The MON1-CCZ1 complex plays dual roles in autophagic degradation and vacuolar protein transport in rice.

Autophagy is a highly conserved cellular program in eukaryotic cells which mediates the degradation of cytoplasmic components through the lysosome, also named the vacuole in plants. However, the molecular mechanisms underlying the fusion of autophagosomes with the vacuole remain unclear. Here, we report the functional characterization of a rice (Oryza sativa) mutant with defects in storage protein transport in endosperm cells and accumulation of numerous autophagosomes in root cells. Cytological and immunocytochemical experiments showed that this mutant exhibits a defect in the fusion between autophagosomes and vacuoles. The mutant harbors a loss-of-function mutation in the rice homolog of Arabidopsis thaliana MONENSIN SENSITIVITY1 (MON1). Biochemical and genetic evidence revealed a synergistic interaction between rice MON1 and AUTOPHAGY-RELATED 8a in maintaining normal growth and development. In addition, the rice mon1 mutant disrupted storage protein sorting to protein storage vacuoles. Furthermore, quantitative proteomics verified that the loss of MON1 function influenced diverse biological pathways including autophagy and vacuolar transport, thus decreasing the transport of autophagic and vacuolar cargoes to vacuoles. Together, our findings establish a molecular link between autophagy and vacuolar protein transport, and offer insights into the dual functions of the MON1-CCZ1 (CAFFEINE ZINC SENSITIVITY1) complex in plants. © 2024 The Author(s). Journal of Integrative Plant Biology published by John Wiley & Sons Australia, Ltd on behalf of Institute of Botany, Chinese Academy of Sciences.

Citation

Binglei Zhang, Yihua Wang, Yun Zhu, Tian Pan, Haigang Yan, Xin Wang, Ruonan Jing, Hongming Wu, Fan Wang, Yu Zhang, Xiuhao Bao, Yongfei Wang, Pengcheng Zhang, Yu Chen, Erchao Duan, Xiaohang Han, Gexing Wan, Mengyuan Yan, Xiejun Sun, Cailin Lei, Zhijun Cheng, Zhichao Zhao, Ling Jiang, Yiqun Bao, Yulong Ren, Jianmin Wan. The MON1-CCZ1 complex plays dual roles in autophagic degradation and vacuolar protein transport in rice. Journal of integrative plant biology. 2025 Jan;67(1):35-54

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PMID: 39474758

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