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 pathogenVerticillium dahliaeare typically associated with wilt symptoms due to occlusion of xylem tissues, the relatedV. longisporuminducesde novoformation 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 secretedVerticilliumprotein,<underline>TRA</underline>NS<underline>D</underline>IFFERENTIATION<underline>E</underline>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.