Dual roles of an Arabidopsis ESCRT component FREE1 in regulating vacuolar protein transport and autophagic degradation

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 112; no. 6; pp. 1886 - 1891
• Main Authors: Gao, Caiji, Zhuang, Xiaohong, Cui, Yong, Fu, Xi, He, Yilin, Zhao, Qiong, Zeng, Yonglun, Shen, Jinbo, Luo, Ming, Jiang, Liwen
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 10.02.2015; National Acad Sciences
• Subjects: Arabidopsis - genetics; Arabidopsis - physiology; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Autophagy; Autophagy - physiology; Biological Sciences; Biosynthesis; Carrier Proteins - genetics; Carrier Proteins - metabolism; Endosomal Sorting Complexes Required for Transport - metabolism; Flowers & plants; Fluorescence Resonance Energy Transfer; Microscopy, Confocal; Microscopy, Electron, Transmission; Multivesicular Bodies - metabolism; Photobleaching; Plant growth; Protein Transport - genetics; Protein Transport - physiology; Proteins; Vesicular Transport Proteins - genetics; Vesicular Transport Proteins - metabolism; FYVE domain; ESCRT machinery; autophagic degradation; FREE1; vacuole biogenesis
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1421271112

Protein turnover can be achieved via the lysosome/vacuole and the autophagic degradation pathways. Evidence has accumulated revealing that efficient autophagic degradation requires functional endosomal sorting complex required for transport (ESCRT) machinery. However, the interplay between the ESCRT machinery and the autophagy regulator remains unclear. Here, we show that FYVE domain protein required for endosomal sorting 1 (FREE1), a recently identified plant-specific ESCRT component essential for multivesicular body (MVB) biogenesis and plant growth, plays roles both in vacuolar protein transport and autophagic degradation. FREE1 also regulates vacuole biogenesis in both seeds and vegetative cells of Arabidopsis . Additionally, FREE1 interacts directly with a unique plant autophagy regulator SH3 DOMAIN-CONTAINING PROTEIN2 and associates with the PI3K complex, to regulate the autophagic degradation in plants. Thus, FREE1 plays multiple functional roles in vacuolar protein trafficking and organelle biogenesis as well as in autophagic degradation via a previously unidentified regulatory mechanism of cross-talk between the ESCRT machinery and autophagy process. Significance Macroautophagy (hereafter as autophagy) involves the delivery of cytosolic materials via autophagosome upon its fusion with the endosome and lysosome/vacuole. The endosomal sorting complex required for transport (ESCRT) machinery is responsible for the formation of intraluminal vesicles (ILVs) in multivesicular bodies (MVBs) and the sorting of ubiquitinated membrane cargos into MVB ILVs for degradation. Here, we show that, in addition to regulating MVB biogenesis, the plant-specific ESCRT component FYVE domain protein required for endosomal sorting 1 (FREE1) also plays dual roles in vacuolar protein transport and autophagic degradation. FREE1 directly interacts with a plant autophagy regulator SH3 DOMAIN-CONTAINING PROTEIN2 to manipulate the autophagic degradation in plants. Thus, we demonstrate multiple functions of FREE1 and a direct link between the ESCRT machinery and autophagy process in plants.