Sustainable natural bioresources in crop protection: antimicrobial hydroxycoumarins induce membrane depolarization-associated changes in the transcriptome of Ralstonia solanacearum

Abstract

Background: Ralstonia solanacearum is one of the most devastating pathogens affecting crop production worldwide. The hydroxycoumarins (umbelliferone, esculetin and daphnetin) represent sustainable natural bioresources on controlling plant bacterial wilt. However, the antibacterial mechanism of hydroxycoumarins against plant pathogens still remains poorly understood. Results: Here we characterized the effect of three hydroxycoumarins on the transcriptome of R. solanacearum. All three hydroxycoumarins were able to kill R. solanacearum, but their antibacterial activity impacted differently the bacterial transcriptome, indicating that their modes of action might be different. Treatment of R. solanacearum cultures with hydroxycoumarins resulted in a large number of differentially expressed genes (DEGs), involved in basic cellular functions and metabolic process, such as down-regulation of genes involved in fatty acid synthesis, lipopolysaccharides biosynthesis, RNA modification, ribosomal submits, oxidative phosphorylation and electrontransport, as well as up-regulation of genes involved in transcriptional regulators, drug efflux, and oxidative stress responses. Future studies based on in vitro experiments are proposed to investigate lipopolysaccharides biosynthesis pathway leading to R. solanacearum cell death caused by hydroxycoumarins. Deletion of lpxB substantially inhibited the growth of R. solanacearum, and reduced virulence of pathogen on tobacco plants. Conculsion: Our transcriptomic analyses show that specific hydroxycoumarins suppressed gene expression involved in fatty acid synthesis, RNA modification, ribosomal submits, oxidative phosphorylation and electrontransport. These findings provide evidence that hydroxycoumarins inhibit R. solanacearum growth through multi-target effect. Hydroxycoumarins could serve as sustainable natural bioresources against plant bacterial wilt through membrane destruction targeting the lipopolysaccharides biosynthesis pathway.