Cytokinin-activated DIRIGENT13 promotes lignan synthesis to regulate root growth and abiotic stress tolerance by modulating ROS homeostasis in Arabidopsis

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Dirigent (DIR) proteins determine the regio- and stereoselectivity of phenoxy radical coupling between monolignols during (neo)lignan synthesis. However, the role of DIR proteins and lignans in plant development and stress responses remains to be clarified. Here, we show that ArabidopsisDIRIGENT13 (DIR13) is a direct target of cytokinin signaling and that its expression is strongly induced through direct binding of the cytokinin-responsive transcription factors ARR1, ARR10, and ARR12 to the DIR13 promoter. DIR13 is localized in the root endodermis and at the margins of lateral root primordia and emerging lateral roots. Although dispensable for Casparian strip formation, DIR13 promotes both primary and lateral root growth. Untargeted metabolomics and imaging mass spectrometry analyses revealed that DIR13 promotes (neo)lignan synthesis in primary and lateral roots. DIR13 attenuates the inhibitory effects of salt stress on germination and root growth. Moreover, DIR13 promotes reactive oxygen species (ROS) accumulation under both control and salt-stress conditions. Cytokinin further enhances salt-induced ROS production, probably through the synergistic activation of DIR13 transcription by salt and cytokinin. Our results suggest that lignans affect root growth, likely by modulating ROS homeostasis through their ROS-scavenging activity. Overall, we reveal a role for DIR13-produced lignans in ROS-regulated abiotic stress tolerance and the control of root architecture.