The apocarotenoid β‐ionone regulates the transcriptome of Arabidopsis thaliana and increases its resistance against Botrytis cinerea.

SUMMARY: Carotenoids are isoprenoid pigments indispensable for photosynthesis. Moreover, they are the precursor of apocarotenoids, which include the phytohormones abscisic acid (ABA) and strigolactones (SLs) as well as retrograde signaling molecules and growth regulators, such as β‐cyclocitral and zaxinone. Here, we show that the application of the volatile apocarotenoid β‐ionone (β‐I) to Arabidopsis plants at micromolar concentrations caused a global reprogramming of gene expression, affecting thousands of transcripts involved in stress tolerance, growth, hormone metabolism, pathogen defense, and photosynthesis. This transcriptional reprogramming changes, along with induced changes in the level of the phytohormones ABA, jasmonic acid, and salicylic acid, led to enhanced Arabidopsis resistance to the widespread necrotrophic fungus Botrytis cinerea (B.c.) that causes the gray mold disease in many crop species and spoilage of harvested fruits. Pre‐treatment of tobacco and tomato plants with β‐I followed by inoculation with B.c. confirmed the effect of β‐I in increasing the resistance to this pathogen in crop plants. Moreover, we observed reduced susceptibility to B.c. in fruits of transgenic tomato plants overexpressing LYCOPENE β‐CYCLASE, which contains elevated levels of endogenous β‐I, providing a further evidence for its effect on B.c. infestation. Our work unraveled β‐I as a further carotenoid‐derived regulatory metabolite and indicates the possibility of establishing this natural volatile as an environmentally friendly bio‐fungicide to control B.c. Significance Statement: Plants rely on a wide range of metabolites to coordinate their growth and to respond to environmental stimuli. The family of carotenoid‐cleavage products, apocarotenoids, is emerging as a source of growth‐regulating and signaling molecules conferring protection against abiotic and biotic stresses. We show that the apocarotenoid, β‐ionone, is a regulatory metabolite that reshapes Arabidopsis transcriptome and hormone content, increasing resistance to the necrotrophic fungus Botrytis cinerea (B.c.) in Arabidopsis, tobacco and tomato plants. [ABSTRACT FROM AUTHOR]