Repression of tropolone production and induction of a Burkholderia plantarii pseudo-biofilm by carot-4-en-9,10-diol, a cell-to-cell signaling disrupter produced by Trichoderma virens.
BACKGROUND
The tropolone-tolerant Trichoderma virens PS1-7 is a biocontrol agent against Burkholderia plantarii, causative of rice seedling blight. When exposed to catechol, this fungus dose-dependently produced carot-4-en-9,10-diol, a sesquiterpene-type autoregulatory signal molecule that promotes self-conidiation of T. virens PS1-7 mycelia. It was, however, uncertain why T. virens PS1-7 attenuates the symptom development of the rice seedlings infested with B. plantarii.


RESULTS
To reveal the antagonism by T. virens PS1-7 against B. plantarii leading to repression of tropolone production in a coculture system, bioassay-guided screening for active compounds from a 3-d culture of T. virens PS1-7 was conducted. As a result, carot-4-en-9,10-diol was identified and found to repress tropolone production of B. plantarii from 10 to 200 µM in a dose-dependent manner as well as attenuate virulence of B. plantarii on rice seedlings. Quantitative RT-PCR analysis revealed that transcriptional suppression of N-acyl-L-homoserine lactone synthase plaI in B. plantarii was the main mode of action by which carot-4-en-9,10-diol mediated the quorum quenching responsible for repression of tropolone production. In addition, the unique response of B. plantarii to carot-4-en-9,10-diol in the biofilm formed in the static culture system was also found. Although the initial stage of B. plantarii biofilm formation was induced by both tropolone and carot-4-en-9,10-diol, it was induced in different states. Moreover, the B. plantarii biofilm that was induced by carot-4-en-9,10-diol at the late stage showed defects not only in matrix structure but also cell viability.


CONCLUSIONS
Our findings demonstrate that carot-4-en-9,10-diol released by T. virens PS1-7 acts as an interkingdom cell-to-cell signaling molecule against B. plantarii to repress tropolone production and induces pseudo-biofilm to the cells. This observation also led to another discovery that tropolone is an autoregulatory cell-to-cell signaling molecule of B. plantarii that induces a functional biofilm other than a simple B. plantarii virulence factor.
Graduate School of Agriculture & Research Faculty of Agriculture, Hokkaido University, Sapporo, Japan.
Mengcen
M
Wang
Makoto
M
Hashimoto
Yasuyuki
Y
Hashidoko
D000900:Anti-Bacterial Agents / Q000096:biosynthesis / Q000494:pharmacology*; D000898:Antibiosis; D018441:Biofilms; D019117:Burkholderia / Q000187:drug effects / Q000472:pathogenicity / Q000502:physiology*; D002338:Carotenoids / Q000096:biosynthesis / Q000494:pharmacology*; D015870:Gene Expression / Q000187:drug effects; D015964:Gene Expression Regulation, Bacterial / Q000187:drug effects; D005798:Genes, Bacterial; D012275:Oryza / Q000382:microbiology; D010935:Plant Diseases; D053038:Quorum Sensing; D014242:Trichoderma / Q000502:physiology*; D014334:Tropolone / Q000378:metabolism*; D014774:Virulence / Q000187:drug effects
D000900:Anti-Bacterial Agents; D002338:Carotenoids; D014334:Tropolone