Apocarotenoid application differentially shape leaf molecular composition and associated rhizosphere soil microbial communities in tomato plants

Plants exposed to abiotic stresses undergo physiological, biochemical, and molecular changes and Raman spectroscopy, together with eco-physiological measurements, enables the in vivo detection of the stress impact on the plant responses. Apocarotenoids, i.e., carotenoid-derived metabolites, are signalling molecules known to contribute to plant drought tolerance. However, their impact on the rhizosphere- and root-associated microbial communities in natural conditions has been unraveled only for few apocarotenoids. Here, the effects of two cyclic β-apocarotenoids, i.e., β-cyclocitric acid (β-CCA) and trimethylcyclohexanone (TCH), were investigated in tomato plants grown in pots filled with natural soil, both under well-watered and water stress conditions, combining gas exchange measurements using a porometer/fluorometer and Raman spectroscopy on leaves, evaluation of arbuscular mycorrhizal fungal colonization in roots, and metabarcoding on rhizosphere soil. Results showed that β-CCA significantly decreased the relative intensity of bands associated with carotenoid, carbohydrate, and pectin, and that both β-CCA and TCH positively affected the native mycorrhizal status in terms of frequency of mycorrhization under well-watered conditions. In the rhizosphere, the considered molecules altered the microbial alpha diversity, modulating the abundance of plant growth promoting microorganisms. Overall, the results suggest that application of β-CCA may serve as a promising strategy to improve plant resilience, changing the metabolism of some relevant leaf compounds and promoting beneficial root-microbe interactions.