The degradation of plasma membrane and other membrane-associated proteins require their sorting at endosomes for delivery to the vacuole. Through the endocytic pathway, ubiquitinated membrane proteins (cargo) are delivered to endosomes where the ESCRT (endosomal sorting complex required for transport) machinery sorts them into intralumenal vesicles for degradation. Plants contain both conserved and plant-specific ESCRT subunits. In this review, I discuss the role of characterized plant ESCRT components, the evolutionary diversification of the plant ESCRT machinery, and a recent study showing that endosomal intralumenal vesicles form in clusters of concatenated vesicle buds by temporally uncoupling membrane constriction from membrane fission.

Plant endosomal trafficking

The sorting and packaging of proteins (cargo) into vesicles for transport between donor and acceptor organelles require the selection and concentration of cargo molecules in a limited area of the donor membrane. Cargo molecules can, directly or through adaptors, recruit a cytoplasmic protein coat that aids in the deformation of the membrane into a bud. Adaptor proteins, besides binding cargo, can also directly bind specific phosphoinositides on membranes and other accessory proteins [1]. Internalization by endocytosis and endosomal sorting and degradation are essential cellular processes in the turnover of plasma membrane receptors, transporters, and enzymes. The ability to adjust the composition of the plasma membrane in response to environmental and signaling cues is critical for cell survival, development, and physiological responses. Thus, the complex molecular machineries that control the selection of endocytic and endosomal cargo, vesicle formation, recycling, and degradation are tightly tuned to specific signaling cues within cells.

The major sorting signal for endosomal-mediated degradation is ubiquitin. As part of their degradative sorting pathway, plasma membrane proteins become ubiquitinated, internalized by endocytosis, and delivered to endosomes. In plant cells, the trans-Golgi network (TGN) acts as early endosome receiving the endocytic cargo [2,3]. Other endosomal compartments that act later in this pathway seem to arise from TGN-derived membranes. At endosomes, ubiquitinated proteins are either deubiquitinated and recycled back to the plasma membrane or sorted by the ESCRT (endosomal sorting complex required for transport) machinery into endosome intralumenal vesicles. The ESCRT machinery mediates membrane budding away from the cytoplasm, that is, a vesiculation process in a reverse topology to most vesiculation events, including clathrin-coated endocytosis. As the endosomal membranes become capable of associating with ESCRT proteins and therefore of internalizing portions of their limiting membrane into intralumenal vesicles, they gradually mature into late multivesicular endosome (MVE) that ultimately fuses with vacuoles releasing their contents for degradation.

In budding yeast and animals, there are five multimeric ESCRT complexes (ESCRT-0 to -III and VPS4-VTA1) and other ESCRT-associated proteins that work sequentially in the clustering and sequestration of ubiquitinated cargo proteins into endosomal intralumenal vesicles. ESCRT proteins are found in Archea and all five major groups of eukaryotes, including plants [4]. Plants seem to express most of the ESCRT proteins originally identified in metazoans and yeast with the exception of the canonical ESCRT-0 [4,5] (Table 1), and their protein–protein interaction networks seem to be conserved [69]. Despite the general trend of ESCRT conservation across eukaryotes, some ESCRT subunits have undergone drastic gene expansion in multicellular organisms. In addition, plants have evolved specific ESCRT-related proteins not found in other lineages.

Table 1
ESCRT and ESCRT-related proteins in budding yeast, mammals, and Arabidopsis thaliana
Saccharomyces cerevisiae Mammals Arabidopsis Arabidopsis locus name 
ESCRT-0 ESCRT-0   
Vps27 HRS   
Hse1p STAM1   
 STAM2   
  TOM1-like protein  
 Tom1L1 TOM1A At2g38410 
 Tom1L2-1 TOM1B At5g01760 
 Tom1L2-3 TOM1C At1g76970 
 Tom1L3 TOM1D At4g32760 
 Tom1 TOM1E At1g06210 
  TOM1F At1g21380 
  TOM_L At5g16880 
  TOM1G At5g63640 
  TOM1H At3g08790 
ESCRT-I ESCRT-I ESCRT-I  
Vps23p/Stp22 TSG101/VPS23 ELC/VPS23A At3g12400 
  ELC-like/VPS23B At5g13860 
Vps28p VPS28 VPS28-1 At4g21560 
  VPS28-2 At4g05000 
Vps37p VPS37A VPS37-1 At3g53120 
 VPS37B VPS37-2 At2g36680 
 VPS37C   
 VPS37D   
Mvb12p MVB12   
ESCRT-II ESCRT-II ESCRT-II  
Vps22p EAP30 VPS22 At4g27040 
Vps25p EAP25 VPS25 At4g19003 
Vps36p EAP45 VPS36 At5g04920 
ESCRT-III ESCRT-III ESCRT-III  
Vps2p CHMP2A VPS2.1 At2g06530 
 CHMP2B VPS2.2 At5g44560 
  VPS2.3 At1g03950 
Vps20p CHMP6 VPS20.1 At5g63880 
  VPS20.2 At5g09260 
Vps24p CHMP3 VPS24.1 At5g22950 
  VPS24.2 At3g45000 
Snf7p/Vps32p CHMP4A SNF7.1/VPS32.1 At4g29160 
 CHMP4B SNF7.2/VPS32.2 At2g19830 
 CHMP4C   
Did2p CHMP1A CHMP1A At1g73030 
 CHMP1B CHMP1B At1g17730 
Vps60p CHMP5 VPS60.1 At3g10640 
  VPS60.2 At5g04850 
Ist1p IST1 ISTL11 At1g34220 
Vps4 complex VPS4 complex SKD1 complex  
Vps4p VPS4A SKD1 At2g27600 
 VPS4B   
Vta1 LIP5 LIP5 At4g26750 
Saccharomyces cerevisiae Mammals Arabidopsis Arabidopsis locus name 
ESCRT-0 ESCRT-0   
Vps27 HRS   
Hse1p STAM1   
 STAM2   
  TOM1-like protein  
 Tom1L1 TOM1A At2g38410 
 Tom1L2-1 TOM1B At5g01760 
 Tom1L2-3 TOM1C At1g76970 
 Tom1L3 TOM1D At4g32760 
 Tom1 TOM1E At1g06210 
  TOM1F At1g21380 
  TOM_L At5g16880 
  TOM1G At5g63640 
  TOM1H At3g08790 
ESCRT-I ESCRT-I ESCRT-I  
Vps23p/Stp22 TSG101/VPS23 ELC/VPS23A At3g12400 
  ELC-like/VPS23B At5g13860 
Vps28p VPS28 VPS28-1 At4g21560 
  VPS28-2 At4g05000 
Vps37p VPS37A VPS37-1 At3g53120 
 VPS37B VPS37-2 At2g36680 
 VPS37C   
 VPS37D   
Mvb12p MVB12   
ESCRT-II ESCRT-II ESCRT-II  
Vps22p EAP30 VPS22 At4g27040 
Vps25p EAP25 VPS25 At4g19003 
Vps36p EAP45 VPS36 At5g04920 
ESCRT-III ESCRT-III ESCRT-III  
Vps2p CHMP2A VPS2.1 At2g06530 
 CHMP2B VPS2.2 At5g44560 
  VPS2.3 At1g03950 
Vps20p CHMP6 VPS20.1 At5g63880 
  VPS20.2 At5g09260 
Vps24p CHMP3 VPS24.1 At5g22950 
  VPS24.2 At3g45000 
Snf7p/Vps32p CHMP4A SNF7.1/VPS32.1 At4g29160 
 CHMP4B SNF7.2/VPS32.2 At2g19830 
 CHMP4C   
Did2p CHMP1A CHMP1A At1g73030 
 CHMP1B CHMP1B At1g17730 
Vps60p CHMP5 VPS60.1 At3g10640 
  VPS60.2 At5g04850 
Ist1p IST1 ISTL11 At1g34220 
Vps4 complex VPS4 complex SKD1 complex  
Vps4p VPS4A SKD1 At2g27600 
 VPS4B   
Vta1 LIP5 LIP5 At4g26750 
*

Eleven additional genes in Arabidopsis encode IST1 domain-containing proteins (ISTL1 At1g34220; ISTL2 At1g25420; ISTL3 At4g35730; ISTL4 At4g29440; ISTL5 At2g19710; ISTL6 At1g13340; ISTL7 At4g32350; ISTL8 At1g79910; ISTL9 At1g52315; ISTL10 At2g14830; ISTL11 At3g15490; ISTL12 At1g51900). Only ISTL1 has been implicated in multivesicular endosome sorting [28]. Whether the other ISTL proteins are components of the plant ESCRT machinery remains to be established.

The plant ESCRT machinery

Within eukaryotes, only fungi and animals have the typical ESCRT-0 subunits Vps27p/Hrs (Vacuolar Protein Sorting 27/Hepatocyte Growth Factor-Regulated Tyrosine Kinase Substrate) and Hse1p/STAM1/2 (Signal Transducing Adaptor Molecule1/2) [4]. Both ESCRT-0 subunits contain a VHS (Vps27, Hrs, and STAM) domain that mediates membrane association and a ubiquitin-interacting motif (UIM) that binds ubiquitinated cargo [10,11]. Vps27p/Hrs also has a FYVE (Fab-1, YGL023, Vps27, and EEA1) domain [12] known to bind phosphatidylinositol 3-phosphate (PI3P) [13]. However, most eukaryotic groups, including plants, do not have these ESCRT-0 components. What proteins do initially recognize the ubiquitinated cargo in the absence of ESCRT-0? TOM1 (Target of Myb1) proteins, which also contain VHS domains and are able to bind membranes and ubiquitin, are highly conserved among eukaryotes and seem to be the functional equivalent of an ancestral ESCRT-0 [14]. The Arabidopsis thaliana (At) genome encodes nine TOL (TOM1-LIKE) proteins that bind ubiquitin and participate in the endocytic trafficking of plasma membrane proteins, such as the auxin efflux facilitator PIN2 [15]. Thus, from an evolutionary perspective, Vps27p/Hrs and Hse1p/STAM would be more recent evolutionary acquisitions in metazoans and fungi.

In animals and yeast, ESCRT-I is a heterotetrameric complex composed of Vps23p/Tsg101 (Tumor Susceptibility Gene 101), Vps28p/VPS28, Vps37p/VPS28, and Mvb12p (Multivesicular Body 12) or the Mvb12-like subunit UBAP1 (ubiquitin-associated protein 1) [16]. ESCRT-I exists as a complex in the cytoplasm and is recruited to endosomal membranes upon interaction with the ESCRT-0 complex [1719]. Arabidopsis contains two isoforms of each of the ESCRT-I subunits Vps23p (ELCH/VPS23A and VPS23B), Vps28p (VPS28-1 and VPS28-2), and Vps37p (VPS37-1 and VPS37-2), but no obvious Mvb12-like proteins [4]. Arabidopsis ELCH participates in trichome development and cell division [9]. Arabidopsis vps28-2 and vps37-1 mutant plants are compromised in pathogen responses but otherwise develop normally, suggesting functional redundancy with the other VPS28 and VPS37 isoforms [20]. A plant-specific ESCRT-I-related component called FREE1 (FYVE DOMAIN PROTEIN REQUIRED FOR ENDOSOMAL SORTING 1) was identified in Arabidopsis. FREE1 binds ubiquitin, PI3P, and interacts with ELCH/VPS23A and VPS23B [21]. FREE1 is essential for endosomal vesiculation, seedling development [21,22], polar localization of the iron transporter IRT1 [23], and degradation of plasma membrane proteins and cytosolic abscisic acid (ABA) receptors [24]. In addition, the Arabidopsis Src homology-3 (SH3) domain-containing protein 2 (SH3P2) has been recently shown to bind ubiquitin and acts with ESCRT-I and the deubiquitylating enzyme (DUB) AMSH3 (ASSOCIATED MOLECULE WITH THE SH3 DOMAIN OF STAM3) in endosomal cargo trafficking [25].

In yeast, ESCRT-I recruits ESCRT-II, which consists of three subunits, Vps25p, Vps22p, and Vps36p, in a 2 : 1 : 1 ratio, respectively. Arabidopsis contains only one gene encoding each of the ESCRT-II subunits. A recent study of Arabidopsis VPS36 showed its critical role in embryo and seedling development, trafficking of plasma membrane proteins, and vacuole and MVE formation [26].

The late-acting ESCRT complexes, ESCRT-III and VPS4–LIP5, do not bind the ubiquitinated cargo directly, but mediate membrane constriction and scission at the neck of forming intralumenal vesicles. In yeast and animals, the ESCRT-III complex consists of four core subunits, Vps20p/CHMP6 (Charged Multivesicular Body Protein 6); Snf7p (Sucrose Non-Fermenting 7)/CHMP4; Vps24p/CHMP3; and Vps2p/CHMP2; and three accessory subunits, Did2p/CHMP1; Vps60p/CHMP5; and Ist1p/IST1 (Increased Salt Tolerance 1). Various ESCRT-III subunits contain MIM domains [27] that interact with the MIT domains present in other ESCRT proteins, such as VPS4 and LIP5. All ESCRT-III subunits in Arabidopsis are represented by two closely related isoforms with the exception of Vps2p and Ist1p. Arabidopsis genomes encode three Vps2-like proteins (VPS2.1, VPS2.2, and VPS2.3) [5] and 12 Ist1-like proteins (ISTL1–12) [28] (Figure 1). The diversification of these two subunits in plants is an interesting example of gene duplication followed by function diversification, as the multiple plant isoforms of Vps2p and Ist1p do not seem to act redundantly. For example, only AtVPS2.1 and AtISTL1 seem to play bona fide ESCRT functions [28,29], whereas the function of the other VPS2 and ISTL isoforms is currently unknown.

Molecular phylogenetic analysis of ESCRT-III protein sequences from the vascular plant Arabidopsis thaliana (At), a moss as an example of a non-vascular plant (Physcomitrella patens, Pp), budding yeast (Saccharomyces cerevisiae), and humans (Homo sapiens, Hs) by maximum likelihood.

Figure 1.
Molecular phylogenetic analysis of ESCRT-III protein sequences from the vascular plant Arabidopsis thaliana (At), a moss as an example of a non-vascular plant (Physcomitrella patens, Pp), budding yeast (Saccharomyces cerevisiae), and humans (Homo sapiens, Hs) by maximum likelihood.

The topology of the tree with the highest log-likelihood is shown. Initial tree(s) for the heuristic search were obtained automatically by applying neighbor-joining and BioNJ algorithms to a matrix of pairwise distances estimated using a JTT model and then selecting the topology with a superior log-likelihood value. The analysis involved 58 amino acid sequences. Evolutionary analyses were conducted in MEGA7 [47].

Figure 1.
Molecular phylogenetic analysis of ESCRT-III protein sequences from the vascular plant Arabidopsis thaliana (At), a moss as an example of a non-vascular plant (Physcomitrella patens, Pp), budding yeast (Saccharomyces cerevisiae), and humans (Homo sapiens, Hs) by maximum likelihood.

The topology of the tree with the highest log-likelihood is shown. Initial tree(s) for the heuristic search were obtained automatically by applying neighbor-joining and BioNJ algorithms to a matrix of pairwise distances estimated using a JTT model and then selecting the topology with a superior log-likelihood value. The analysis involved 58 amino acid sequences. Evolutionary analyses were conducted in MEGA7 [47].

The AAA ATPase VPS4 binds and mediates the remodeling of ESCRT-III filaments [3032], probably leading to membrane fission at the vesicle neck and recycling of ESCRT components back to the cytoplasm. In Arabidopsis, there is only one VPS4 homolog named SKD1 (suppressor of K+ deficiency) and, similarly to animals and yeast, its ATPase activity is positively regulated by LIP5 [8]. LIP5 is not necessary for plant survival, but is critical for normal responses to both biotic and abiotic stresses [8,33,34]. Interestingly, Arabidopsis contains a plant-specific protein called PROS (POSITIVE REGULATOR OF SKD1) that increases in vitro ATPase activity of SKD1 and, although it is structurally different from LIP5, can partially rescue protein sorting defects in a yeast strain lacking the LIP5 homolog Vta1 [35]. How LIP5 and PROS co-ordinate the activation of SKD1 in plants is currently unknown.

Mechanism of endosome intralumenal vesicle formation in plants

There are many unanswered questions regarding ESCRT-mediated intralumenal vesicle formation in endosomes. One pertains to the mechanism by which ESCRT components trap the cargo. ESCRT-0, -I, and -II contain ubiquitin-binding subunits that interact with the ubiquitinated cargo proteins at endosomal membranes. However, deubiquitinating enzymes remove the ubiquitin on cargo proteins before their final sequestration into intralumenal vesicles [3638]. This means that, differently from other types of coat-mediated vesiculation, at some point the ESCRT coat loses direct physical contact with the cargo proteins before the vesicle is completely released. In this context, what is preventing the deubiquitinated cargo proteins from diffusing away from their ESCRT-mediated aggregation site? The ESCRT-III subunit Snf7p/VPS32 is known to assemble into long spiral filaments and induce membrane curvature [31,39]. Although ESCRT-III does not seem to bind ubiquitin, the ESCRT-III spirals at the vesicle neck could have a critical role in corralling the ESCRT cargo at the vesicle bud [39,40]. However, whether the membrane-associated ESCRT-III filaments act as a barrier, crowding cargo molecules and preventing their escape by lateral diffusion, has not been demonstrated. But even if ESCRT-III filaments at the vesicle bud neck corral membrane proteins and prevent cargo escape, there is still one more hurdle to overcome. If the ESCRTs are removed from the membrane and recycled back to the cytoplasm by VPS4 before the neck is completely closed, cargo proteins could diffuse away from the budding vesicle. If the ESCRTs remain associated with the endosomal membranes after neck fission, it is possible that part of the ESCRTs could be trapped in the newly formed vesicle and degraded together with the cargo proteins.

Another unresolved issue is how exactly the ESCRTs mediate constriction and membrane fission in endosomes. During intralumenal vesicle formation, the recruitment of ESCRT-II and the assembly of the ESCRT-III complex initiate membrane bending [31,39,41,42]. Based on in vitro studies, yeast and animal Snf7p/VPS32 proteins expressed in bacteria are known to form spiral polymers of different diameters [31,39] but not small enough to drive membrane fission. The binding of VPS4 leads to the remodeling of the ESCRT-III filaments [31,32] and potentially to the subsequent constriction of the forming vesicle neck and vesicle release. Protein crowding [43,44] and relaxation of ESCRT-III spirals [39] at the endosomal budding sites could also contribute to membrane bending. However, how neck constriction and membrane scission are temporally regulated remains unknown.

A recent study in plants using electron tomography, diffusion coefficients of ESCRT cargo proteins, and mathematical simulations shed light onto some of these questions (Figure 2A–I). According to this study, in the absence of a diffusion barrier, half of the cargo proteins could diffuse away from an endosomal vesicle bud in 7 ms [45] (Figure 2H,I). The tomographic analysis of plant endosomes also showed that intralumenal vesicles do not form individually but as large networks of interconnected or concatenated vesicles (Figure 2A–F). After one-vesicle bud forms, another one closer to the limiting membrane is established, pushing the first bud further into the endosomal lumen (Figure 2G). These concatenated vesicle clusters remain connected by narrow bridges of ∼17 nm in diameter, similar in dimensions to the vesicle bud necks connected to the endosomal limiting membrane. The ESCRT-III component AtSNF7 was detected in these intervesicle bridges, suggesting that ESCRT-III proteins remain trapped inside the vesicle cluster in MVEs. Consistently, AtSNF7 was also detected inside vacuoles. Other ESCRT-III subunits, such as AtCHMP1A, AtVPS24.1, AtVPS2.1, and AtISTL1, have been also detected in isolated plant vacuoles by proteomic approaches [46], indicating that AtSNF7 is not the only ESCRT-III proteins trapped inside MVEs and delivered to vacuoles. Mutants for the ESCRT-III subunit CHMP1 and for LIP5 showed a reduced number of intralumenal vesicles and limited concatenation. Based on the present study, it is possible to conclude that at least in plants: (1) ESCRT-mediated membrane constriction and fission can be uncoupled in endosomes resulting in the formation of concatenated clusters of intralumenal vesicles. (2) As ESCRT-III proteins remain associated with luminal membranes inside the vesicle clusters, they are delivered together with cargo protein to the vacuolar for degradation, indicating that not all ESCRT proteins are recycled from the surface of endosomes. (3) The persistent presence of ESCRT-III filaments at the intervesicle bridges and vesicle bud necks may act as diffusion barriers and aid in cargo entrapment within endosome luminal membranes. (4) The co-ordinated action of individual ESCRT components is important for the endosomal vesicle formation and concatenation.

Formation of intralumenal vesicles in plant MVEs and simulation of cargo escape.

Figure 2.
Formation of intralumenal vesicles in plant MVEs and simulation of cargo escape.

Tomographic slice (A) and corresponding tomographic reconstruction (A′) of a wild-type MVE from Arabidopsis. (B) Tomographic slice and (B′) tomographic reconstruction of the MVE depicted in A and A′, showing an interconnected network of vesicle buds with narrow membrane bridges (arrowheads). (C–F) Tomographic slices showing examples of concatenated vesicle bud networks still connected to the endosomal limiting membrane. Interconnecting membrane bridges are indicated by red arrows. (G) Model of vesicle bud concatenation based on electron tomography analysis. Asterisks indicate an early stage in membrane bending during vesicle formation. (H) Geometries of vesicle buds derived from electron tomograms used for the cargo diffusion simulations depicted in (I). The green-shaded area corresponds to the region where the cargo molecules (40 PIN2 particles) were placed to start the simulation; orange-shaded regions correspond to the vesicle bud neck and interconnecting membrane bridges; blue shades label the rest of the internalized membrane, and white areas correspond to the endosomal limiting membrane. (I) Simulated escape times of 40 PIN2 particles placed on the lower hemisphere of the vesicle bud using a DV (diffusion coefficient at vesicle) value of 0.17 µm2. Colored lines indicate the mean number of remaining cargo particles over time from over 300 simulations and the shaded region corresponds to the standard deviation. Gray vertical lines indicate the mean time required for 50% of the cargo (20 PIN2 particles) to reach the limiting membrane. These simulations incorporated volume exclusion considerations and a 5-fold decrease in DV when cargo particles enter neck or bridge regions (DN or diffusion coefficient at neck). 1V, one-vesicle bud; 2V, two-vesicle bud; 3V, three-vesicle bud (scale bars = 50 nm in A, A′, 20 nm in BI″, 10 nm in H). From ref. [28].

Figure 2.
Formation of intralumenal vesicles in plant MVEs and simulation of cargo escape.

Tomographic slice (A) and corresponding tomographic reconstruction (A′) of a wild-type MVE from Arabidopsis. (B) Tomographic slice and (B′) tomographic reconstruction of the MVE depicted in A and A′, showing an interconnected network of vesicle buds with narrow membrane bridges (arrowheads). (C–F) Tomographic slices showing examples of concatenated vesicle bud networks still connected to the endosomal limiting membrane. Interconnecting membrane bridges are indicated by red arrows. (G) Model of vesicle bud concatenation based on electron tomography analysis. Asterisks indicate an early stage in membrane bending during vesicle formation. (H) Geometries of vesicle buds derived from electron tomograms used for the cargo diffusion simulations depicted in (I). The green-shaded area corresponds to the region where the cargo molecules (40 PIN2 particles) were placed to start the simulation; orange-shaded regions correspond to the vesicle bud neck and interconnecting membrane bridges; blue shades label the rest of the internalized membrane, and white areas correspond to the endosomal limiting membrane. (I) Simulated escape times of 40 PIN2 particles placed on the lower hemisphere of the vesicle bud using a DV (diffusion coefficient at vesicle) value of 0.17 µm2. Colored lines indicate the mean number of remaining cargo particles over time from over 300 simulations and the shaded region corresponds to the standard deviation. Gray vertical lines indicate the mean time required for 50% of the cargo (20 PIN2 particles) to reach the limiting membrane. These simulations incorporated volume exclusion considerations and a 5-fold decrease in DV when cargo particles enter neck or bridge regions (DN or diffusion coefficient at neck). 1V, one-vesicle bud; 2V, two-vesicle bud; 3V, three-vesicle bud (scale bars = 50 nm in A, A′, 20 nm in BI″, 10 nm in H). From ref. [28].

Concluding remarks

Plant endosomal sorting relies on both conserved and plant-specific ESCRT components. The large diversification of certain ESCRT subunits, most notably the SKD1 regulator ISTL proteins, suggests that the plant ESCRT machinery could have evolved either different regulatory mechanism or entire new functions within the endomembrane system. In plants, membrane constriction and fission are uncoupled in endosomes, resulting in vesicle concatenation. Whether this is a plant-specific process related to the uniqueness of the plant ESCRT machinery or a widespread phenomenon across eukaryotes remains to be established.

Abbreviations

     
  • At

    Arabidopsis thaliana

  •  
  • CHMP

    charged multivesicular body protein

  •  
  • ESCRT

    endosomal sorting complex required for transport

  •  
  • FREE1

    FYVE DOMAIN PROTEIN REQUIRED FOR ENDOSOMAL SORTING 1

  •  
  • FYVE

    Fab-1, YGL023, Vps27, and EEA1

  •  
  • Hrs

    Hepatocyte Growth Factor-Regulated Tyrosine Kinase Substrate

  •  
  • IST1

    Increased Salt Tolerance 1

  •  
  • Mvb12p

    Multivesicular Body 12

  •  
  • MVE

    multivesicular endosome

  •  
  • PI3P

    phosphatidylinositol 3-phosphate

  •  
  • PROS

    POSITIVE REGULATOR OF SKD1

  •  
  • SH3

    Src homology-3

  •  
  • SKD1

    suppressor of K+ deficiency

  •  
  • Snf7p

    Sucrose Non-Fermenting7

  •  
  • STAM1/2

    Signal Transducing Adaptor Molecule1/2

  •  
  • TGN

    trans-Golgi network

  •  
  • TOM1

    target of Myb1

  •  
  • Tsg101

    Tumor Susceptibility Gene 101

  •  
  • VHS

    Vps27, Hrs, and STAM

  •  
  • Vps27p

    Vacuolar Protein Sorting 27

Funding

Work on endosomal trafficking in the Otegui laboratory is supported by grant NSF MCB1614965 to M.S.O.

Competing Interests

The Author declares that there are no competing interests associated with this manuscript.

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