Indole alkaloid production by the halo blight bacterium treated with the phytoalexin genistein

Authors: Cooper, Bret; Yang, Ronghui; Campbell, Kimberly

Submitted to: Phytopathology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/28/2024
Publication Date: 6/7/2024
Citation: Cooper, B., Yang, R., Campbell, K. 2024. Indole alkaloid production by the halo blight bacterium treated with the phytoalexin genistein. Phytopathology. 114(6):1196-1205. https://doi.org/10.1094/PHYTO-11-23-0445-R.
DOI: https://doi.org/10.1094/PHYTO-11-23-0445-R

Interpretive Summary: Halo blight disease, caused by a bacterium, reduces harvests of the dry, edible common bean. Resistant beans respond to infection by producing phytoalexins, antibiotic compounds. One such phytoalexin is genistein. To learn more about genistein, USDA-ARS scientists in Beltsville, Maryland, used mass spectrometry, an analytical technique, to measure the changes in proteins and metabolites after bacteria were exposed to genistein. The results show that the bacterium tolerates genistein and, in response, produces indole alkaloids that resemble the plant hormone auxin. Hence, the bacterium can recognize the bean defense response and subsequently may produce bean-altering compounds that assist bacterial pathogenicity. These findings will be of interest to scientists in the government, at universities, and at private institutions who want to understand how pathogens infect plants.

Technical Abstract: When Pseudomonas savastanoi pv. phaseolicola, the bacterium that causes halo blight, induces hypersensitive immunity in common bean leaves, salicylic acid and several phytoalexins accumulate at the site of infection. In vitro, both salicylic acid and the phytoalexin resveratrol exert antibiotic activities and toxicities that stall the replication and motility of P. savastanoi pv. phaseolicola and adversely disrupt its proteome and metabolism. These efficacious properties likely contribute to the cessation of bacterial spread in beans. Genistein is an isoflavonoid phytoalexin that also accumulates during bean immunity, so we tested its antibiotic potential. Quantitative proteomics revealed that genistein did not induce proteomic changes in P. savastanoi pv. phaseolicola in the same way that salicylic acid or resveratrol did. Rather, a dioxygenase that could function to metabolize genistein was among the most highly induced enzymes. Indeed, high-throughput metabolomics provided direct evidence for genistein catabolism. Metabolomics also revealed that genistein induced the bacterium to produce indole compounds, several which had structural similarity to auxin. Additional mass spectrometry analyses proved that the bacterium produced an isomer of the auxin indole-3-acetic acid, but not indole-3-acetic acid proper. These results reveal that P. savastanoi pv. phaseolicola can tolerate bean genistein and that the bacterium likely responds to bean-produced genistein, using it as a signal to increase pathogenicity possibly by altering host cell physiology or metabolism through the production of auxin mimics.