Impact of bacteriophages on plant-pathogen interactions in a tripartite system

With the world population on the rise, it is crucial to optimize the utilization of arable resources and minimize food loss. Plant pathogenic bacteria which are estimated to account for 10% of our annual yield losses are gaining resistance against classical control strategies like antibiotics, which are a major problem. Bacteriophages as very specialized bacterial viruses hold great potential to overcome this challenge. Therefore, we investigate phages as a sustainable and targeted solution for biocontrol in agriculture with the potential to shape the plant microbiome.

Our research has led to the isolation and characterization of novel phages for the economically relevant plant pathogen Xanthomonas (Erdrich et al., 2022). Among those, we recently isolated the strictly virulent phage Seregon, which proved to be suitable for biocontrol of the plant pathogen Xanthomonas campestris. However, the influence of bacteriophages on plant physiology, particularly during interactions with pathogenic bacteria in planta, remains a significant knowledge gap. Understanding the phage's impact on bacterial infection dynamics and plant defence responses is pivotal for successful application strategies.

Here, we present infection studies of Arabidopsis thaliana with the plant pathogen Xanthomonas campestris. The application of the Xanthomonas phage Seregon could successfully counteract the bacterial infection almost to the level of the uninfected control. A meta-transcriptome analysis provided unprecedented insights into expression dynamics in this tripartite system and showed decreased plant defence gene upregulation in the presence of the bacteriophage. While X. campestris infection led to the expression of several salicylic acid-responsive genes and activation of the glucosinolate biosynthetic pathway. Furthermore, we observed a significant reduction of virulence expression in the bacterial transcriptome in the presence of the phage.

In conclusion, we show that natural phage diversity can be harnessed for phage-based plant biocontrol. Furthermore, our findings indicate that the application of phages effectively protects Arabidopsis thaliana against the pathogen Xanthomonas campestris. These results highlight the promising role of phages in plant protection strategies and pave the way for further exploration of their use in agricultural practices.

References

Erdrich et al. 2022. Viruses 14 (7): 1449

Erdrich et al. 2024. Microbial Biotechnology 6 (17): e14507