Plant-Specific PB1 Domain Complex Mediates Poplar Defence and Is Targeted by Rust Fungus Secreted Protein MlpSD1

The Phox and Bem1 (PB1) modular domain mediates specific protein-protein interactions that are crucial for immune signalling in eukaryotes. However, the immune signalling network mediated by plant PB1 domain-containing proteins remains poorly understood. In this study, we demonstrate that the poplar rust resistance proteins with PB1 domains, members 1 and 2 (PdRPM1 and PdRPM2), form heterodimers in poplar via their N-terminal PB1 domains. These domains exhibit distinct amino acid sequences that diverge from the canonical PB1-PB1 interactions found in other eukaryotes, representing a plant-specific variant. Knockout of PdRPM1/2 in poplar significantly increased both pustule number and total pustule area following infection with Melampsora larici-populina (Mlp). Further analysis revealed that PdRPM1/2 contributes to poplar resistance against Mlp by regulating the levels of reactive oxygen species (ROS) and jasmonoyl-isoleucine, the biosynthesis of flavonoids, as well as the transcription of defence-related genes. Furthermore, loss of PdRPM1 was sufficient to increase poplar susceptibility to Mlp. We also identified a small secreted protein produced by Mlp during infection that interacts with PdRPM1 and disrupts the assembly of the PdRPM1/2 complex. Based on its role, we named this protein M. larici-populina suppressor of dimerisation 1 (MlpSD1). Thus, we have identified a novel plant-specific PB1 domain-mediated disease resistance complex in poplar and uncovered a rust-derived secreted protein that disrupted the formation of this complex.