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Investigation of the interplay between the developmental responses induced by growth hormones and the response to biotrophic pathogens

Final Report Summary - STRESS AND DEV (Investigation of the interplay between the developmental responses induced by growth hormones and the response to biotrophic pathogens.)

Publishable Summary

Fast growing plants are more susceptible to stresses whereas slow growing plants are more stress resistant. These observations lead to the theory of the dilemma of plants, where plants have to choose between growing and responding to stress. This antagonistic relationship between growth and stress responses is often used by the pathogens to suppress plant defence and to infect the plant. Many successful pathogens produce symptoms reminiscent of the induction of a developmental program such as hypertrophy, hyperplasia, hypocotyl elongation and increase of bushiness. In plants, phytohormones coordinate growth and development and many pathogens are able to produce developmental hormones by themselves or inducing the production by the plant. Thus it can be hypothesized that pathogens are coercing the plant developmental program by inducing and/or producing phytohormones to suppress the induction of the defence pathways. Auxin is a growth regulator that play role in virtually all aspects of the plant development. Also during plant pathogen interactions, auxin has been described as a positive regulator of pathogen virulence. On one hand, auxin has a negative impact on the resistance against leaf biotrophic pathogens; further the auxin-signaling response is a hallmark of plant responses to tumor-inducing pathogens. However, the mechanisms underlying the role of auxin during plant pathogen interactions are not yet understood.
The aims of this proposal were i) to understand the mechanism by which auxin and cytokinin, the two most important growth hormones in roots, interact with the salicylic acid (SA) signalling, which is the main defence pathway against biotrophic pathogenic microorganisms, and ii) to understand how the induction of a developmental program interferes with the induction of the salicylic acid signalling pathway. We address these questions through two complementary approaches. First, using in vitro experiments and direct treatment of Arabidopsis thaliana seedlings, we investigate the crosstalk between auxin and the salicylic acid. SA is the main phytohormone controlling plant resistance to biotrophic and hemibiotrophic pathogens. Then, we challenged mutants in key regulators of auxin signaling with Plasmodiophora brassicae, a gall inducing pathogen and causal agent of clubroot, one of the most damaging diseases of Brassicaceae worldwide.
Auxin is a key inducer of both callus and lateral roots. Our work demonstrated that SA treatment prevented this induction. This suppression of lateral roots was independent of the NPR1-dependent SA-signaling pathway. We then demonstrated that mutation of arf3 and arf21, two repressor Auxin Response Factors, and suppression of the cytokinin-signaling pathway abrogated the SA-mediated suppression of lateral roots. Finally, a network of small RNAs, including miR390 and Tas3A, regulated ARF3. We showed that SA directly affected this network.
We also highlighted that auxin signalling plays a previously unsuspected role in the inhibition of gall symptom development. Indeed, mutations of two key auxin regulators: arf7 and arf19 rendered the plant more susceptible to P. brassicae. We demonstrated further that ARF7 and ARF19 were part of the jasmonic acid response and of the basal resistance response of Arabidopsis against P. brassicae.
All together, this work opens new hypothesis on the crosstalk between auxin and plant response to pathogens. On one hand, the balance between auxin and SA regulates the plant response to environment. On the other hand, we demonstrated that contrary to previously thought auxin is a positive regulator of plant response to P. brassicae, a gall inducing pathogen. Results obtained in this project can be used in the medium term to develop new crop varieties more productive and showing durable resistance to pathogens.