Disease suppressive soils offer effective protection to plants against infection by soil-borne pathogens, including fungi, oomycetes, bacteria, and nematodes. The specific disease suppression that operates in these soils is, in most cases, microbial in origin. Therefore, suppressive soils are considered as a rich resource for the discovery of beneficial microorganisms with novel antimicrobial and other plant protective traits. To date, several microbial genera have been proposed as key players in disease suppressiveness of soils, but the complexity of the microbial interactions as well as the underlying mechanisms and microbial traits remain elusive for most disease suppressive soils.

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Disease suppressive soils offer effective protection to plants against infection by soil-borne pathogens, including fungi, oomycetes, bacteria, and nematodes. The specific disease suppression that operates in these soils is, in most cases, microbial in origin. Therefore, suppressive soils are considered as a rich resource for the discovery of beneficial microorganisms with novel antimicrobial and other plant protective traits. To date, several microbial genera have been proposed as key players in disease suppressiveness of soils, but the complexity of the microbial interactions as well as the underlying mechanisms and microbial traits remain elusive for most disease suppressive soils.

Disease suppressive soils are the best examples of microbiome-mediated protection of plants against root infections by soil-borne pathogens. Two types of disease suppressiveness are distinguished. General suppressiveness of soils is attributed to the activity of the collective microbial community and is often associated with competition for available resources Mazzola, ; Weller et al. General suppressiveness of soils can be boosted by addition of organic matter Bonanomi et al.

Specific suppressiveness is due to the concerted activities of specific groups of microorganisms that interfere with some stage of the life cycle of the soil-borne pathogen. The characteristics of general and specific suppressiveness have remarkable similarities with the innate and adaptive immune responses in animals Raaijmakers and Mazzola, That is, the innate immune response in animals gives a primary and non-specific defensive response similar to what occurs in general suppressiveness of soils.

The adaptive immune response in animals and specific disease suppression in soils both require specialized cells to suppress the pathogen, require time and have a memory Lapsansky et al. Hence, a mechanistic understanding of the soil immune response may enable us to engineer the soil and plant microbiomes to enrich for specific groups of antagonistic microbes and activities as a sustainable alternative to control plant diseases and to enhance crop productivity Berendsen et al.

Here, we will first highlight the most important findings of past studies on microbes and mechanisms involved in specific disease suppressiveness of soils. The first suppressive soil was reported in by Atkinson for Fusarium wilt disease of cotton Atkinson, ; Scher and Baker, ; Amir and Alabouvette, ; Lemanceau et al. Since then, specific suppressiveness of soils has been reported for a range of pathogens, including fungi such as Gaeumannomyces graminis var tritici Raaijmakers and Weller, ; De Souza et al.

The microbiological basis of disease suppressive soils was first addressed by Henry a , b and later widely demonstrated in other studies via soil pasteurization, application of biocides Scher and Baker, ; Alabouvette, ; Mazzola, ; Weller et al.

Furthermore, higher microbial diversities have been detected in disease suppressive soils than in conducive soils Garbeva et al. Following these observations and approaches, various microbes and underlying mechanisms involved in specific disease suppressiveness were proposed and, in several cases, identified.

The mechanisms underlying specific suppressiveness identified in these early studies include competition, parasitism and antibiosis Kloepper et al. For Fusarium wilt suppressive soils, competition for carbon by non-pathogenic F.

Addition of siderophore-producing Pseudomonas from suppressive soils or their siderophores into conducive soils rendered these soils suppressive to F.

The role of parasitism in disease suppressive soils has been studied for several soil-borne pathogens including the fungi S.

Fradkin and Patrick, , and the oomycetes P. Parasitic microorganisms identified in these studies were mostly fungi e. Despite the widespread distribution of rhizosphere bacteria with parasitic traits, such as the production of cell wall degrading enzymes, there are no studies that have conclusively demonstrated their role in specific disease suppressiveness of soils.

For example, strains of Stenotrophomonas maltophilia can suppress the oomycete P. Furthermore, bacteria within the genus Collimonas produce chitinases and have been reported to feed on fungi De Boer et al. Whether these or other mycoparasitic rhizobacterial genera are enriched or more active in disease suppressive soils is, to our knowledge, not yet known. Among the antibiotics with a role in disease suppressive soils, 2,4-diacetylphloroglucinol DAPG and phenazines PHZ have been studied in more depth Haas and Defago, ; Raaijmakers and Mazzola, DAPG and pyrrolnitrin were shown to be involved in suppression of R.

Volatile compounds with antimicrobial activities have also been proposed to play a role in disease suppressiveness of soils. Early studies indicated a role of ammonia Ko et al.

Following this line of research, several microbial genera have been proposed for their role in specific disease suppressiveness. These include fluorescent Pseudomonas Kloepper et al. Although several microorganisms efficiently controlled the target pathogen under in vitro or greenhouse conditions, the majority failed under field environments. This inconsistency in in vivo activity has been mainly attributed to an insufficient ability to survive and colonize the rhizosphere or to express their protective characteristics under field conditions at the right time and right place Alabouvette et al.

Also, disease suppressiveness is generally thought to be attributed to microbial consortia rather than to one microbial species only. For example, PHZ-producing Pseudomonas isolated from a Fusarium wilt suppressive soil could suppress Fusarium wilt disease of flax only when re-introduced with non-pathogenic F. For example, bacterial and fungal diversity analyzed by DGGE and subsequent sequencing of the isolated bands showed a higher abundance of the fungi Aspergillus penicillioides, Eurotium sp.

Also dominance of Fusarium spp. Additionally, Cretoiu et al. Using PhyloChip analyses of the rhizobacterial community compositions in soils suppressive or conducive to the fungal root pathogen R. The results of these and other recent studies are summarized in Table 1 and discussed below with emphasis on the role of soil and rhizosphere bacteria.

TABLE 1. Summary of microbial taxa associated with disease suppressive soils and identified by different cultivation-independent techniques. A wide range of bacterial taxa were found in higher abundance in suppressive soils Table 1. With regard to fungi, Penton et al. Among the fungi most frequently associated with disease suppressive soils to other pathogens are Mortierella, Trichoderma, Fusarium , and Malasezzia Table 1. Recently, Poudel et al.

However, these descriptive analyses need to be combined with other techniques to pinpoint the specific microbial traits involved in suppressiveness and to distinguish between cause and effect. Mechanistically, recent studies pointed to antimicrobial volatiles, including sesquiterpenes Minerdi et al. In these studies, however, these volatile compounds were detected under in vitro conditions and their production in vivo should be validated to provide more conclusive proof of the role of antimicrobial volatiles in disease suppressiveness of soils.

Nevertheless, its validation in situ has technical challenges since volatile-producing microorganisms should be positioned in their ecological context the rhizosphere but also physically separated from the pathogen to exclude the role of compounds other than volatiles. Among the antimicrobial peptides, specific emphasis has been given in recent studies to the role of lipopeptides in disease suppressive soils. In independent studies, the two structurally similar, chlorinated lipopeptides thanamycin and nunapeptin were shown to contribute to suppressiveness of soils against the fungal root pathogen R.

Furthermore, using a combination of different techniques, Cha et al. Next-generation sequencing analyses revealed an increase of Actinobacteria in this suppressive soil leading to the isolation and genomic characterization of Streptomyces isolate S Genome mining of Streptomyces S pointed at the production of conprimycin as a metabolite involved in suppressing Fusarium.

A chemogenomic approach further suggested that conprimycin acts by interfering with fungal cell wall biosynthesis Cha et al. To further target the active microbial communities and to identify other microbial traits involved in disease suppressive soils, DNA-SIP Radajewski et al. For example, by using metagenomic approaches Hjort et al. Furthermore, Chapelle et al. They found that upon pathogen exposure, stress-related genes were upregulated in rhizobacteria belonging to the Oxalobacteraceae, Sphingobacteriaceae, Burkholderiaceae, Alcaligenaceae, Cystobacteraceae, Sphingomonadaceae, Cytophagaceae, Comamonadaceae , and Verrucomicrobia.

Based on these results they proposed a model in which the fungal pathogen secretes oxalic and phenylacetic acid during colonization of the root system, thereby exerting oxidative stress in the rhizobacterial community as well as in the plant. This stress response in turn leads to the activation of survival strategies of the rhizobacterial community leading to enhanced motility, biofilm formation and the production of yet unknown secondary metabolites.

Collectively, these recent studies exemplify that combining different approaches and technologies allows a more in-depth analysis of the microbial and chemical ecology of disease suppressive soils, as depicted in Figure 1. Schematic overview of currently available approaches involving microbiological, molecular, chemical and bioinformatic methods that can be adopted and integrated to generate a more complete picture of the microbial consortia and mechanisms involved in disease suppressive soils.

In the early days of research on disease suppressive soils, several valuable insights were obtained for the role of individual microbial genera Weller et al. In most disease suppressive soils, however, suppressiveness appears to be due to the concerted activities of multiple microbial genera working together at specific sites or operating at different stages of the infection process of the pathogen.

Understanding the temporal and spatial microbial dynamics of disease suppressive soils as well as the corresponding modes of action will be needed to facilitate the development of effective, consistent and durable disease management tools.

A model predicting Fusarium wilt suppressiveness, including several soil factors combined with the abundance of three keystone microbial taxa, was designed recently by Trivedi et al. Relevant functions involved in disease suppressiveness can be executed by multiple microbial taxa, but metatranscriptome, metaproteome and metabolome studies of disease suppressive soils are still underrepresented. Thus, rather than introducing beneficial microorganisms, agricultural research should focus on identifying the factors that influence key microorganisms or traits responsible for suppressiveness Kinkel et al.

Hence, research on management practices aiming to select or stimulate resident microbial communities or activities that enhance suppressiveness is emerging.

Examples are the use of specific soil amendments including chitin Cretoiu et al. Crop losses due to plant pests and diseases are a common problem worldwide.

Improving productivity is crucial to reduce rural poverty and to increase food security worldwide Flood, ; Cerda et al. Therefore, managing and preserving soil health is essential for sustainable agriculture and optimum ecosystem functioning Larkin, The use of pesticides is a traditional control strategy, but the development of pathogen resistance and an increasing public concern about the adverse effects on plant, animal and human health necessitate alternative and sustainable control methods.

Engineering the soil and plant microbiome has been suggested as a novel and promising means for plant health Mueller and Sachs, Moreover, Kinkel et al. RGE drafted the manuscript. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Abbasi, P.

Establishing suppressive conditions against soilborne potato diseases with low rates of fish emulsion applied serially as a pre-plant soil amendment.

Plant Pathol. Abdeljalil, N. Bio-suppression of Sclerotinia stem rot of tomato and biostimulation of plant growth using tomato-associated rhizobacteria. Adam, M. Specific microbial attachment to root knot nematodes in suppressive soil. Alabouvette, C. Agronomie 6, — Microbiological control of soil-borne phytopathogenic fungi with special emphasis on wilt-inducing Fusarium oxysporum.

New Phytol. Almario, J. Assessment of the relationship between geologic origin of soil, rhizobacterial community composition and soil receptivity to tobacco black root rot in Savoie region France. Plant Soil , — Amir, H.


Deciphering the Rhizosphere Microbiome for Disease-Suppressive Bacteria [2011]

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Deciphering the rhizosphere microbiome for disease-suppressive bacteria.

Thank you for visiting nature. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser or turn off compatibility mode in Internet Explorer. In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript. The rhizosphere is the infection court where soil-borne pathogens establish a parasitic relationship with the plant. To infect root tissue, pathogens have to compete with members of the rhizosphere microbiome for available nutrients and microsites.


Current Insights into the Role of Rhizosphere Bacteria in Disease Suppressive Soils

Disease-suppressive soils are exceptional ecosystems in which crop plants suffer less from specific soil-borne pathogens than expected owing to the activities of other soil microorganisms. For most disease-suppressive soils, the microbes and mechanisms involved in pathogen control are unknown. By coupling PhyloChip-based metagenomics of the rhizosphere microbiome with culture-dependent functional analyses, we identified key bacterial taxa and genes involved in suppression of a fungal root pathogen. More than 33, bacterial and archaeal species were detected, with Proteobacteria, Firmicutes, and Actinobacteria consistently associated with disease suppression. Our data indicate that upon attack by a fungal root pathogen, plants can exploit microbial consortia from soil for protection against infections. This site needs JavaScript to work properly. Please enable it to take advantage of the complete set of features!

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