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Disentangling metabolic- and defense-control of cell death in plant root-fungal interactions

Cell death is intricately connected with life in multicellular organisms. The balance between cell death, proliferation and differentiation shapes organ development and is critical for the maintenance of tissue homeostasis throughout life. Cell death also plays a central role in host-microbe interactions. Pathogenicity as well as mutualism requires a sophisticated control of host defense responses and nutrient fluxes. Hence, a mutualistic interaction does not imply absence of plant defense and necessitates host metabolic rearrangements. Recently it was shown that regulated cell death (RCD) in roots is required for the establishment of a compatible interaction with the symbiotic endophytic fungi of the order Sebacinales (Basidiomycota). This colonization-dependent cell death is thought to be important for fungal accommodation during root niche differentiation but the host biochemical pathways that underpin the execution of this cellular program and the fungal effectors that initiate this process remain largely unknown. Colonization by the S. indica follows a biphasic strategy. After a biotrophic phase the fungus switches to a cell death phase restricted to the epidermal and first cortex layers which is needed for establishment of symbiosis in barley and Arabidopsis (Lahrmann et al., 2013). Recently we were able to show

  • by proteomics that the beneficial endophyte S. indica secretes two enzymes into the apoplast, the nuclease NucA and the ecto-nucleotidase E5NT, which accumulate at the onset of symbiotic host cell death (Nizam, S. et al., 2019).
  • by biochemical approaches that the combined activity of these two enzymes releases deoxynucleosides from DNA, with a strong preference for dAdo, a potent cell death inducer in animal systems.
  • that dAdo is a host cell death inducer in plants that depends on its uptake via the Arabidopsis transporter ENT3.
  • that a mutation of AtENT3 leads to reduced fungal-mediated cell death during root colonization.
  • this previously undescribed cell death mechanism in plants is similar to Staphylococcus aureus dAdo-mediated immune cell death in animals, which appears to ensure bacterial survival in host tissues.

Using an Arabidopsis mutant line screen with over 6800 T-DNA insertion SALK lines, we have additionally identified an uncharacterized TIR-NLR receptor involved in dAdo-induced cell death, providing an important link to immunometabolism in plants. We showed for the first time that fungal effector enzymes can act synergistically in the apoplast and produce a metabolite that regulate immunity and cell death inside the host cell. On the long run, this will change the view on effector biology and how to study synergistic effector functions in planta. This project is part of a larger initiative on cell death (CRC 1403) and the i-HEAD initiative.