Bacterial self-toxicity induced by a plant immune system

Authors: Cooper, Bret; Beard, Hunter; Yang, Ronghui; Garrett, Wesley; Campbell, Kimberly

Submitted to: Journal of Proteome Research
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/26/2021
Publication Date: 6/7/2021
Citation: Cooper, B., Beard, H.S., Yang, R., Garrett, W.M., Campbell, K. 2021. Bacterial self-toxicity induced by a plant immune system. Journal of Proteome Research. 20:3664-3677. https://doi.org/10.1021/acs.jproteome.1c00232.
DOI: https://doi.org/10.1021/acs.jproteome.1c00232

Interpretive Summary: Halo blight disease, caused by a bacterium, reduces harvests of the dry, edible common bean. Natural resistance genes in the bean plant can provide protection against some strains. This resistance does not kill the bacteria; instead it stops bacterial spread. How spread stops is unknown. In this study, we used mass spectrometry, an analytical technique, to measure the amounts of bacterium proteins in bean leaves inoculated with a halo blight strain that triggers resistance and with another strain that infects and causes disease. Out of more than 700 bacterium proteins evaluated, there were 149 proteins that decreased in resistant plants. These proteins control pathogenicity and motility. Another protein that was reduced was lactoylglutathione lyase, an enzyme that eliminates the toxic molecule methylglyoxal. Bean plants produce salicylic acid during resistance. Salicylic acid controls bean resistance responses, but we also found that salicylic acid inhibits halo blight bacterium growth and increases the accumulation of toxic methylglyoxal in the bacterium. Hence, the results show that the plant attacks the bacterium by reducing bacterial proteins needed for virulence and motility, and the plant alters the metabolism of the bacterium by increasing toxic molecules in the bacterium. These results will be of interest to scientists in the government, at universities, and at private institutions who want to understand how beans protect themselves from halo blight infection.

Technical Abstract: The plant immune response that stops bacterial infection is mediated by the salicylic acid hormonal defense signal transduction pathway. How this pathway directly affects the bacteria is unknown. In this study, mass spectrometry of bacterial infections isolated from resistant and susceptible beans revealed that resistant beans restricted bacterial spread and inhibited the accumulation of bacterial proteins required for virulence, secretion, motility, chemotaxis, quorum sensing, and biofilm production. Resistance also reduced amounts of bacterial methylglyoxal detoxification enzymes. Treatment with salicylic acid increased bacterial methylglyoxal concentrations. Increased methylglyoxal concentrations led to a decline in bacterial reproductive fitness. These findings support a model whereby the plant immune system reprograms the bacterial proteome to reduce pathogenicity and to induce bacterial self-toxicity.