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Manipulating the banana rhizosphere microbiome for biological control of Panama disease.

ABSTRACT: Panama disease caused by Fusarium oxysporum f. sp. cubense infection on banana is devastating banana plantations worldwide. Biological control has been proposed to suppress Panama disease, though the stability and survival of bio-control microorganisms in field setting is largely unknown. In order to develop a bio-control strategy for this disease, 16S rRNA gene sequencing was used to assess the microbial community of a disease-suppressive soil. Bacillus was identified as the dominant bacterial group in the suppressive soil. For this reason, B. amyloliquefaciens NJN-6 isolated from the suppressive soil was selected as a potential bio-control agent. A bioorganic fertilizer (BIO), formulated by combining this isolate with compost, was applied in nursery pots to assess the bio-control of Panama disease. Results showed that BIO significantly decreased disease incidence by 68.5%, resulting in a doubled yield. Moreover, bacterial community structure was significantly correlated to disease incidence and yield and Bacillus colonization was negatively correlated with pathogen abundance and disease incidence, but positively correlated to yield. In total, the application of BIO altered the rhizo-bacterial community by establishing beneficial strains that dominated the microbial community and decreased pathogen colonization in the banana rhizosphere, which plays an important role in the management of Panama disease.

SUBMITTER: Xue C

PROVIDER: S-EPMC4525139 | biostudies-literature | 2015

REPOSITORIES: biostudies-literature

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Manipulating the banana rhizosphere microbiome for biological control of Panama disease.

Xue Chao C Penton C Ryan CR Shen Zongzhuan Z Zhang Ruifu R Huang Qiwei Q Li Rong R Ruan Yunze Y Shen Qirong Q

Scientific reports 20150805

Panama disease caused by Fusarium oxysporum f. sp. cubense infection on banana is devastating banana plantations worldwide. Biological control has been proposed to suppress Panama disease, though the stability and survival of bio-control microorganisms in field setting is largely unknown. In order to develop a bio-control strategy for this disease, 16S rRNA gene sequencing was used to assess the microbial community of a disease-suppressive soil. Bacillus was identified as the dominant bacterial ...[more]

PMID: 26242751

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Project description:Fusarium oxysporum (Fo) belongs to a group of soil-borne hyphomycetes that are taxonomically collated in the Fusarium oxysporum Species Complex (FOSC). Hitherto, those infecting bananas were placed in the forma specialis cubense (Foc). Recently, however, these genetically different Foc lineages were recognized as new Fusarium spp. placed in the Fusarium of Banana Complex (FOBC). A member of this complex F. odoratissimum II-5 that uniquely comprises the so-called Tropical Race 4 (TR4), is a major problem sweeping through production zones of Cavendish banana in several regions of the world. Because of this, there is an urgent need for a phenotyping method that allows the screening for resistance to TR4 of large numbers of banana genotypes. Most Fusarium species produce three types of spores: macroconidia, microconidia and the persistent chlamydospores that can contaminate soils for many years. Inoculum production has been an important bottleneck for efficient phenotyping due to the low or variable number of conidia and the elaborate laboratory procedures requiring specific infrastructure. Here, we report a rapid, simple and high-yielding spore production method for nine F. oxysporum formae speciales as well as the biocontrol species Fo47 and Fo618-12. For Fusarium spp. causing Fusarium wilt or Panama disease of banana, we used the protocol for four species comprising the recognized physiological races, including Tropical Race 4 (TR4). We subsequently tested the produced inoculum in comparative inoculation trials on banana plants to evaluate their efficiency. All assays resulted in typical symptoms within 10 weeks; significant differences in final disease ratings were observed, depending on inoculum concentration. Pouring inoculum directly onto banana plants showed the most consistent and reproducible results, as expressed in external wilting, internal discoloration and determined by real-time PCR assays on entire rhizomes. Moreover, this method allows the inoculation of 250 plants per hour by one individual thereby facilitating the phenotyping of large mutant and breeding populations.

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.

Project description:Bacteriophages, viruses that specifically target plant pathogenic bacteria, have emerged as a promising alternative to traditional agrochemicals. However, it remains unclear how phages should be applied to achieve efficient pathogen biocontrol and to what extent their efficacy is shaped by indirect interactions with the resident microbiota. Here, we tested if the phage biocontrol efficacy of Ralstonia solanacearum phytopathogenic bacterium can be improved by increasing the phage cocktail application frequency and if the phage efficacy is affected by pathogen-suppressing bacteria already present in the rhizosphere. We find that increasing phage application frequency improves R. solanacearum density control, leading to a clear reduction in bacterial wilt disease in both greenhouse and field experiments with tomato. The high phage application frequency also increased the diversity of resident rhizosphere microbiota and enriched several bacterial taxa that were associated with the reduction in pathogen densities. Interestingly, these taxa often belonged to Actinobacteria known for antibiotics production and soil suppressiveness. To test if they could have had secondary effects on R. solanacearum biocontrol, we isolated Actinobacteria from Nocardia and Streptomyces genera and tested their suppressiveness to the pathogen in vitro and in planta. We found that these taxa could clearly inhibit R. solanacearum growth and constrain bacterial wilt disease, especially when combined with the phage cocktail. Together, our findings unravel an undiscovered benefit of phage therapy, where phages trigger a second line of defense by the pathogen-suppressing bacteria that already exist in resident microbial communities.ImportanceRalstonia solanacearum is a highly destructive plant-pathogenic bacterium with the ability to cause bacterial wilt in several crucial crop plants. Given the limitations of conventional chemical control methods, the use of bacterial viruses (phages) has been explored as an alternative biological control strategy. In this study, we show that increasing the phage application frequency can improve the density control of R. solanacearum, leading to a significant reduction in bacterial wilt disease. Furthermore, we found that repeated phage application increased the diversity of rhizosphere microbiota and specifically enriched Actinobacterial taxa that showed synergistic pathogen suppression when combined with phages due to resource and interference competition. Together, our study unravels an undiscovered benefit of phages, where phages trigger a second line of defense by the pathogen-suppressing bacteria present in resident microbial communities. Phage therapies could, hence, potentially be tailored according to host microbiota composition to unlock the pre-existing benefits provided by resident microbiota.

Dataset Information

Manipulating the banana rhizosphere microbiome for biological control of Panama disease.

Publications

Manipulating the banana rhizosphere microbiome for biological control of Panama disease.

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