The apocarotenoid ß-ionone regulates the transcriptome of Arabidopsis thaliana and increases its resistance against Botrytis cinerea

Carotenoids are isoprenoid pigments vital for photosynthesis. Moreover, they are the precursor of apocarotenoids including the phytohormones abscisic acid (ABA) and strigolactones (SLs), and retrograde signaling molecules and growth regulators (e.g., ß-cyclocitral and zaxinone). The apocarotenoid ß-ionone (ß-I) was previously reported to exert antimicrobial effects, however, at very high millimolar concentrations. Here, we showed that the application of this volatile 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. These changes, along with modulating the levels of the phytohormones ABA, jasmonic acid and salicylic acid, led to enhanced Arabidopsis resistance to Botrytis cinerea (B.c.); one of the most aggressive and widespread pathogenic fungi affecting numerous plant hosts and causing severe losses of post-harvested fruits. Pre-treatment of tobacco and tomato plants with ß-I followed by inoculation with B.c. confirms the conserved effect of ß-I in crop plants. Moreover, there was reduced susceptibility to B.c. in LYCOPENE ß-CYCLASE-expressing tomato fruits possessing elevated levels of endogenous ß-I, indicating beneficial biological activities of this compound in planta. Our work unraveled ß-I as a further carotenoid-derived regulatory metabolite and opens up new possibilities to control B.c. infection by establishing this natural volatile as an environmentally friendly bio-fungicide. Overall design: To investigate the function of b-ionone we treated Arabidopsis plants by spraying this volatile compound on the plants and then they were kept in a closed environment. Leaf samples were taken at different time points. The same approach was used for pathogen infection of the plants with the fungus botrytis cinerea and leaf samples were collected at 24 hours post infection. We also combined both treatments and spray the plants with b-ionone for 24 hours followed by botrytis cinerea infection and take samples at 24 and 48 hours post infection.