A root-based N-hydroxypipecolic acid standby circuit to direct immunity and growth of Arabidopsis shoots.

Soil-borne microorganisms can systemically affect shoot resistance to pathogens relying on jasmonic acid and/or salicylic acid. However, the emanating root triggers in these scenarios remain elusive. Here we identify an N-hydroxypipecolic-acid-(NHP-)directed, salicylic-acid-related mechanism of root-triggered systemic resistance in Arabidopsis, which uses components of systemic acquired resistance known in leaves. However, in contrast to the inductive nature of systemic acquired resistance, FLAVIN-DEPENDENT MONOOXYGENASE 1 (FMO1) continuously synthesizes NHP in roots, while the glucosyltransferase UGT76B1 concomitantly conjugates and immobilizes NHP. Physical grafting experiments and tissue-specific knockouts revealed that the loss of UGT76B1 in roots leads to enhanced NHP release, initiating shoot responses. This counteracting standby FMO1/UGT76B1 circuit is specifically and sensitively modulated by root-associated microorganisms. Endophytic and (hemi)biotrophic fungi induce UGT76B1 degradation and FMO1 expression, resulting in varying levels of NHP being released to the shoot, where this root signal differently modulates defence and growth.