β-ionone regulates Arabidopsis thaliana transcriptome and increases its resistance against Botrytis cinerea

Carotenoids are isoprenoid pigments vital for photosynthesis. Moreover, they are the precursor of apocarotenoids that include the phytohormones abscisic acid (ABA) and strigolactones (SLs), and retrograde signaling molecules and growth regulators, such as {beta}-cyclocitral and zaxinone. The apocarotenoid {beta}-ionone ({beta}-I) was previously reported to exert antimicrobial effects. Here, we showed that the application of this scent 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 postharvest fruits. Pre-treatment of tobacco and tomato plants with {beta}-I followed by inoculation with B.c. confirms the conserved effect of {beta}-I and induced immune responses in leaves and fruits. Moreover, there was reduced susceptibility to B.c. in LYCOPENE {beta}-CYCLASE- expressing tomato fruits possessing elevated levels of the endogenous {beta}-I, indicating beneficial biological activities of this compound in planta. Our work unraveled {beta}-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.