Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, China.
The Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing, China.
mBio. 2024 Apr 10;15(4):e0334423. doi: 10.1128/mbio.03344-23. Epub 2024 Mar 19.
Autophagy is a central biodegradation pathway critical in eliminating intracellular cargo to maintain cellular homeostasis and improve stress resistance. At the same time, the key component of the mitogen-activated protein kinase cascade regulating cell wall integrity signaling MoMkk1 has an essential role in the autophagy of the rice blast fungus . Still, the mechanism of how MoMkk1 regulates autophagy is unclear. Interestingly, we found that MoMkk1 regulates the autophagy protein MoAtg9 through phosphorylation. MoAtg9 is a transmembrane protein subjected to phosphorylation by autophagy-related protein kinase MoAtg1. Here, we provide evidence demonstrating that MoMkk1-dependent MoAtg9 phosphorylation is required for phospholipid translocation during isolation membrane stages of autophagosome formation, an autophagic process essential for the development and pathogenicity of the fungus. In contrast, MoAtg1-dependent phosphorylation of MoAtg9 negatively regulates this process, also impacting growth and pathogenicity. Our studies are the first to demonstrate that MoAtg9 is subject to MoMkk1 regulation through protein phosphorylation and that MoMkk1 and MoAtg1 dichotomously regulate autophagy to underlie the growth and pathogenicity of .IMPORTANCE utilizes multiple signaling pathways to promote colonization of host plants. MoMkk1, a cell wall integrity signaling kinase, plays an essential role in autophagy governed by a highly conserved autophagy kinase MoAtg1-mediated pathway. How MoMkk1 regulates autophagy in coordination with MoAtg1 remains elusive. Here, we provide evidence that MoMkk1 phosphorylates MoAtg9 to positively regulate phospholipid translocation during the isolation membrane or smaller membrane structures stage of autophagosome formation. This is in contrast to the negative regulation of MoAtg9 by MoAtg1 for the same process. Intriguingly, MoMkk1-mediated MoAtg9 phosphorylation enhances the fungal infection of rice, whereas MoAtg1-dependant MoAtg9 phosphorylation significantly attenuates it. Taken together, we revealed a novel mechanism of autophagy and virulence regulation by demonstrating the dichotomous functions of MoMkk1 and MoAtg1 in the regulation of fungal autophagy and pathogenicity.
自噬是一种重要的中心降解途径，对于消除细胞内货物以维持细胞内环境平衡和提高应激抗性至关重要。与此同时，调节细胞壁完整性信号的丝裂原活化蛋白激酶级联反应的关键组成部分 MoMkk1 在水稻真菌的自噬中具有重要作用。然而，MoMkk1 调节自噬的机制尚不清楚。有趣的是，我们发现 MoMkk1 通过磷酸化调节自噬蛋白 MoAtg9。MoAtg9 是一种跨膜蛋白，受自噬相关蛋白激酶 MoAtg1 的磷酸化作用。在这里，我们提供了证据，证明 MoMkk1 依赖性 MoAtg9 磷酸化对于自噬体形成过程中的隔离膜阶段的磷脂转运是必需的，这是真菌发育和致病性所必需的自噬过程。相比之下，MoAtg1 依赖性 MoAtg9 磷酸化负调节该过程，也影响生长和致病性。我们的研究首次证明 MoAtg9 受到 MoMkk1 通过蛋白磷酸化的调节，并且 MoMkk1 和 MoAtg1 二分法调节自噬以作为基础生长和致病性。
