Banana disease-suppressive soil drives Bacillus assembled to defense Fusarium wilt of banana.
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ABSTRACT:
SUBMITTER: Fan H
PROVIDER: S-EPMC10437119 | biostudies-literature | 2023
REPOSITORIES: biostudies-literature
Publications
Banana disease-suppressive soil drives <i>Bacillus</i> assembled to defense Fusarium wilt of banana.
Fan Huacai H He Ping P Xu Shengtao S Li Shu S Wang Yongfen Y Zhang Wenlong W Li Xundong X Shang Hui H Zeng Li L Zheng Si-Jun SJ
Frontiers in microbiology 20230803
Fusarium wilt of banana (FWB) caused by <i>Fusarium oxysporum</i> f. sp. <i>cubense</i> tropical race 4 (<i>Foc</i> TR4), poses a serious problem for sustainable banana production. Biological control is one of the effective measures to control this destructive disease. High-throughput sequencing of soil microorganisms could significantly improve the efficiency and accuracy of biocontrol strain screening. In this study, the soil microbial diversity of six main banana-producing areas in Yunnan was ...[more]
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Project description:Members of the microbiotas colonizing the plant endophytic compartments and the surrounding bulk and rhizosphere soil play an important role in determining plant health. However, the relative contributions of the soil and endophytic microbiomes and their mechanistic roles in achieving disease suppression remain elusive. To disentangle the relative importance of the different microbiomes in the various plant compartments in inhibiting pathogen infection, we conducted a field experiment to track changes in the composition of microbial communities in bulk and rhizosphere soil and of root endophytes and leaf endosphere collected from bananas planted on Fusarium-infested orchards in disease-suppressive and disease-conducive soils. We found that the rhizosphere and roots were the two dominant plant parts whose bacterial communities contributed to pathogen suppression. We further observed that Pseudomonas was potentially a key organism acting as a pathogen antagonist, as illustrated by microbial community composition and network analysis. Subsequently, culturable pathogen-antagonistic Pseudomonas strains were isolated, and their potential suppressive functions or possible antibiosis in terms of auxin or siderophore synthesis and phosphate solubilization were screened to analyze the mode of action of candidate disease-suppressive Pseudomonas strains. In a follow-up in vivo and greenhouse experiment, we revealed that microbial consortia of culturable Pseudomonas strains P8 and S25 (or S36), isolated from banana plantlet rhizosphere and roots, respectively, significantly suppressed the survival of pathogens in the soil, manipulated the soil microbiome, and stimulated indigenous beneficial microbes. Overall, our study demonstrated that root-associated microbiomes, especially the antagonistic Pseudomonas sp. components, contribute markedly to soil suppression of banana Fusarium wilt. IMPORTANCE Soil suppression of Fusarium wilt disease has been proven to be linked with the local microbial community. However, the contribution of endophytic microbes to disease suppression in wilt-suppressive soils remains unclear. Moreover, the key microbes involving in Fusarium wilt-suppressive soils and in the endophytic populations have not been fully characterized. In this study, we demonstrate that root-associated microbes play vitally important roles in disease suppression. Root-associated Pseudomonas consortia were recognized as a key component in inhibiting pathogen abundance associated with the host banana plants. This finding is crucial to developing alternate strategies for soilborne disease management by harnessing the plant microbiome.
| S-EPMC10100972 | biostudies-literature
Project description:Disease-suppressive soils are soils in which specific soil-borne plant pathogens cause only limited disease although the pathogen and susceptible host plants are both present. Suppressiveness is in most cases of microbial origin. We conducted a comparative metabarcoding analysis of the taxonomic diversity of fungal and bacterial communities from suppressive and non-suppressive (conducive) soils as regards Fusarium wilts sampled from the Châteaurenard region (France). Bioassays based on Fusarium wilt of flax confirmed that disease incidence was significantly lower in the suppressive soil than in the conducive soil. Furthermore, we succeeded in partly transferring Fusarium wilt-suppressiveness to the conducive soil by mixing 10% (w/w) of the suppressive soil into the conducive soil. Fungal diversity differed significantly between the suppressive and conducive soils. Among dominant fungal operational taxonomic units (OTUs) affiliated to known genera, 17 OTUs were detected exclusively in the suppressive soil. These OTUs were assigned to the Acremonium, Chaetomium, Cladosporium, Clonostachys, Fusarium, Ceratobasidium, Mortierella, Penicillium, Scytalidium, and Verticillium genera. Additionally, the relative abundance of specific members of the bacterial community was significantly higher in the suppressive and mixed soils than in the conducive soil. OTUs found more abundant in Fusarium wilt-suppressive soils were affiliated to the bacterial genera Adhaeribacter, Massilia, Microvirga, Rhizobium, Rhizobacter, Arthrobacter, Amycolatopsis, Rubrobacter, Paenibacillus, Stenotrophomonas, and Geobacter. Several of the fungal and bacterial genera detected exclusively or more abundantly in the Fusarium wilt-suppressive soil included genera known for their activity against F. oxysporum. Overall, this study supports the potential role of known fungal and bacterial genera in Fusarium wilt suppressive soils from Châteaurenard and pinpoints new bacterial and fungal genera for their putative role in Fusarium wilt suppressiveness.
| S-EPMC5893819 | biostudies-literature
Project description:BackgroundFusarium wilt of banana (Musa spp.) caused by the fungal pathogen Fusarium oxysporum f. sp. cubense (Foc) is a typical soilborne disease, that severely devastates the banana industry worldwide, and soil microbial diversity is closely related to the spread of Fusarium wilt. To understand the relationship between microbial species and Fusarium wilt, it is important to understand the microbial diversity of the Fusarium wilt-diseased and disease-free soils from banana fields.ResultsBased on sequencing analysis of the bacterial 16S rRNA genes and fungal internal transcribed spacer (ITS) sequences, Foc abundance, fungal or bacterial richness and diversity were higher in the diseased soils than in the disease-free soils. Although Ascomycota and Zygomycota were the most abundant fungi phyla in all soil samples, Ascomycota abundance was significantly reduced in the disease-free soils. Mortierella (36.64%) was predominant in the disease-free soils. Regarding bacterial phyla, Proteobacteria, Acidobacteria, Chloroflexi, Firmicutes, Actinobacteria, Gemmatimonadetes, Bacteroidetes, Nitrospirae, Verrucomicrobia and Planctomycetes were dominant phyla in all soil samples. In particular, Firmicutes contributed 16.20% of the total abundance of disease-free soils. At the bacterial genus level, Bacillus, Lactococcus and Pseudomonas were abundant in disease-free soils with abundances of 8.20, 5.81 and 2.71%, respectively; lower abundances, of 4.12, 2.35 and 1.36%, respectively, were found in diseased soils. The distribution characteristics of fungal and bacterial genera may contribute to the abundance decrease of Foc in the disease-free soils.ConclusionUnique distributions of bacteria and fungi were observed in the diseased and disease-free soil samples from banana fields. These specific genera are useful for constructing a healthy microbial community structure of soil.
| S-EPMC6626388 | biostudies-literature
Project description:Microbial contributions to natural soil suppressiveness have been reported for a range of plant pathogens and cropping systems. To disentangle the mechanisms underlying suppression of banana Panama disease caused by Fusarium oxysporum f. sp. cubense tropical race 4 (Foc4), we used amplicon sequencing to analyze the composition of the soil microbiome from six separate locations, each comprised of paired orchards, one potentially suppressive and one conducive to the disease. Functional potentials of the microbiomes from one site were further examined by shotgun metagenomic sequencing after soil suppressiveness was confirmed by greenhouse experiments. Potential key antagonists involved in disease suppression were also isolated, and their activities were validated by a combination of microcosm and pot experiments. We found that potentially suppressive soils shared a common core community with relatively low levels of F. oxysporum and relatively high proportions of Myxococcales, Pseudomonadales, and Xanthomonadales, with five genera, Anaeromyxobacter, Kofleria, Plesiocystis, Pseudomonas, and Rhodanobacter being significantly enriched. Further, Pseudomonas was identified as a potential key taxon linked to pathogen suppression. Metagenomic analysis showed that, compared to the conducive soil, the microbiome in the disease suppressive soil displayed a significantly greater incidence of genes related to quorum sensing, biofilm formation, and synthesis of antimicrobial compounds potentially active against Foc4. We also recovered a higher frequency of antagonistic Pseudomonas isolates from disease suppressive experimental field sites, and their protective effects against banana Fusarium wilt disease were demonstrated under greenhouse conditions. Despite differences in location and soil conditions, separately located suppressive soils shared common characteristics, including enrichment of Myxococcales, Pseudomonadales, and Xanthomonadales, and enrichment of specific Pseudomonas populations with antagonistic activity against the pathogen. Moreover, changes in functional capacity toward an increase in quorum sensing, biofilm formation, and antimicrobial compound synthesizing involve in disease suppression.
| S-EPMC9513836 | biostudies-literature
Project description:Crops lack genetic resistance to most necrotrophic pathogens. To compensate for this disadvantage, plants recruit antagonistic members of the soil microbiome to defend their roots against pathogens and other pests. The best examples of this microbially based defense of roots are observed in disease-suppressive soils in which suppressiveness is induced by continuously growing crops that are susceptible to a pathogen, but the molecular basis of most is poorly understood. Here we report the microbial characterization of a Korean soil with specific suppressiveness to Fusarium wilt of strawberry. In this soil, an attack on strawberry roots by Fusarium oxysporum results in a response by microbial defenders, of which members of the Actinobacteria appear to have a key role. We also identify Streptomyces genes responsible for the ribosomal synthesis of a novel heat-stable antifungal thiopeptide antibiotic inhibitory to F. oxysporum and the antibiotic's mode of action against fungal cell wall biosynthesis. Both classical- and community-oriented approaches were required to dissect this suppressive soil from the field to the molecular level, and the results highlight the role of natural antibiotics as weapons in the microbial warfare in the rhizosphere that is integral to plant health, vigor and development.
| S-EPMC4681868 | biostudies-literature
Project description:Fusarium wilt (FW) caused by Fusarium oxysporum f. sp. cubense Tropical Race 4 (TR4) is a soil-borne disease that infects bananas, causing severe economic losses worldwide. To reveal the relationship between bacterial populations and FW, the bacterial communities of healthy and TR4-infected rhizosphere and bulk soils were compared using 16S rRNA gene sequencing. Soil physicochemical properties associated with FW were also analyzed. We found the community structure of bacteria in the healthy and TR4 infected rhizosphere was significantly different compared to bulk soil within the same farm. The rhizosphere soils of infected plants exhibited higher richness and diversity than healthy plant with significant abundance of Proteobacteria. In the healthy rhizosphere soil, beneficial bacteria such as Burkholderia and Streptomyces spp. were more abundant. Compared to the infected rhizosphere soil, healthy rhizosphere soil was associated with RNA metabolism and transporters pathways and a high level of magnesium and cation exchange capacity. Overall, we reported changes in the key taxa of rhizospheric bacterial communities and soil physicochemical properties of healthy and FW-infected plants, suggesting their potential role as indicators for plant health.
| S-EPMC8770495 | biostudies-literature
Project description:Fusarium wilt of banana, caused by Fusarium oxysporum f. sp. cubense tropical race 4 (Foc TR4), is a widely distributed soilborne disease that poses a serious threat to banana production. Many control measures have been implemented but have not been effective. Here, we evaluated a combined strategy for Fusarium wilt control that involves a biological agent (Bacillus velezensis strain EB1) and a bioactive compound (potassium sorbate). Our results showed that potassium sorbate inhibited Foc TR4 in a dose-dependent manner. Potassium sorbate did not limit the growth of EB1 in vitro; instead, it promoted the growth and antagonistic ability of EB1 by upregulating the expression of antagonism-related genes. In greenhouse experiments, the combined application of EB1 and potassium sorbate significantly reduced the disease index of Fusarium wilt by suppressing fungal growth in the roots and promoting plant growth. Overall, our results demonstrated that potassium sorbate and B. velezensis EB1 can be used together for the sustainable management of banana Fusarium wilt.
| S-EPMC11539603 | biostudies-literature
Project description:Biological control agents (BCAs) are considered as one of the most important strategies for controlling Fusarium wilt, and bioorganic fertilizer, in particular, has been extensively investigated. However, little is known regarding how a biocontrol microorganism affects the suppression mechanisms when combined with different amendments. In this study, a pot experiment was performed using banana plants to investigate the different mechanisms by which the biocontrol bacterium Bacillus velezensis HN03 (isolated from our laboratory) and amendments suppress Fusarium wilt. The incidence of banana wilt was decreased under HN03 and was reduced further when HN03 was combined with compost, particularly wormcast. In the suppression of Fusarium wilt, HN03 was found to influence the soil environment in various ways. HN03 increased the peroxidase level, which improves plant defense, and was highest when combined with wormcast, being 69 times higher than when combined with cow dung compost. The high accumulation of Mg and P in the "HN03 + wormcast" and Zn and Mn in the "HN03 + cow dung" treatments was negatively correlated with disease incidence. Furthermore, HN03 re-established the microbial community destroyed by the pathogen and further increased the level of suppression in the wormcast. HN03 also enhanced the functional traits of the soil, including defensive mechanism-related traits, and these traits were further enhanced by the combination of HN03 + wormcast.
| S-EPMC7701294 | biostudies-literature
Project description:BackgroundPlant microbiome highlights the importance of endosphere microbiome for growth and health of the host plant. Microbial community analysis represents an elegant way to identify keystone microbial species that have a more central position in the community. The aim of this study was to access the interactions between the keystone bacterial species and plants during banana Fusarium wilt process, by comparing the endophytic bacterial and fungal community in banana roots and shoot tips during growth and wilting processes. The keystone bacterial species were isolated and further engineered to improve banana wilt resistance.ResultsBanana endosphere microbiome structure varied during plant growth and wilting processes. Bacterial and fungal diversity in the shoot tips and roots increased with the development of the banana plantlets. The bacterial groups belonging to the Enterobacteriaceae family with different relative abundances were detected in all the samples. The Klebsiella spp. might be the keystone bacteria during the growth of banana plantlets. The relative abundance of Fusarium associated with the wilt disease did not increase during the wilting process. The endophytic Enterobacteriaceae strains Enterobacter sp. E5, Kosakonia sp. S1, and Klebsiella sp. Kb were isolated on Enterobacteriaceae selective medium and further engineered by expressing 1-aminocyclopropane-1-carboxylate (ACC) deaminase on the bacterial cell walls (designated as E5P, S1P, and KbP, respectively). Pot experiments suggested that plants inoculated with strains E5, E5P, S1, and S1P increased resistance to the Fusarium wilt disease compared with the controls without inoculation, whereas the Klebsiella inoculation (Kb and KbP) did not increase the wilt resistance. Compared with the inoculation with the wild strains E5 and S1, the inoculation with engineered strains E5P and S1P significantly increased wilt resistance and promoted plant growth, respectively. The results illustrated that the keystone species in the banana microbiome may not be dominant in numbers and the functional role of keystone species should be involved in the wilt resistance.ConclusionThe ACC deaminase activity of engineered bacteria was essential to the Fusarium wilt resistance and growth promotion of banana plants. Engineering keystone bacteria in plant microbiome with ACC deaminase on the cell walls should be a promising method to improve plant growth and disease resistance.
| S-EPMC6521393 | biostudies-literature
Project description:In the last century, the banana crop and industry experienced dramatic losses due to an epidemic of Fusarium wilt of banana (FWB), caused by Fusarium oxysporum f.sp. cubense (Foc) race 1. An even more dramatic menace is now feared due to the spread of Foc tropical race 4. Plant genetic resistance is generally considered as the most plausible strategy for controlling effectively such a devastating disease, as occurred for the first round of FWB epidemic. Nevertheless, with at least 182 articles published since 1970, biological control represents a large body of knowledge on FWB. Remarkably, many studies deal with biological control agents (BCAs) that reached the field-testing stage and even refer to high effectiveness. Some selected BCAs have been repeatedly assayed in independent trials, suggesting their promising value. Overall under field conditions, FWB has been controlled up to 79% by using Pseudomonas spp. strains, and up to 70% by several endophytes and Trichoderma spp. strains. Lower biocontrol efficacy (42-55%) has been obtained with arbuscular mycorrhizal fungi, Bacillus spp., and non-pathogenic Fusarium strains. Studies on Streptomyces spp. have been mostly limited to in vitro conditions so far, with very few pot-experiments, and none conducted in the field. The BCAs have been applied with diverse procedures (e.g., spore suspension, organic amendments, bioformulations, etc.) and at different stages of plant development (i.e., in vitro, nursery, at transplanting, post-transplanting), but there has been no evidence for a protocol better than another. Nonetheless, new bioformulation technologies (e.g., nanotechnology, formulation of microbial consortia and/or their metabolites, etc.) and tailor-made consortia of microbial strains should be encouraged. In conclusion, the literature offers many examples of promising BCAs, suggesting that biocontrol can greatly contribute to limit the damage caused by FWB. More efforts should be done to further validate the currently available outcomes, to deepen the knowledge on the most valuable BCAs, and to improve their efficacy by setting up effective formulations, application protocols, and integrated strategies.
| S-EPMC6459961 | biostudies-literature