, D., Défago, G. Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat Rev Microbiol 3, 307–319 (2005). https://doi.org/10.1038/nrmicro1129

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