The metacaspase TaMCA1-mediated crosstalk between autophagy and PCD contributes to the defense response of wheat seedlings against powdery mildew.

Powdery mildew (PM), is a significant fungal disease that poses a considerable threat to global agricultural productivity. Autophagy and programmed cell death (PCD) are crucial plant defense responses against PM. However, the role of metacaspases (MCAs) in mediating the interplay between autophagy and PCD in wheat's resistance to PM remains unknown. We discovered that the subcellular localization of TaMCA1 in wheat protoplasts is regulated by its N-terminal domain. Silencing TaMCA1 in the susceptible Henong 6425 enhanced resistance to PM, accompanied by excess reactive oxygen species (ROS) accumulation, increased caspase-3-like protease activity, decreased autophagy and elevated HR-PCD. Conversely, silencing TaMCA1 in the resistant Jinhe 12339 led to heightened susceptibility to PM, characterized by increased autophagy, reduced HR-PCD and ROS that may facilitate Bgt invasion. Notably, silencing TaMCA1 caused increased autophagy in Jinhe 12339, and decreased autophagy in Henong 6425. TaMCA1 interacts with TaATG8/TaATG12 as well as HR-PCD regulators like TaLSD1 and TaLSD3, respectively. Furthermore, silencing TaATG12 decreased susceptibility of Henong 6425 (S), while increasing the susceptibility of Jinhe12339 (R) against PM. We conclude that maintaining a high level of PCD is essential for wheat's resistance to PM. TaMCA1 regulates this resistance by modulating PCD levels through ROS and autophagy.