Jasmonate restrains the enhanced growth response of lateral roots induced systemically by a local water deficit

Water availability in drying soils is most often spatially heterogeneous, requiring plants to adjust their root system architecture to sustain water uptake. This acclimation response to water deficit (WD) relies on the integration of local and systemic signals. The later and their mode of action remain poorly understood. Using hydroponic split-root systems in maize and Arabidopsis, we show that, with respect to control well-watered plants, a local WD does not affect shoot biomass but suppresses lateral root (LR) growth in the water-deprived compartment while promoting LR elongation in the well-watered compartment. Spatiotemporal analyses in maize revealed an early and transient (<2h) transcriptomic response of LRs triggered by both local and systemic WD signals. This response involved activation of jasmonate (JA) biosynthesis and signaling components, including MYC2 like regulators and JAZ repressors. It occurred in both the water-deprived and well-watered root halves of split roots, with no evidence of long-distance transport of JA. Furthermore, exogenous methyl jasmonate locally inhibited LR elongation, whereas the Arabidopsis JA insensitive jar1-1 mutant showed an enhanced systemic LR growth response to a local WD. Together, these findings demonstrate that JA acts as an early negative regulator that counterbalances the systemic enhancement of LR growth induced by a local WD, thereby fine-tuning root system architecture and water uptake during local soil drying.