The type II metacaspase 4 modulates wheat responses to barley stripe mosaic virus infection.

Wheat stripe mosaic disease, induced by barley stripe mosaic virus (BSMV), threatens wheat production. Identifying resistance genes and elucidating their underlying mechanisms are essential for breeding resistant cultivars. Here, we identified a type II metacaspase (MCA) gene from Triticum aestivum, designated TaMCA4, which encodes a 421 amino acid protein containing conserved type II MCA domains and characteristic linker region and is localized in the cytoplasm. TaMCA4 expression was significantly upregulated upon BSMV infection. Silencing TaMCA4 increased viral accumulation, heightened disease susceptibility, and impaired plant growth. This increased susceptibility was associated with exacerbated oxidative stress, with elevated levels of H₂O₂, O2•-, and malondialdehyde (MDA), ultimately leading to reduced photosystem II (PSII) efficiency. Furthermore, TaMCA4 silencing suppressed the BSMV-induced activities of superoxide dismutase (SOD), peroxidase (POD), and catalase (CAT). Autophagy and programmed cell death (PCD) were involved in the wheat response to BSMV infection. TaMCA4 was degraded via the autophagy pathway, although no direct interaction was detected between TaMCA4 and proteins encoded by core autophagy related genes (ATGs). Silencing TaMCA4 caused excessive activation of autophagy in BSMV infected wheat seedling leaves, accompanied by degradation of various organelles, ultimately resulting in autophagic cell death. Overexpressing TaMCA4 effectively inhibited autophagy activity and Bax-induced PCD in tobacco leaves. RNA sequencing-based transcriptome profiling further revealed that both BSMV infection and TaMCA4 silencing caused significant alterations in numerous differentially expressed genes (DEGs), encompassing various molecular functions and metabolic pathways. Collectively, our finding suggest that TaMCA4 may positively regulate wheat defense against BSMV infection and is associated with the modulation of PCD- and autophagy-related responses.