J Integr Plant Biol ›› 2025, Vol. 67 ›› Issue (1): 35-54.DOI: 10.1111/jipb.13792  cstr: 32098.14.jipb.13792

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  • 收稿日期:2023-12-19 接受日期:2024-09-27 出版日期:2025-01-01 发布日期:2025-01-15

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

Binglei Zhang1,2†, Yihua Wang3,4†, Yun Zhu1†, Tian Pan3, Haigang Yan3, Xin Wang1, Ruonan Jing1, Hongming Wu3, Fan Wang1, Yu Zhang3, Xiuhao Bao3, Yongfei Wang3, Pengcheng Zhang3, Yu Chen1, Erchao Duan3,4, Xiaohang Han1, Gexing Wan1, Mengyuan Yan1, Xiejun Sun1, Cailin Lei1, Zhijun Cheng1, Zhichao Zhao1, Ling Jiang3,4, Yiqun Bao2*, Yulong Ren1* and Jianmin Wan1,3,4*   

  1. 1. State Key Laboratory of Crop Gene Resources and Breeding, National Key Facility for Crop Gene Resources and Genetic Improvement, Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, China
    2. College of Life Sciences, Nanjing Agricultural University, Nanjing 210095, China
    3. State Key Laboratory of Crop Genetics & Germplasm Enhancement and Utilization, Nanjing Agricultural University, Nanjing 210095, China
    4. Zhongshan Biological Breeding Laboratory, Nanjing 210095, China
    †These authors contributed equally to this work.
    *Correspondences: Yulong Ren (renyulong@caas.cn); Yiqun Bao (baoyiqun@njau.edu.cn); Jianmin Wan (wanjianmin@caas.cn, Dr. Wan is fully responsible for the distribution of all materials associated with this article in the manuscript).
  • Received:2023-12-19 Accepted:2024-09-27 Online:2025-01-01 Published:2025-01-15
  • Supported by:
    This work was supported by grants from the National Key R&D Program of China (2021YFF1000200), Innovation Program of Chinese Academy of Agricultural Sciences, National Natural Science Foundation of China (31830064 and 32172085), and International Science & Technology Innovation Program of Chinese Academy of Agricultural Sciences (CAAS‐ZDRW202109). This work was also supported by the Central Public‐Interest Scientific Institution Basal Research Fund, China (Y2021YJ18) and Jiangsu Nanjing Rice Germplasm Resources National Field Observation and Research Station.

Abstract: 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.

Key words: autophagic degradation, MON1–CCZ1, Rab7, rice, vacuolar trafficking

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