title: A unique plant ESCRT component, FREE1, regulates multivesicular body protein sorting and plant growth.
abstract: Tight control of membrane protein homeostasis by selective degradation is crucial for proper cell signaling and multicellular organismal development. Membrane proteins destined for degradation, such as misfolded proteins or activated receptors, are usually ubiquitinated and sorted into the intraluminal vesicles (ILVs) of prevacuolar compartments/multivesicular bodies (PVCs/MVBs), which then fuse with vacuoles/lysosomes to deliver their contents to the lumen for degradation by luminal proteases. The formation of ILVs and the sorting of ubiquitinated membrane cargoes into them are facilitated by the endosomal sorting complex required for transport (ESCRT) machinery. Plants possess most evolutionarily conserved members of the ESCRT machinery but apparently lack orthologs of ESCRT-0 subunits and the ESCRT-I component Mvb12. Here, we identified a unique plant ESCRT component called FYVE domain protein required for endosomal sorting 1 (FREE1). FREE1 binds to phosphatidylinositol-3-phosphate (PI3P) and ubiquitin and specifically interacts with Vps23 via PTAP-like tetrapeptide motifs to be incorporated into the ESCRT-I complex. Arabidopsis free1 mutant is seedling lethal and defective in the formation of ILVs in MVBs. Consequently, endocytosed plasma membrane (PM) proteins destined for degradation, such as the auxin efflux carrier PIN2, cannot reach the lumen of the vacuole and mislocalize to the tonoplast. Collectively, our findings provide the first functional characterization of a plant FYVE domain protein, which is essential for plant growth via its role as a unique evolutionary ESCRT component for MVB biogenesis and vacuolar sorting of membrane proteins.
authors.affiliation: Centre for Cell & Developmental Biology and State Key Laboratory of Agrobiotechnology, School of Life Sciences, The Chinese University of Hong Kong, Shatin, New Territories, Hong Kong, China.
authors.forename: Caiji
authors.initials: C
authors.lastname: Gao
authors.affiliation: Centre for Cell & Developmental Biology and State Key Laboratory of Agrobiotechnology, School of Life Sciences, The Chinese University of Hong Kong, Shatin, New Territories, Hong Kong, China; Key Laboratory of Plant Resources, Conservation and Sustainable Utilization, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou 510650, China.
authors.forename: Ming
authors.initials: M
authors.lastname: Luo
authors.affiliation: Centre for Cell & Developmental Biology and State Key Laboratory of Agrobiotechnology, School of Life Sciences, The Chinese University of Hong Kong, Shatin, New Territories, Hong Kong, China.
authors.forename: Qiong
authors.initials: Q
authors.lastname: Zhao
authors.affiliation: Centre for Cell & Developmental Biology and State Key Laboratory of Agrobiotechnology, School of Life Sciences, The Chinese University of Hong Kong, Shatin, New Territories, Hong Kong, China.
authors.forename: Renzhi
authors.initials: R
authors.lastname: Yang
authors.affiliation: Centre for Cell & Developmental Biology and State Key Laboratory of Agrobiotechnology, School of Life Sciences, The Chinese University of Hong Kong, Shatin, New Territories, Hong Kong, China.
authors.forename: Yong
authors.initials: Y
authors.lastname: Cui
authors.affiliation: Centre for Cell & Developmental Biology and State Key Laboratory of Agrobiotechnology, School of Life Sciences, The Chinese University of Hong Kong, Shatin, New Territories, Hong Kong, China.
authors.forename: Yonglun
authors.initials: Y
authors.lastname: Zeng
authors.affiliation: Division of Life Science, Division of Biomedical Engineering and State Key Laboratory of Molecular Neuroscience, Hong Kong University of Science and Technology, Clear Water Bay, Kowloon, Hong Kong, China.
authors.forename: Jun
authors.initials: J
authors.lastname: Xia
authors.affiliation: Centre for Cell & Developmental Biology and State Key Laboratory of Agrobiotechnology, School of Life Sciences, The Chinese University of Hong Kong, Shatin, New Territories, Hong Kong, China; CUHK Shenzhen Research Institute, The Chinese University of Hong Kong, Shenzhen 518057, China. Electronic address: ljiang@cuhk.edu.hk.
authors.forename: Liwen
authors.initials: L
authors.lastname: Jiang
mesh_terms: D017360:Arabidopsis / Q000235:genetics* / Q000378:metabolism; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism / Q000502:physiology*; D056827:Endosomal Sorting Complexes Required for Transport / Q000378:metabolism; D011992:Endosomes / Q000378:metabolism; D015870:Gene Expression; D008247:Lysosomes / Q000378:metabolism; D057146:Multivesicular Bodies / Q000378:metabolism; D021381:Protein Transport / Q000235:genetics; D014617:Vacuoles / Q000378:metabolism; D033921:Vesicular Transport Proteins / Q000235:genetics / Q000378:metabolism / Q000502:physiology*
chemical_list: D029681:Arabidopsis Proteins; D056827:Endosomal Sorting Complexes Required for Transport; C000597558:FREE1 protein, Arabidopsis; D033921:Vesicular Transport Proteins