Biocontrol of Bacterial Wilt Disease Through Complex Interaction Between Tomato Plant, Antagonists, the Indigenous Rhizosphere Microbiota, and Ralstonia solanacearum

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.

Streptomyces strains modulate dynamics of soil bacterial communities and their efficacy in disease suppression caused by Phytophthora capsici

“…For example, Arabidopsis roots in response to a leaf pathogen infection attract Bacillus subtilis into the rhizosphere 49 . In the current study, the most enrichment in IT20 samples was recorded for the genus Devosia affiliated to Gammaproteobacteria, it was previously described that this genus is increased in response to B. velezensis and P. fluorescens , involved in biocontrol activity against R. solanacearum on tomato 50 . Another increase in relative abundance was recorded for the genus Gallionella that was previously described as a member of the core microbiome of the wheat healthy plant 23 .…”

Efficacy of indigenous plant growth-promoting rhizobacteria and Trichoderma strains in eliciting resistance against bacterial wilt in a tomato

“…The treatments of P. fluorescens Pf3 + T. longibrachiatum UNS11 were recorded highest wilt protection of 62% as compared to control treatment (97%). Our research outcomes authenticate earlier reports that in the control of bacterial wilt, the use of beneficial microbes in combination treatments was more effective than individual agents (Thilagavathi et al 2007 andElsayed et al 2020). The present results agreed with the R. solanacearum wilt disease reduction in tomato plants by treatment with Bacillus sp.…”

Microbiome Modulation—Toward a Better Understanding of Plant Microbiome Response to Microbial Inoculants

“…However, the majority of studies revealed only transient establishment or low abundance of the microbial inoculants during plant growth ( Scherwinski et al, 2008 ; Schreiter et al, 2014b ; Eltlbany et al, 2019 ). In order to understand establishment efficiency, it is important to consider rhizosphere and rhizoplane colonization patterns of the inoculant ( Götz et al, 2006 ; Elsayed et al, 2020 ). A successful establishment depends on strain traits ( Adesina et al, 2009 ), application mode ( Götz et al, 2006 ; Schmidt et al, 2012 ), and on the structure of the target microbiome ( van Elsas et al, 2012 ).…”

“…Similar effects were observed in tomato plants infected with Ralstonia solanacearum B3B through the inoculation of Bacillus velezensis B63 or Pseudomonas fluorescens P142. Here, a microbiome shift toward genera that comprise multiple strains with plant growth promoting activity such as Arthrobacter and Gaiella (Actinobacteria ) or Ochrobactrum ( Alphaproteobacteria ) was observed ( Elsayed et al, 2020 ). Fusarium stalk rot in maize caused by Fusarium graminearum can be controlled via application of Trichoderma harzianum CCTCC-RW0024, which resulted in an increase of plant growth promoting Acidobacteria ( Saravanakumar et al, 2017 ).…”

“…Representative isolates of the health indicators ( Brevibacterium frigoritolerans HRS1, Bacillus niacini HRS2, Solibacillus silvestris HRS3, and Bacillus luciferensis HRS4) were able to induce an immune activation and extended plant protection against R. solanacearum. In addition, several studies described the depletion of potential pathogens due to inoculant application ( Schmidt et al, 2012 ; Saravanakumar et al, 2017 ; Elsayed et al, 2020 ). These studies provide indications that depletion of pathogens might be an accompanying effect to the enrichment of plant-beneficial strains, which together constitutes the observed microbiome shifts.…”