Root-derived long-range signals activate ABA synthesis in frd3 leaves to enhance drought resistance

Vascular plants have evolved sophisticated mechanisms of long-distance signaling to cope with environmental stress. Reactive oxygen species (ROS) act as systemic signals in plant stress responses. However, it is not known whether ROS serve as root-to-shoot signals in the drought response. Here, we show that ferric reductase defective3 (frd3) mutants exhibit enhanced drought resistance concomitant with increased NCED3 transcript levels and ABA contents in leaves. The frd3 mutants also have an elevated hydrogen peroxide (H2O2) level in roots and leaves compared with the wild type. Grafting experiments demonstrate that drought resistance can be conferred by the frd3 rootstock, suggesting that long-distance signals derived in frd3 roots trigger ABA level increases in leaves and thereby enhance drought resistance and that H2O2 is a strong candidate for long-distance signals. Furthermore, comparative transcriptome and proteomics analyses revealed that many genes and proteins involved in the abiotic stress response, ROS homeostasis, and signaling pathways were affected in the frd3 mutant, supporting the drought resistance phenotype. Taken together, our findings suggest that frd3 root-derived long-range signals activate ABA synthesis in leaves and enhance drought resistance, indicating possible root-to-shoot H2O2 signaling in the plant drought response.

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