Deciphering the mechanism of fungal pathogen-induced disease-suppressive soil

Authors: WEN, TAO - Nanjing Agricultural University; DING, ZHENXU - Nanjing Agricultural University; Thomashow, Linda; Hale, Lauren; YANG, SHENGDIE - Nanjing Agricultural University; XIE, PENGHAO - Nanjing Agricultural University; LIU, XIAOYU - Nanjing Agricultural University; WANG, HEQI - Nanjing Agricultural University; SHEN, QIROGN - Nanjing Agricultural University; YUAN, JUN - Nanjing Agricultural University

Submitted to: New Phytologist
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/14/2023
Publication Date: 3/17/2023
Citation: Wen, T., Ding, Z., Thomashow, L.S., Hale, L.E., Yang, S., Xie, P., Liu, X., Wang, H., Shen, Q., Yuan, J. 2023. Deciphering the mechanism of fungal pathogen-induced disease-suppressive soil. New Phytologist. 238(6):2634-2650. https://doi.org/10.1111/nph.18886.
DOI: https://doi.org/10.1111/nph.18886

Interpretive Summary: Disease suppressive soils can greatly reduce losses caused by agricultural crop pathogens. However, very little has been resolved regarding the underlying mechanisms by which native soil microbiomes function to suppress plant diseases. Herein, we evaluated cucumber continuously cultivated under the pressure of Fusarium wilt causative agent, Fusarium oxysporum and revealed increasing capacity for disease suppression. The associated microbiome of the conditioned, disease suppressive soil included two enriched genera, Bacillus and Sphingomonas. Isolates of these genera were shown to induce plant oxidative bursts, which assist in pathogen control. Based on isolate growth rates and metagenomic sequencing data, these genera responded to conditionally-produced cucumber root exudates. Altogether these results provide an important theoretical basis for suppressive-soil formation from which effective approaches for prevention of soil-borne disease can be built.

Technical Abstract: The concept of disease-suppressive soil indicates that confrontation of plants with phytopathogens chronically leads to recruitment and accumulation of beneficial microorganisms. However, more mechanisms need to be deciphered regarding which microorganisms confer these benefits and how the disease suppression is achieved. Here, we conditioned soil by continuously growing eight generations of cucumber inoculated with Fusarium oxysporum f.sp. cucumerinum in a root-split system. The disease incidence was found to gradually decrease upon pathogen infection and this disease suppression was transferrable. Microbial composition analysis showed two key microbes, Bacillus and Sphingomonas, gradually accumulated across the eight generations of cucumber under pathogen pressure. Cultured isolates of Bacillus and Sphingomonas spp applied to soils triggered a higher quantity of reactive oxygen species (ROS mainly OH·) in cucumber roots. Disease resistant cucumber grown in the pathogen conditioned soil also had higher ROS concentrations and relative abundances of Bacillus and Sphingomonas, indicating that these key microbes protected the cucumber from pathogen infection by inducing oxidative burst in roots. Metagenomics sequencing revealed enriched pathways, which included a two-component system, bacterial secretion system and flagellar assembly, that responded to the activation of microbe-induced ROS by Bacillus and Sphingomonas taxa. Untargeted metabolomics analysis combined with an in vitro application assay suggested that the significant changes in root exudate profiles under pathogen infection, where attributed to threonic acid and lysine, which were pivotal components to recruit Bacillus and Sphingomonas. Collectively, our study deciphered a “cry for help” case wherein cucumber releases to threonic acid and lysine to enrich beneficial microbes which raise the ROS level of host and prevent pathogen attack. More importantly, this may be one of the fundamental mechanisms underpinning disease-suppressive soil formation.