The BTB/POZ‐MATH Protein ZmBPM1 Interacts With Autophagy‐related Protein ZmATG6 and Modulates the NLR Protein Rp1‐D21‐Mediated Defense Response in Maize
Chang‐Xiao Tang, Tong‐Tong Liu, Qi‐Dong Ge, Xiao‐Ying Liu, Wanxiao Wang, Yang Sun, Yanfei Liu, Faqiang Li, Guan‐Feng WangABSTRACT
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.