The plant pathogen Pseudomonas aeruginosa triggers a DELLA-dependent seed germination arrest in Arabidopsis

To anticipate potential seedling damage, plants block seed germination under unfavorable conditions. Previous studies investigated how seed germination is controlled in response to abiotic stresses through gibberellic and abscisic acid signaling. However, little is known about whether seeds respond to rhizosphere bacterial pathogens. We found that Arabidopsis seed germination is blocked in the vicinity of the plant pathogen Pseudomonas aeruginosa. We identified L-2-amino-4-methoxy-trans-3-butenoic acid (AMB), released by P. aeruginosa, as a biotic compound triggering germination arrest. We provide genetic evidence that in AMB-treated seeds DELLA factors promote the accumulation of the germination repressor ABI5 in a GA-independent manner. AMB production is controlled by the quorum sensing system IQS. In vitro experiments show that the AMB-dependent germination arrest protects seedlings from damage induced by AMB. We discuss the possibility that this could serve as a protective response to avoid severe seedling damage induced by AMB and exposure to a pathogen.
eLife digest The plant embryo within a seed is well protected. While it cannot stay within the seed forever, the embryo can often wait for the right conditions before it develops into a seedling and continues its life cycle. Indeed, plants have evolved several ways to time this process – which is known as germination – to maximize the chances that their seedlings will survive. For example, if the environment is too hot or too dark, the seed will make a hormone that stops it from germinating. In addition to environmental factors like light and temperature, a seed in the real word is continuously confronted with soil microbes that may harm or benefit the plant. However, few researchers have asked whether seeds control their germination in response to other living organisms. The bacterium Pseudomonas aeruginosa lives in a wide spectrum of environments, including the soil, and can cause diseases in both and plants and animals. Chahtane et al. now report that seeds of the model plant Arabidopsis thaliana do indeed repress their germination when this microbe is present. Specifically, the seeds respond to a molecule released from the bacteria called L-2-amino-4-methoxy-trans-3-butenoic acid, or AMB for short. Like the bacteria, AMB is harmful to young seedlings, but Chahtane et al. showed that the embryo within the seed is protected from its toxic effects. Further experiments revealed that the seed's response to the bacterial molecule requires many of the same signaling components that repress germination when environmental conditions are unfavorable. However, Chahtane et al. note that AMB activates these components in an unusual way that they still do not understand. The genes that control the production of AMB are known to also control how bacterial populations behave as they accumulate to high densities. It is therefore likely that Pseudomonas aeruginosa would make AMB if it reached a high density in the soil. This raises the possibility that plants have specifically evolved to stop germination if there are enough microbes nearby to pose a risk of disease. This hypothesis, however, is only one of several possible explanations and remains speculative at this stage; further work is now needed to evaluate it. Nevertheless, identifying how AMB interferes with the signaling components that control germination and plant growth may guide the design of new herbicides that could, for example, control weeds in the farming industry.