Many
bacteria use quorum sensing (QS) to regulate phenotypes that
ultimately benefit the bacterial population at high cell densities.
These QS-dependent phenotypes are diverse and can have significant
impacts on the bacterial host, including virulence factor production,
motility, biofilm formation, bioluminescence, and root nodulation.
As bacteria and their eukaryotic hosts have coevolved over millions
of years, it is not surprising that certain hosts appear to be able
to sense QS signals, potentially allowing them to alter QS outcomes.
Recent experiments have established that eukaryotes have marked responses
to the N-acyl l-homoserine lactone (AHL)
signals used by Gram-negative bacteria for QS, and the responses of
plants to AHLs have received considerable scrutiny to date. However,
the molecular mechanisms by which plants, and eukaryotes in general,
sense bacterial AHLs remain unclear. Herein, we report a systematic
analysis of the responses of the model plants Arabidopsis
thaliana and Medicago truncatula to a series
of native AHLs and byproducts thereof. Our results establish that
AHLs can significantly alter seedling growth in an acyl-chain length
dependent manner. Based upon A. thaliana knockout
studies and in vitro biochemical assays, we conclude
that the observed growth effects are dependent upon AHL amidolysis
by a plant-derived fatty acid amide hydrolase (FAAH) to yield l-homoserine. The accumulation of l-homoserine appears
to encourage plant growth at low concentrations by stimulating transpiration,
while higher concentrations inhibit growth by stimulating ethylene
production. These results offer new insights into the mechanisms by
which plant hosts can respond to QS signals and the potential role
of QS in interkingdom associations.