Understanding the Impact of Cultivar, Seed Origin, and Substrate on Bacterial Diversity of the Sugar Beet Rhizosphere and Suppression of Soil-Borne Pathogens

Abstract

The rhizosphere microbiome is crucial for plant health, especially for preventing roots from being infected by soil-borne pathogens. Microbiota-mediated pathogen response in the soil-root interface may hold the key for microbiome-based control strategies of phytopathogens. We studied the pathosystem sugar beet-late sugar beet root rot caused by <i>Rhizoctonia solani</i> in an integrative design of combining <i>in vitro</i> and <i>in vivo</i> (greenhouse and field) trials. We used five different cultivars originating from two propagation sites (France, Italy) with different degrees of susceptibility towards <i>R. solani</i> (two susceptible, one moderately tolerant and two cultivars with partial resistance). Analyzing bacterial communities in seeds and roots grown under different conditions by 16S rRNA amplicon sequencing, we found site-, cultivar-, and microhabitat-specific amplicon sequences variants (ASV) as well as a seed core microbiome shared between all sugar beet cultivars (121 ASVs representing 80%-91% relative abundance). In general, cultivar-specific differences in the bacterial communities were more pronounced in seeds than in roots. Seeds of <i>Rhizoctonia</i>-tolerant cultivars contain a higher relative abundance of the genera <i>Paenibacillus</i>, <i>Kosakonia</i>, and <i>Enterobacter</i>, while <i>Gaiellales, Rhizobiales</i>, and <i>Kosakonia</i> were enhanced in responsive rhizospheres. These results indicate a correlation between bacterial seed endophytes and <i>Rhizoctonia</i>-tolerant cultivars. Root communities are mainly substrate-derived but also comprise taxa exclusively derived from seeds. Interestingly, the signature of <i>Pseudomonas poae</i> Re*1-1-14, a well-studied sugar-beet specific biocontrol agent, was frequently found and in higher relative abundances in <i>Rhizoctonia</i>-tolerant than in susceptible cultivars. For microbiome management, we introduced microbial inoculants (consortia) and microbiome transplants (vermicompost) in greenhouse and field trials; both can modulate the rhizosphere and mediate tolerance towards late sugar beet root rot. Both, seeds and soil, provide specific beneficial bacteria for rhizosphere assembly and microbiota-mediated pathogen tolerance. This can be translated into microbiome management strategies for plant and ecosystem health.