A single pathogen-secreted protein reprograms plants for drought resilience

Climate change-enforced drought stress conditions and diseases caused by pathogens often co-occur and represent one of the greatest challenges in plant science ^1–3 . Wilt pathogens that colonize water-conducting plant tissues can aggravate the problem and affect a wide range of agricultural crops ^4,5 . However, whilst fungal infections with the vascular pathogen Verticillium dahliae are typically associated with wilt symptoms due to occlusion of xylem tissues, the related V. longisporum induces de novo formation of tracheary elements ^6,7 . This promotes not only its virulence but also enables elevated water storage capacity of the infected host plant and resilience against drought stress conditions ^6,7 . Here, we identified a secreted Verticillium protein, TRA NS D IFFERENTIATION E FFECTOR (TRADE), which triggers cell identity switches of bundle sheath cells into tracheary elements. We show that TRADE interacts with the intracellular plant protein VARICOSE (VCS), a conserved component of the mRNA turnover machinery and ortholog of the metazoan protein ENHANCER OF DECAPPING 4 (EDC4/HEDLS/Ge-1) ⁸ . The TRADE-VCS interaction induces SUCROSE NON-FERMENTING 1 (SNF1)-related protein kinase (SRK)-dependent phosphorylation and thus dysfunction of VCS. This affects the abundance of mRNAs encoding master regulators of xylem differentiation and demonstrates how a single pathogen effector protein triggers complex tissue-specific developmental reprogramming and thus promotes abiotic stress resilience.