TIR domain-containing proteins employ dual regulatory mechanisms to confer TaEDS1-dependent immunity in wheat

The Toll/interleukin-1 receptor (TIR) domains are widely conserved across prokaryotes and eukaryotes. In plants, TIR nucleotide-binding leucine-rich repeat (TNL) proteins serve as the intracellular receptors that defend against pathogens. However, monocots lack TNLs. Wheat (Triticum aestivum) has few TIR domain-containing proteins, and their biological functions remain uncharacterized. Here, we report the identification of a TIR-nucleotide-binding site (NBS)-tetratricopeptide repeat (TNP) protein, TaTNP1, that is involved in wheat resistance against Puccinia striiformis f. sp. tritici (Pst). The P-loop motif in the NBS domain is required for TaTNP1 overexpression-conferred resistance. By contrast, TaTNP1-knockout lines exhibited compromised PAMP-triggered immunity and enhanced susceptibility to Pst. These genetic data indicate that TaTNP1 functions as a positive regulator of wheat immunity. Furthermore, this study demonstrated the contribution of wheat Enhanced Disease Susceptibility 1 (TaEDS1) to Pst resistance using TaEDS1-silenced and -overexpressing lines. In contrast to the TIR-only protein TaTIR, which is an active TIR that triggers TaEDS1-dependent cell death, TaTNP1 plays a non-catalytic, stabilizing role in immunity by directly binding to TaEDS1 and protecting it from proteasomal degradation. Collectively, our findings reveal new insights into how TIR domain-containing proteins modulate wheat immunity, not only through catalytic production of signaling molecules but also via direct binding and stabilization of TaEDS1.