Abstract
Ralstonia solanacearum (biovar2, race3) is the causal agent of bacterial wilt and this quarantine phytopathogen is responsible for massive losses in several commercially important crops. Biological control of this pathogen might become a suitable plant protection measure in areas where R. solanacearum is endemic. Two bacterial strains, Bacillus velezensis (B63) and Pseudomonas fluorescens (P142) with in vitro antagonistic activity toward R. solanacearum (B3B) were tested for rhizosphere competence, efficient biological control of wilt symptoms on greenhouse-grown tomato, and effects on the indigenous rhizosphere prokaryotic communities. The population densities of B3B and the antagonists were estimated in rhizosphere community DNA by selective plating, real-time quantitative PCR, and R. solanacearum-specific fliC PCR-Southern blot hybridization. Moreover, we investigated how the pathogen and/or the antagonists altered the composition of the tomato rhizosphere prokaryotic community by 16S rRNA gene amplicon sequencing. B. velezensis (B63) and P. fluorescens (P142)-inoculated plants showed drastically reduced wilt disease symptoms, accompanied by significantly lower abundance of the B3B population compared to the non-inoculated pathogen control. Pronounced shifts in prokaryotic community compositions were observed in response to the inoculation of B63 or P142 in the presence or absence of the pathogen B3B and numerous dynamic taxa were identified. Confocal laser scanning microscopy (CLSM) visualization of the gfp-tagged antagonist P142 revealed heterogeneous colonization patterns and P142 was detected in lateral roots, root hairs, epidermal cells, and within xylem vessels. Although competitive niche exclusion cannot be excluded, it is more likely that the inoculation of P142 or B63 and the corresponding microbiome shifts primed the plant defense against the pathogen B3B. Both inoculants are promising biological agents for efficient control of R. solanacearum under field conditions.
Highlights
The utilization of microbes to improve plant growth and health is gaining momentum
All tomato control plants grown in soil infested with high B3B dose (TCR; 1.8 106 B3B CFU g−1 soil) had collapsed 14 days post infection, while no uniform wilting symptoms were observed when the soil was infested with low B3B population density (4.4 104 CFU g−1 soil)
Our results showed that the strains, B. velezensis B63 and P. brassicacearum P142, are promising candidates for future biocontrol of R. solanacearum under field conditions, through significantly lowered R. solanacearum densities in tomato shoots and in the rhizosphere
Summary
The utilization of microbes to improve plant growth and health is gaining momentum. While significant knowledge on the links between plant traits and their microbiota was obtained from generation sequencing technologies (Panke-Buisse et al, 2015), downstream applications of that knowledge are still difficult (Herrmann and Lesueur, 2013). R. solanacearum strains (Yabuuchi et al, 1995) form a species complex in the Burkholderiaceae family, divided into four phylotypes associated to geographic locations following human societies and agriculture expansion (I: Asia, II: America, III: Africa, IV: Pacific; Lowe-Power et al, 2018a,b) This soilborne phytopathogen can infect more than 200 plant species, including crucial commercial crops. R. solanacearum survives for long periods in the environment (Graham et al, 1979; Grey and Steck, 2001) and when stressed (e.g., by cold temperatures; van Elsas et al, 2000, 2001; Kong et al, 2014), R. solanacearum initiates a resistance phase, the so-called “viable but non-culturable state” (VBNC), making it readily prone for dissemination via surface irrigation or infested soils It may colonize rhizospheres of numerous non-host crops and weeds, or even hide under latent infection forms in endophytic compartments (Ciampi et al, 1980; van Overbeek et al, 2004). Warm areas favor the development of the R. solanacearum wilting symptoms (Bocsanczy et al, 2014), cold-tolerant strains belonging to the brown rot phylotype IIB1 (Cellier and Prior, 2010) can infect host plants in temperate zones (Milling et al, 2009), making R. solanacearum a major threat to agriculture worldwide
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