The Co-Association of Enterobacteriaceae and Pseudomonas with Specific Resistant Cucumber against Fusarium Wilt Disease

SIMPLE SUMMARY: Pathogenic attack is a serious biotic stress that negatively affects agricultural and food production in the world. Currently, the use of beneficial plant bacteria for healthy plant growth is attractive due to the demand for eco-friendly and sustainable agriculture. In this study, the culture-free analyses of the root bacterial communities of six cucumber cultivars were compared to define the important differential bacteria associated with the resistant and moderately resistant cultivars against Fusarium oxysporum f. sp. cucumerinum, and the disease-suppressive function of the differential bacterium alone or in a complex were tested in a pot experiment. Our results highlighted that Enterobacteriacea/Pantoea, Enterobacteriaceae/Cronobacter, and Pseudomonadaceae/Pseudomonas were important differential phyla/genera associated with specific resistant cultivars, while Massilia only differed in response to pathogenic attack. The pot experiments confirmed that the differential bacteria complexes Pantoea + Pseudomonas and Cronobacter effectively alleviated disease occurrence. In conclusion, we provide supporting evidence on the potential of root bacteria from resistant cultivars to be regulated or applied to control cucumber wilt disease and promote healthy cucumber growth under pathogenic stress. ABSTRACT: The root microbiota contributes to the plant’s defense against stresses and pathogens. However, the co-association pattern of functional bacteria that improves plant resistance has not been interpreted clearly. Using Illumina high-throughput sequencing technology, the root bacterial community profiles of six cucumber cultivars with different resistance in response to the causative agent of cucumber Fusarium wilt (CFW), Fusarium oxysporum f. sp. cucumerinum (Foc), were analyzed. The principal coordinate analysis indicated that the interactions of the cultivars and pathogens drove the cucumber root bacterial communities (p = 0.001). The resistance-specific differential genera across the cultivars were identified, including Massilia in the resistant cultivars, unclassified Enterobacteriaceae in resistant CL11 and JY409, Pseudomonas in JY409, Cronobacter in moderately resistant ZN106, and unclassified Rhizobiaceae and Streptomyces in susceptible ZN6. The predominant root bacterium Massilia accounted for the relative abundance of up to 28.08–61.55%, but dramatically declined to 9.36% in Foc-inoculated susceptible ZN6. Pseudomonas ASV103 and ASV48 of Pseudomonadaceae and Cronobacter ASV162 of Enterobacteriaceae were consistently differential across the cultivars at the phylum, genus, and ASV levels. Using the culture-based method, antagonistic strains of Enterobacteriaceae with a high proportion of 51% were isolated. Furthermore, the bacterial complexes of Pantoea dispersa E318 + Pseudomonas koreensis Ps213 and Cronobacter spp. C1 + C7 reduced the disease index of CFW by 77.2% and 60.0% in the pot experiment, respectively. This study reveals the co-association of specific root bacteria with host plants and reveals insight into the suppressing mechanism of resistant cultivars against CFW disease by regulating the root microbiota.