The BTB/POZ-MATH Protein ZmBPM1 Interacts With Autophagy-related Protein ZmATG6 and Modulates the NLR Protein Rp1-D21-Mediated Defense Response in Maize.

BTB/POZ-MATH (BPM) proteins are key regulators to modulate the stability of their substrates via the 26S proteasome. However, their function in plant immunity, particularly in modulating the activity of nucleotide-binding, leucine-rich repeat (NLR) receptor, remains unknown. Here, we demonstrate that maize ZmBPM1, but not its close homolog ZmBPM2, negatively regulates the autoactive NLR protein Rp1-D21 by promoting its degradation through both the 26S proteasome and the autophagy pathways. ZmBPM1 overexpression inhibits Rp1-D21-mediated hypersensitive response (HR), whereas its mutation enhances the HR strength in maize. Notably, ZmBPM1 is primarily localized in the autophagosome-like punctate structures and facilitates relocation of Rp1-D21 from the nucleo-cytoplasmic compartment to these punctate structures. Furthermore, ZmBPM1 promotes the degradation of Rp1-D21 through autophagy pathway by interacting with the autophagy-related protein ZmATG6a/ZmATG6b, therefore inhibiting Rp1-D21-mediated HR. Strikingly, ZmBPM1 also acts as a negative regulator of resistance against southern corn rust caused by Puccinia polysora, a fungus that appears to enhance ZmBPM1-mediated autophagic activity. Our study thus identifies an autophagy-dependent mechanism by which a BPM protein finely controls NLR homeostasis and plant immunity, revealing a previously unrecognized immune regulation mechanism in plants.