Suppression of banana Panama disease induced by soil microbiome reconstruction through an integrated agricultural strategy

Authors: SHEN, ZONGZHUAN - Nanjing Agricultural University; XUE, CHAO - Nanjing Agricultural University; PENTON, C. - Arizona State University; Thomashow, Linda; ZHANG, NA - Nanjing Agricultural University; WANG, BEIBEI - Hainan University; RUAN, YUNZE - Hainan University; LI, RONG - Nanjing Agricultural University; SHEN, QIRONG - Nanjing Agricultural University

Submitted to: Soil Biology and Biochemistry
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/23/2018
Publication Date: 10/25/2018
Citation: Shen, Z., Xue, C., Penton, C.R., Thomashow, L.S., Zhang, N., Wang, B., Ruan, Y., Li, R., Shen, Q. 2018. Suppression of banana Panama disease induced by soil microbiome reconstruction through an integrated agricultural strategy. Soil Biology and Biochemistry. 128:164-174. https://doi.org/10.1016/j.soilbio.2018.10.016.
DOI: https://doi.org/10.1016/j.soilbio.2018.10.016

Interpretive Summary: Fusarium wilt disease of banana, is caused by the fungus Fusarium oxysporum f. sp. cubense race 4. This serious disease currently threatens worldwide banana production. No single agricultural practice has yet been developed to effectively manage this disease. In the present study, greenhouse experiments were conducted to evaluate the control of wilt on severely diseased banana growing in soil treated with biological fertilizers and a solution of ammonia in water for fumigation. Treatments over a period of two years were evaluated for disease control and the composition of the soil microbial community. Results of both two-season experimental studies showed that biofertilizer application after aqueous ammonia fumigation significantly reduced the incidence of Fusarium wilt disease of banana with approximately 55% disease control efficiency and promotion of plant biomass, compared to the control application of cow manure to non-fumigated soil. Ammonia alone significantly reduced the abundance of the pathogen and the diversity of bacteria and fungi present. Biofertilizer application after fumigation further depleted the abundance of the pathogen. Biofertilizer application and fumigation altered the soil microbial community composition, with the bacterial community responding first to fumigation while the fungal community responded first to fertilization. Certain genera that are known to contribute to disease control in other systems were significantly enriched by ammonia fumigation and biofertilizer application, and were significantly correlated with disease suppression and plant biomass. Furthermore, fumigation and biofertilization significantly increased the soil pH and nutrient contents, with simultaneous effects on the microbial community. Overall, the observed disease suppression and increased plant biomass can be attributed to the reduced abundance of the wilt pathogen due to the fumigation and biofertilization and to a condition of general disease suppression resulting from altered soil properties that enabled the establishment of a beneficial soil microbiome.

Technical Abstract: Fusarium wilt disease of banana, caused by the fungus Fusarium oxysporum f. sp. cubense race 4, is a serious soil-borne fungal disease that currently threatens worldwide banana production. No single agricultural practice has yet been developed to effectively manage this disease. In the present study, greenhouse experiments were conducted to evaluate the effect of an integrated biofertilizer application after aqueous ammonia fumigation strategy to enhance control of Fusarium wilt disease in severely infected banana mono-cropped soils using quantitative PCR and MiSeq sequencing. Results of both two-season experimental studies showed that biofertilizer application after aqueous ammonia fumigation significantly reduced the incidence of Fusarium wilt disease of banana with approximately 55% disease control efficiency and promotion of plant biomass, compared to the control application of cow manure to non-fumigated soil. Aqueous ammonia fumigation significantly reduced total fungal and F. oxysporum abundances and bacterial and fungal diversities. Biofertilizer application after fumigation further depleted the abundance of the pathogen. Biofertilizer application and fumigation altered the soil microbial community composition with the bacterial community responding first to fumigation while the fungal community responded first to fertilization. Although Bacillus, which included our inoculated strain, was not enriched after biofertilization, putative beneficial microbes such as Paenibacillus, Virgibacillus, Nitrosomonas, and Nitrobacter were significantly enriched by ammonia fumigation and biofertilizer application, and were significantly correlated with disease suppression and plant biomass. Furthermore, fumigation and biofertilization significantly increased the soil pH and nutrient contents, with concomitant effects on the microbial community. Overall, the observed disease suppression and increased plant biomass resulting from soil fumigation followed by biofertilization can be attributed to the reduced abundance of F. oxysporum due to fumigation and biofertilization and to general suppression resulting from altered soil properties that enabled the establishment of a beneficial soil microbiome.