Root-secreted (-)-loliolide modulates both belowground defense and aboveground flowering in Arabidopsis and tobacco (Nicotiana benthamiana).

Plant defense, growth and reproduction can be modulated by chemicals emitted from neighboring plants, mainly via volatile aboveground signals. However, belowground signals and their underlying control mechanisms are largely unknown. Here, we experimentally demonstrate that the root-secreted carotenoid (-)-loliolide mediates both defensive and reproductive responses in wild-type Arabidopsis (WT), a carotenoid-deficient Arabidopsis mutant (szl1-1) and tobacco. WT plants flower later than szl1-1, and secrete (-)-loliolide into the soil but szl1-1 roots do not. When Arabidopsis and tobacco occur together, WT Arabidopsis induces nicotine production and defense-related gene expression in tobacco, whereas szl1-1 impairs the induction but accelerates tobacco flowering. Furthermore, nicotine production and the expression of the key genes involved in nicotine biosynthesis (QPT, PMT1), plant defense (CAT1, SOD1, PR-2a, PI-II, TPI), and flowering (AP1, LFY, SOC1, FT3, FLC) are differently regulated by incubation with WT and szl1-1 root exudates, or (-)-loliolide. In particular, (-)-loliolide upregulated flowering suppressors (FT3 and FLC) and transiently downregulated flowering stimulators (AP1 and SOC1), delaying tobacco flowering. Therefore, root-secreted (-)-loliolide modulates plant belowground defense and aboveground flowering, yielding critical insights into plant-plant signaling interactions.