arabidopsis vps38 is required for vacuolar trafficking but ...37 1this work was supported by grants...

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Short title: Arabidopsis VPS38 for vacuolar sorting 1

2

Taijoon Chung 3

Department of Biological Sciences, Pusan National University, Geumjeong-gu, Busan, 4

46241, Republic of Korea; +82-51-510-2265 (office), +82-51-581-2962 (fax) 5

6

Article Title 7

Vacuole trafficking protein VPS38 is dispensable for autophagy 8 9

Han Nim Lee,a Xavier Zarza,b Jeong Hun Kim,a Min Ji Yoon,a,2 Sang-Hoon Kim,c 10

Jae-Hoon Lee,c Nadine Paris,d Teun Munnik,b Marisa S. Otegui,e and Taijoon Chung a,f,3 11

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aDepartment of Biological Sciences, Pusan National University, Busan 46241, Korea 13

bSwammerdam Institute for Life Sciences, Section Plant Cell Biology, University of 14

Amsterdam, 1098 XH Amsterdam, The Netherlands 15

cDepartment of Biology Education, Pusan National University, Busan 46241, Korea 16

dBiochimie et Physiologie Moléculaire des Plantes, Institutd Biologie Intégrative des 17

Plantes, UMR 5004 CNRS/UMR 0386 INRA/Montpellier SupAgro/Université 18

Montpellier 2, F-34060 Montpellier Cedex 1, France 19

eLaboratory of Cell and Molecular Biology and Department of Botany, University of 20

Wisconsin-Madison, Madison, WI 53706, United States 21

fInstitute of Systems Biology, Pusan National University, Busan 46241, Korea 22

Plant Physiology Preview. Published on November 28, 2017, as DOI:10.1104/pp.17.01297

Copyright 2017 by the American Society of Plant Biologists

www.plantphysiol.orgon March 23, 2020 - Published by Downloaded from Copyright © 2017 American Society of Plant Biologists. All rights reserved.

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ORCID: 0000-0002-4919-4913 (T.M), 0000-0003-4699-6950 (M.S.O.), 0000-0002-24

5318-9105 (T.C.) 25

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One Sentence Summary 27

Arabidopsis VPS38 is required for the intracellular localization of PI3P, an important 28

lipid regulator of endosomal and vacuolar trafficking. 29

30

Footnotes 31

H.N.L. performed most of the experiments; X.Z. performed phospholipid analysis, 32

M.S.O. performed transmission electron microscopy; J.H.K., M.J.Y., and S.-H.K. 33

provided technical assistance; H.N.L. and N.P. contributed new analytic tools; H.N.L., 34

X.Z., J.-H.L., N.P., T.M., M.S.O., and T.C. analyzed data; and H.N.L., X.Z., J.-H.L., 35

N.P., T.M., M.S.O., and T.C. wrote the paper. 36

1This work was supported by grants NRF-2014R1A1A1A05003740 and “Cooperative 37

Research Program for Agriculture Science & Technology Development (PJ01110801), 38

RDA, Korea” to T.C., the Netherlands Organization for Scientific Research (NWO 39

867.15.020 and 711.017.005) to T.M., and NSF MCB1614965 to M.S.O. 40

2Current address: Division of Life Sciences, School of Life Sciences and Biotechnology, 41

Korea University, Seoul 02841, Korea 42

3Address correspondence to: [email protected]. 43



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ABSTRACT 44

Phosphatidylinositol 3-phosphate (PI3P) is a signaling molecule that controls a variety 45

of processes in endosomal, autophagic and vacuolar/lysosomal trafficking in yeasts and 46

mammals. Vacuolar protein sorting 34 (Vps34) is a conserved phosphatidylinositol 3-47

kinase (PI3K) present in multiple complexes with specific functions and regulation. In 48

yeast, the PI3K complex II consists of Vps34p, Vps15p, Vps30p/Atg6p, and Vps38p, 49

and is essential for vacuolar protein sorting. Here, we describe the Arabidopsis thaliana 50

homolog of yeast Vps38p and human UV radiation resistance-associated gene (UVRAG) 51

protein. Arabidopsis VPS38 interacts with VPS30/ATG6 both in yeast and in planta. 52

Although the level of PI3P in Arabidopsis vps38 mutants is similar to that in wild type, 53

vps38 cells contain enlarged multivesicular endosomes and fewer organelles enriched in 54

PI3P than the wild type. The vps38 mutants are defective in the trafficking of vacuolar 55

cargo and its receptor VACUOLAR SORTING RECEPTOR 2;1. The mutants also 56

exhibit abnormal cytoplasmic distributions of endocytic cargo, such as auxin efflux 57

carriers PINFORMED 1 (PIN1) and PIN2. Constitutive autophagy is normal in the 58

mutants but starvation-induced autophagy was slightly inhibited. We conclude that 59

Arabidopsis VPS38 is dispensable for autophagy but essential for efficient targeting of 60

biosynthetic and endocytic cargo to the vacuole. 61

62

63



4

INTRODUCTION 64

Vacuoles are the most conspicuous compartments in mature plant cells (Marty, 1999). 65

Their biogenesis and maintenance are not well understood, partly because cargo 66

destined for the vacuole is heterogeneous in function and origin. Soluble or membrane 67

cargo can be biosynthetic (e.g., newly synthesized structural proteins, transporters, and 68

resident vacuolar hydrolases) or degradative (i.e., macromolecules that will be degraded 69

in the vacuole). Most of the biosynthetic cargo is synthesized at the endoplasmic 70

reticulum (ER), reaches the trans-Golgi network (TGN) via the Golgi apparatus, and is 71

delivered into the multivesicular endosomes (MVEs), which partially derives from the 72

TGN (Scheuring et al., 2011). Various soluble vacuolar proteins, such as seed storage 73

proteins (SSPs), bind VACUOLAR SORTING RECEPTORs (VSRs) (De Marcos Lousa 74

et al., 2012) to be properly sorted into the vacuole. The recycling of these receptors for a 75

new round of sorting is mediated by the retromer complex and is essential for 76

continuous delivery of soluble cargo to the vacuole (Shimada et al., 2006; Oliviusson et 77

al., 2006). 78

The TGN also functions as early endosome (EE) in plant cells, receiving 79

plasma membrane (PM) proteins internalized by endocytosis and acting as a merging 80

point for the biosynthetic and endosomal trafficking routes (Viotti et al., 2010). At the 81

TGN/EE, a fraction of the endocytosed PM cargo is recycled back to the cell surface, 82

whereas cargo proteins targeted for degradation are recognized by the ESCRT 83

(Endosomal Sorting Complex Required for Transport) machinery and internalized into 84

intraluminal vesicles (ILVs) in MVEs. The limiting membrane of the MVE fuses with 85

the tonoplast, the vacuolar membrane, releasing its contents into the vacuolar lumen 86

where ILVs are degraded. Thus, MVEs acts as late endosomes (LEs) in plant cells. 87



5

Another trafficking route that delivers cargo to the vacuole is autophagy. Here, 88

cytoplasmic constituents are sequestered into organelles called autophagosomes and 89

directly delivered to the vacuole (Kim et al., 2012). When the outer membrane of the 90

autophagosome fuses with the tonoplast, a vesicle containing the autophagic cargo is 91

released as an autophagic body into the vacuolar lumen, where it is rapidly degraded by 92

vacuolar hydrolases. 93

Polyphosphoinositides (PPIs) play critical roles in intracellular signaling 94

pathways and membrane trafficking (Munnik and Nielsen, 2011; Gerth et al., 2017). In 95

particular, phosphatidylinositol 3-phosphate (PI3P) is important for endosomal, 96

vacuolar/lysosomal, and autophagic trafficking through recruitment of effector proteins 97

(Schink et al., 2013). PI3P effectors typically bind to PI3P through their FYVE (Fab1, 98

YOTB/ZK632.12, Vac1, and EEA1) or PX (Phox homology) domains, such as those 99

found in some subunits of the retromer, ESCRT, and autophagy machinery. In yeast and 100

plants, PI3P is produced through phosphorylation of phosphatidylinositol (PI) by PI 3-101

kinase activity of VPS34. In yeast, two types of Vps34-containing complexes are found, 102

sharing three common proteins (Vps34p, Vps15p, and Vps30p/Atg6p) but differing in 103

the fourth. Vps34 complex I contains Atg14p as additional factor, which participates in 104

the formation of autophagosomes, whereas complex II contains Vps38p, which is 105

required for vacuolar protein sorting (Kihara et al., 2001). Both types of VPS34 106

complexes have also been found in mammals and are presumed to exhibit similar 107

functions (Itakura et al., 2008), except that ATG14L and UV radiation resistance-108

associated gene protein (UVRAG) appear to be the mammalian counterparts of Atg14p 109

and Vps38p, respectively. Whether UVRAG homologs participate in autophagy remains 110

controversial (Levine et al., 2015), and there is evidence that UVRAG and ATG14L can 111



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promote membrane fusion, independently of their roles in the PI 3-kinase complex 112

(Liang et al., 2008; Diao et al., 2015). 113

PI3P is a very minor membrane lipid. Typically, PPIs represent less than a 114

percent of all phospholipids, and PI3P only accounts for ~2.5−5% of all PPIs (Munnik 115

et al., 1994a, 1994b; Vermeer et al., 2006). Its turnover, however, is relatively rapid 116

compared to structural phospholipids as judged by 32Pi-labelling experiments in vivo 117

(Munnik et al., 1994a, 1994b; Vermeer et al., 2006; Leprince et al., 2015). Important 118

topological information has come from studies using the expression of a genetically 119

encoded-PI3P biosensor, which is a tandem FYVE domain fused to a fluorescent protein 120

(FP) of any color (Vermeer et al., 2006; Simon et al., 2014). Co-expression with FP-121

tagged membrane markers revealed that PI3P is highly enriched at LE membrane and 122

the tonoplast (Vermeer et al., 2006; Simon et al., 2014). 123

Biosynthesis of PI3P appears to be essential for normal plant development, as 124

gene silencing dramatically retards plant growth and development (Welters et al., 1994). 125

Moreover, no viable homozygous null mutants have been found for vps34, vps15, or 126

atg6 (Fujiki et al., 2007; Lee et al., 2008). Limited information is available from genetic 127

studies on PI3P effectors in Arabidopsis (van Leeuwen et al., 2004), including the 128

ESCRT component FREE1 (Gao et al., 2014) and the retromer subunits SNX1 129

(Pourcher et al., 2010) and SNX2b (Phan et al., 2008). Pharmacological approaches 130

using PI 3-kinase inhibitors like wortmannin (Wm) have been shown to affect vacuolar 131

sorting (Matsuoka et al., 1995) and MVE morphology (Haas et al., 2007), but because 132

Wm may also affect downstream PPI pools and inhibit PI 4-kinases and other kinases, 133

putative functions of PI3P must be confirmed by genetic approaches (Novakova et al., 134

2014). 135



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Here we describe a plant homolog of the yeast Vps38p and mammalian 136

UVRAG. We show that Arabidopsis VPS38 interacts with ATG6 in yeast and in planta. 137

Arabidopsis vps38 mutants show an altered distribution of PI3P, are defective in the 138

vacuolar trafficking of biosynthetic and endocytic cargo, and exhibit enlarged MVEs. In 139

contrast, no drastic effects on autophagy are found. We propose that VPS38 in plants is 140

involved in efficient vacuolar and endosomal sorting. 141

142

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RESULTS 144

Identification of Plant Homologs of ATG14L/Atg14p and UVRAG/Vps38p 145

The Atg14 domain (pfam10186) is found in both ATG14L and UVRAG, the subunits of 146

mammalian Vps34 complexes I and II, respectively. To identify plant homologs, we 147

searched the GenBank RefSeq database, and found three Arabidopsis genes containing 148

Atg14-domain-like sequences: At1g77890, At4g08540, and At2g32760. For the 149

phylogenetic analysis of the resultant Arabidopsis proteins, we searched RefSeq protein 150

databases using At2g32760 protein as a query in DELTA-BLAST. Amino acid sequence 151

alignment of representative DELTA-BLAST hits (Supplemental Fig. S1) revealed that 152

these sequences could be classified into two groups, based on conserved cysteine 153

repeats at their N terminus (Matsunaga et al., 2010). The cysteine repeats are present in 154

yeast Atg14p, human ATG14L and their putative plant homologs At1g77890 and 155

At4g08540. In contrast, yeast Vps38p, metazoan UVRAG homologs, and At2g32760 156

protein lack these cysteine repeats (Fig. 1A). 157

Using sequence alignment of the putative Atg14 and Vps38p/UVRAG proteins 158

to construct a phylogenetic tree, we found that At2g32760 clustered together with the 159

Vps38/UVRAG proteins (Supplemental Fig. S2). Based on this sequence homology and 160

the molecular genetic evidence presented below, we referred to At2g32760 as 161

Arabidopsis VPS38. 162

163

VPS38 Interacts with Components of the PI 3-Kinase Complex 164

A crystal structure of the yeast Vps34 complex II (Rostislavleva et al., 2015) indicated 165

that Vps38p interacts with Atg6p/Vps30p via their coiled-coil regions, whereas only the 166



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N-terminal region of Vps38p is adjacent to Vps34p. Based on this structural information, 167

we tested the interactions between Arabidopsis VPS38 protein and putative components 168

of the PI 3-kinase complex. Our yeast two-hybrid (Y2H) assay revealed interaction of 169



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VPS38 with ATG6 but not with VPS34 (Supplemental Fig. S3A). VPS38-ATG6 170

interaction in planta was verified by pairwise bimolecular fluorescence 171

complementation (BiFC) (Fig. 1, B–E). We detected positive BiFC signals in the pair of 172

NYFP-VPS38 and CYFP-VPS34 (Fig. 1, B and D) but not in the reciprocal pair of 173

NYFP-VPS34 and CYFP-VPS38 (Fig. 1, C and E). This could be due to the fact that the 174

orientation of the two interacting partners, VPS34 and VPS38, only favors 175

reconstitution of YFP in one of the two combinations or that in the pair NYFP-VPS34 176

and CYFP-VPS38, one or both halves of YFP block interaction between VPS34 and 177

VPS38. 178

To investigate the subcellular localization of VPS38, we generated Arabidopsis 179

plants expressing either VPS38-GFP or mRFP-VPS38 fusion proteins under the 180

Cauliflower Mosaic Virus 35S (CaMV35S) promoter. In both cases, mostly diffuse 181

fluorescence signal was observed in the cytoplasm of guard cells (Supplemental Figs. 182

S3B and S3C), but very weak or no fluorescence was detected in other plant parts, 183

including root tips (Supplemental Fig. S3D). The levels of VPS38-GFP (n = 19 T1 184

plants) and mRFP-VPS38 (n = 20 T1 plants) in all transgenic lines were much lower 185

than we expected based on the use of a strong promoter such as CaMV35S. Transgenic 186

seedlings treated with the proteasome inhibitor MG132 contained a higher level of 187

mRFP-VPS38 (Supplemental Fig. S3E), suggesting that overexpressed mRFP-VPS38 is 188

unstable in Arabidopsis. 189

The subcellular localization of mRFP-VPS38 was compared with LE markers 190

YFP-ARA7/RabF2b and with citrine-2xFYVE (Fig. 1, F and G). The FYVE domain, 191

which binds specifically to PI3P in membranes, has been used as a biosensor for PI3P in 192



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Arabidopsis with preferential localization to LEs but also to tonoplast in specific cells 193

(Simon et al., 2014; Vermeer et al., 2006). Although punctate signals of mRFP-VPS38 194

were weak in transgenic plants, they overlapped with a small fraction of endosomal 195

puncta (Fig. 1F, arrowheads). Interestingly, mRFP-VPS38 puncta were easily observed 196

when citrine-2xFYVE was co-expressed, and mRFP-VPS38 was co-localized with 197

citrine-2xFYVE signal (Fig. 1G). The increased abundance of mRFP-VPS38 puncta in 198

the Citrine-2xFYVE background likely resulted from elevated levels of mRFP-VPS38 199

(Supplemental Fig. S3E). These data indicate that mRFP-VPS38 is associated with 200

organelles enriched in PI3P. 201

202

VPS38 Is Required for Seedling Development and Plant Growth 203

To analyze the function of VPS38 in Arabidopsis, three T-DNA mutant alleles 204

designated as vps38-1, vps38-2, and vps38-3 (Fig. 2A) were investigated. The location 205

of the insertion within the VPS38 gene was confirmed by sequencing, and viable 206

homozygous individuals from each allele were isolated. We found that vps38-1 and 207

vps38-2 did not accumulate full-length VPS38 transcripts (Fig. 2B). Instead, vps38-1 208

produced two VPS38 transcripts (asterisks in Fig. 2B), representing aberrant splice 209

variants encoding exon-skipped and truncated VPS38 polypeptides. The vps38-3 plants 210

accumulated full-length wild-type VPS38 transcripts but only at 1% of the wild-type 211

level (Supplemental Table S1 and Fig. 2B). 212

The vps38 homozygous seedlings showed reduced growth compared to wild 213

type (Fig. 2C). Primary root growth and lateral root development were also inhibited 214

(Fig. 2D; Supplemental Fig. S4A). Interestingly, growth on sucrose-lacking medium 215



12

was severely retarded (Supplemental Fig. S4B), which is characteristic of mutants 216

defective in LE functions too (Silady et al., 2008; Kleine-Vehn et al., 2008). Although 217

vps38 adult plants exhibited stunted growth (Supplemental Fig. S4C), they produced 218

viable homozygous seeds. A leaf-curling phenotype was frequently observed in vps38 219

mutants (Supplemental Fig. S4D). Expression of VPS38-GFP or mRFP-VPS38 220

transgenes rescued developmental phenotypes of vps38-1 (Supplemental Fig. S4E), 221

indicating that the fusion proteins were functional (Supplemental Fig. S3, B−D). 222

223

PI3P Is Aberrantly Distributed in vps38 Mutant Cells 224



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To examine the role of VPS38 in PI3P signaling, the subcellular localization of PI3P 225

was investigated in VPS38/+ and vps38 root cells using the PI3P biosensor, citrine-226

2xFYVE. This biosensor predominantly localizes to the MVE/LE and, to a much lesser 227

extent, with the TGN/EE (Simon et al., 2014; Vermeer et al., 2006). Wortmannin (Wm), 228

a PI 3-kinase inhibitor, is known to induce the formation of ring-shaped YFP-2xFYVE 229

signals (Vermeer et al., 2006). As expected, citrine-2xFYVE was found to decorate 230

small and abundant organelles in control, young root cells (Fig. 3A). In vps38 cells, 231

however, citrine-2xFYVE was detected on enlarged organelles, sometimes in a ring-like 232

pattern, mimicking the organelles found in Wm-treated control seedlings (Fig. 3, A and 233

B). Moreover, the number of citrine-2xFYVE puncta was significantly decreased in 234

vps38 seedlings as was found after Wm treatment (Fig. 3C). The number of the citrine-235

2xFYVE puncta in vps38 was further reduced by Wm, suggesting either residual PI3K 236

activity in vps38 or a PI3K-independent action of Wm on PI3P-enriched organelles. 237

To investigate how the vps38 mutation affects PI3P levels, wild-type and vps38 238

seedlings were 32Pi-labelled in vivo and their phosphoinositide levels determined 239

through TLC and HPLC analysis (Munnik, 2013; Munnik and Zarza, 2013). As shown 240

in Figure 3D and 3E, we did not detect statistically significant changes in the amount of 241

32P-labelled PI3P, however we did find significant increases in the levels of PI(4,5)P2 242

and PI4P in vps38 seedlings (Fig. 3, F and G). Together, these results indicate that 243

VPS38 plays a role in the subcellular distribution of PI3P-enriched organelles, although 244

it does not seem to affect the total PI3P content. 245

246

VPS38 Is Dispensable for Autophagy 247

Wm has inhibitory effects on vacuolar transport and autophagy (Shin et al., 2014; 248



14

Zhuang et al., 2013; Matsuoka et al., 1995). To test whether VPS38 is required for 249



15

autophagy, we employed an autophagy marker, GFP-ATG8a (Kim et al., 2013). Upon 250

activation of autophagy, cytosolic GFP-ATG8a becomes lipidated and associated to 251

autophagic membranes (Chung et al., 2010). As a negative control, we used atg7 252

mutants that cannot lipidate ATG8 (Chung et al., 2010) and therefore, only accumulate 253

soluble GFP-ATG8a in the cytosol. 254

To induce autophagy, we subjected the GFP-ATG8a-expressing seedlings to 255

nitrogen starvation and treated them with or without concanamycin A (ConA), an 256

inhibitor of H+-ATPase at the TGN and the vacuole (Matsuoka et al., 1997; Drose et al., 257

1993). ConA impairs vacuolar hydrolytic activity and thereby stabilizes autophagic 258

bodies decorated with GFP-ATG8a. In vps38 cells, the distribution of the GFP-ATG8a 259

signal was similar to wild-type cells, and GFP-ATG8a fluorescence was weaker than in 260

atg7 root cells (Fig. 4A). Autophagic bodies, detected by ConA treatment, were 261

observed in both wild-type and vps38 vacuoles but not in atg7 vacuoles (Fig. 4A). 262

Similarly, the autophagic delivery of GFP-ATG8a to the vacuole was normal in vps38 263

seedlings that were grown with sufficient nitrogen (Supplemental Fig. S5A). 264

Autophagic flux was quantified by immunoblot analysis of GFP-ATG8a and its 265

cleaved GFP fragment, which is generated by the degradation of GFP-ATG8a upon 266

autophagic delivery to the vacuole (Shin et al., 2014). Autophagic flux was slightly 267

reduced in vps38-1 under nitrogen-deficient condition (Fig. 4B). In contrast, autophagic 268

flux in vps38-3 was indistinguishable from that in wild type (Fig. 4B and Supplemental 269

Fig. S5B). Importantly, in both wild type and vps38, Wm treatment inhibited the 270

accumulation of the 27-kDa GFP fragment (Fig. 4C and Supplemental Fig. S5C; Shin et 271

al., 2014). These results suggest that in plants, VPS38 only plays a minor, VPS34-272

independent role in autophagy. 273



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Consistent with the dispensability of VPS38 in autophagy, vps38 mutants did 274

not show the accelerated leaf senescence typically observed in atg mutants 275

(Supplemental Fig. S5D). Similarly, unlike atg7, vps38 mutants did not exhibit 276

pexophagy-related phenotypes, like overaccumulation of catalase (Supplemental Fig. 277



17

S5E; Shibata et al., 2013). Finally, no punctate signal of mRFP-VPS38 was detected at 278

GFP-ATG8a puncta (Supplemental Fig. S3F). 279

280

VPS38 Is Required for Proper Vacuolar Trafficking of Seed Storage Proteins 281

Yeast VPS38 was originally identified from a genetic screen for mutations affecting 282

vacuolar protein sorting (Rothman et al., 1989). To determine whether vacuolar sorting 283

is compromised in Arabidopsis vps38 mutants, we monitored the proteolytic processing 284

of seed storage protein (SSP) precursor. In Arabidopsis seeds, two abundant classes of 285

SSPs are the 12S globulins and 2S albumins. Their precursor forms, pro-12S globulins 286

and pro-2S albumins, are synthesized at the ER, move through the Golgi apparatus, and 287

are processed to mature forms at the LEs and the vacuole (Otegui et al., 2006). We 288

found that vps38 mutant seeds accumulated pro-12S globulin, similar to many 289

Arabidopsis mutants with defective vacuolar trafficking including the retromer mutant 290

vps29 (Fig. 5A; Shimada et al., 2003; Shimada et al., 2006). However, accumulation of 291

pro-2S albumin in vps38 was not as pronounced as in vps29 (Fig. 5A). Moreover, the 292

over-accumulation of SSP precursors in vps38-1 was completely suppressed by the 293

expression of mRFP-VPS38 or VPS38-GFP (Fig. 5A). 294

Trafficking of SSPs into the vacuole is mediated by VSRs. We examined the 295

effect of vps38 on the subcellular distribution of a fluorescently tagged VSR isoform, 296

VSR2;1::citrine-VSR2;1, which restored an early flowering phenotype of vsr2;1 297

(Supplemental Fig. S4F; Avila et al., 2008). In wild-type Arabidopsis, VSR isoforms 298

have been detected at various endomembrane compartments but predominantly 299

localized at the LEs (De Marcos Lousa et al., 2012). In control (VPS38/+) root cells, 300



18

citrine-VSR2;1 exhibited a punctate pattern in the cytoplasm, whereas in vps38 root tip 301

cells, citrine-VSR2;1 associated with fewer and larger compartments (Fig. 5, B–D). Wm 302

is known to induce the enlargement of LEs (Jaillais et al., 2006; Haas et al., 2007). The 303

citrine-VSR2;1-decorated compartments in vps38 cells were bigger than those in wild-304



19

type cells and somewhat smaller than the enlarged endosomes resulting from Wm 305

treatment (Fig. 5D). The strong citrine-VSR2;1 signals on enlarged compartments of 306

vps38 cells is consistent with the hypothesis that the recycling of citrine-VSR2;1 is 307

compromised in the mutants. Notably, Wm did not cause a further reduction in the 308

number of citrine-VSR2;1 puncta in vps38 mutant (Fig. 5C). Taken together, our results 309

indicate that VPS38 plays a critical role for vacuolar trafficking. 310

To further investigate the effect of VPS38 on the localization of citrine-VSR2;1, 311

we crossed a vps38-1 mutant expressing citrine-VSR2;1 with the LE marker line 312

mCherry-RHA1, and observed F2 seedling roots. In wild-type control, citrine-VSR2;1 313

signals largely separated from the endosome marker, but either Wm treatment or vps38 314

mutation significantly increased the tendency of colocalization (Fig. 5, E and F). This 315

result is consistent with our hypothesis that VPS38 is essential for recycling of the 316

vacuolar sorting receptors from endosomes. 317

318

vps38 Cells Contain Enlarged Late Endosomes and Abnormal Vacuoles 319

We investigated the subcellular distribution of various organelle markers in vps38 320

mutants. Transgenic plants carrying fluorescent markers were crossed to the vps38 321

mutants. Using confocal imaging, we found that, in vps38 cells, the LE marker YFP-322

ARA7 decorated enlarged organelles when compared to wild-type root cells (Fig. 6A). 323

YFP-ARA7 puncta were even larger and often ring-shaped, like in Wm-treated wild-324

type controls, consistent with the pattern observed for the PI3P biosensor (Fig. 3A). The 325

number of YFP-ARA7 puncta was reduced in both vps38 and Wm-treated wild-type 326

cells (Fig. 6A). In contrast, the distribution of the Golgi (Fig. 6B) and TGN marker (Fig. 327



20

6C; Dettmer et al., 2006) in vps38 was similar to wild-type cells. 328

Upon Wm treatment, MVEs become enlarged and produce larger intraluminal 329

vesicles (ILVs; Wang et al., 2009; Haas et al., 2007), suggesting a role for PI3P in the 330

formation of ILVs during the sorting of endocytosed proteins for vacuolar degradation. 331

To assess this possibility, we performed transmission electron microscopy of vps38 332

roots (Fig. 6D and Supplemental Fig. S6, A–C). MVEs in vps38 root cells were easily 333

discernible by the presence of ILVs, and they were significantly larger than wild-type 334

MVEs. The ILVs in both vps38-1 and vps38-2 were also significantly larger than wild-335



21

type endosomes, further suggesting that Wm treatment mimics disruption of VPS38 336

function. In addition, we often found in differentiating vps38 root cells abnormal 337

vacuoles with highly convoluted tonoplasts (Supplemental Fig. S6, D–F), further 338

supporting a role of VPS38 in endosomal and vacuolar function. 339

340

VPS38 Is Crucial for Efficient Vacuolar Degradation of Endocytosed Cargo 341

Because endocytosis and endosomal trafficking play critical roles in plant development 342

by controlling the homeostasis of various PM proteins (Reyes et al., 2011), we 343

investigated whether the abnormal growth and development of vps38 mutants (Fig. 2) 344

could be explained by defects in the endocytic pathway. 345

First, we assessed endocytic uptake and endosomal recycling by analyzing the 346

dynamics of the endocytic tracer FM4-64 and the plasma membrane-localized 347

PINFORMED2 (PIN2) protein fused to GFP. We incubated seedlings in FM4-64 348

(Supplemental Fig. S7A), but found no differences in timing it took the tracer to reach 349

the vacuolar membrane in wild-type and vps38 root cells (Supplemental Fig. S7, B and 350

C). Brefeldin A (BFA) causes the formation of the BFA compartment, an aggregate of 351

the Golgi and TGN membranes that blocks the recycling of endocytosed proteins back 352

to the PM (Geldner et al., 2003; Naramoto et al., 2014). In both wild type and vps38 353

cells, FM4-64 accumulated in BFA bodies, which dissipated again upon washing out the 354

BFA (Supplemental Fig. S7D). Thus, VPS38 does not globally affect the uptake and 355

dynamics of endocytic tracer FM4-64. 356

To test whether vps38 mutation affects recycling of the endocytosed proteins, 357

we carried out BFA washout experiments for PIN2-GFP (Supplemental Fig. S7E). De 358



22

novo synthesis of PIN2-GFP was blocked by cycloheximide treatment, BFA was added 359

to block recycling of PIN2-GFP, and BFA was washed out in the presence of 360

cycloheximide to reinitiate the recycling to the PM. The PIN2-GFP signal at the PM of 361

both wild-type and vps38 root cells was increased 2 h after BFA washout (Supplemental 362

Fig. S7, F and G), indicating that VPS38 is not required for the endosomal recycling of 363

PIN2-GFP. Notably, vps38 seemed to show enhanced recycling of PIN2-GFP at both 2 h 364

and 4 h after washout. This could relate to the higher intensity of intracellular PIN2-365

GFP signal at 0 h in vps38 than in wild type (Supplemental Fig. S7, E–G; see below). 366

Next, we assessed the function of VPS38 in endosomal degradative trafficking 367

of the plasma membrane proteins PIN1, PIN2 and BRASSINOSTEROID 368

INSENSITIVE1 (BRI1) fused to GFP. In vps38, PIN1-GFP accumulated in large (up to 369

5 μm in diameter) cytoplasmic compartments, likely enlarged endosomes or small 370

vacuoles, similar to those observed in control root cells treated with Wm (Fig. 7A, 371

Supplemental Fig. S7H; Kleine-Vehn et al., 2008; Jaillais et al., 2007). vps38 root cells 372

also had more intracellular puncta of PIN2-GFP (Fig. 7, B and D) than control, but 373

ratios of intracellular-to-PM signals of BRI1-GFP did not differ between control and 374

vps38 (Fig. 7, C and E). 375

We observed that some of the intracellular PIN2-GFP signal in vps38 was 376

associated with the tonoplast (Fig. 7F). Accumulation of PM proteins in the tonoplast 377

usually results from a failure to sort proteins targeted for vacuolar degradation into ILVs, 378

as in the case of ESCRT mutants (Spitzer et al., 2009; Buono et al., 2016). Therefore, to 379

investigate the potential role of VPS38 in the degradation of endocytosed membrane 380

proteins, we incubated PIN2-GFP- and BRI1-GFP-expressing seedlings in the dark and 381

in the presence of ConA, both of which were used to monitor GFP fluorescence in the 382



23

vacuolar lumen (Kleine-Vehn et al., 2008). As expected, either dark or ConA treatment 383

led to the accumulation of diffuse GFP signal in the vacuolar lumen of cells expressing 384

PIN2-GFP (Fig. 7G) and BRI1-GFP (Supplemental Fig. S7I). Both Wm treatment and 385



24

the vps38 mutation suppressed the accumulation of diffuse PIN2-GFP (Fig. 7G) and 386

BRI1-GFP (Supplemental Fig. S7I) signal in the vacuolar lumen. These results indicate 387

that VPS38 plays a role in the targeting of endocytosed cargo to the vacuole. 388

389

390



25

Discussion 391

In this study, we identified VPS38 as the Arabidopsis homolog of yeast Vps38 and 392

mammalian UVRAG. This argument is supported by similarities in their amino acid 393

sequence (Supplemental Fig. S1), conserved protein interactions (Fig. 1 and 394

Supplemental Fig. S3), and vps38 phenotypes relating to vacuolar and endosomal 395

trafficking (Figs. 5 and 7). Abnormal subcellular structures observed in vps38 cells 396

include enlarged MVEs (Fig. 6). Transport of biosynthetic cargo (e.g., SSPs) to the 397

vacuole is less efficient in vps38, likely because its receptor VSR cannot be fully 398

retrieved from the endosomes (Fig. 5). The targeting of endocytosed membrane cargo to 399

the vacuole is also inhibited (Fig. 7 and Supplemental Fig. S7). The combination of 400

these defective processes in vacuolar sorting may result in irregular plant development 401

and poor responses to nutrient limitation (Fig. 2 and Supplemental Fig. S4). 402

The biochemical functions of VPS38 are not known. Yeast vps38 mutants 403

showed only a slight decrease in PI 3-kinase activity (Kihara et al., 2001). We found 404

that PI3P levels in vps38 were comparable to that of wild type (Fig. 3), suggesting that 405

PI3P levels are robustly regulated in plants (Vermeer et al., 2006). Several mechanisms 406

for maintaining a PI3P level in vps38 are possible. For example, ATG14 homologs 407

and/or unidentified PI 3-kinases may act redundantly in PI3P production, compensating 408

for the lack of VPS38. Alternatively, the activity of PI3P 3-phosphatases or 5-kinases 409

may be reduced in vps38. Interestingly, D4-phosphorylated phosphoinositides PI(4,5)P2 410

and PI4P accumulated in vps38 (Fig. 3), implying a shift in phosphoinositide 411

metabolism toward the D4-phosphorylation pathway (Munnik and Nielsen, 2011; 412

Novakova et al., 2014). Besides a possible redirection effect on phosphoinositide 413



26

metabolism, vps38 mutations cause defective endosomal and vacuolar trafficking, 414

which may in turn lead to a compensatory remodeling of secretory trafficking, 415

endocytosis, and/or metabolism of PI4P and PI(4,5)P2. Conversely, it is also possible 416

that the change in PI(4,5)P2 and PI4P affects the dynamics of some PM proteins and is 417

partially responsible for some of the abnormal vps38 phenotypes. These possibilities 418

remain to be tested in the future. 419

Molecular interactions and subcellular localization of VPS38 fusion proteins 420

(Fig. 1) led us to speculate that VPS38 recruits a putative plant PI 3-kinase complex II 421

to endosomal compartments via direct interaction with ATG6. It remains to be seen 422

whether the complex is poorly targeted to vps38 endosomes, which may explain fewer 423

citrine-2xFYVE puncta (Fig. 3) and enlarged MVEs (Fig. 6) and other vps38 phenotypes 424

that are mimicked by Wm treatment (Figs. 5, 6, and 7). 425

It is well established that PI3P is crucial for membrane dynamics and sorting 426

events on endosomes through the actions of PI3P effectors (Schink et al., 2013). Based 427

on the known PI3P effectors in mammalian and yeast cells and the effects of Wm on the 428

plant vacuolar trafficking (Tse et al., 2004; daSilva et al., 2005), we proposed at least 429

three classes of potential PI3P effectors in the plant vacuolar trafficking: (i) retromer-430

dependent retrograde transport of vacuolar sorting receptors; (ii) ESCRT-dependent ILV 431

formation; and (iii) MVE maturation, which is mediated by Rab5-to-Rab7 conversion 432

(Ebine et al., 2014; Singh et al., 2014). Our genetic analysis indicated that vps38 is most 433

similar to mutants that are defective in retromer and ESCRT. Like vps38, both retromer-434

defective vps29 and ESCRT-related free1 mutants showed accumulation of PM proteins 435

in endosomal compartments (Fig. 7, A and B; Spitzer et al., 2009; Gao et al., 2014; 436



27

Jaillais et al., 2007). In contrast, abnormal targeting of endocytic cargo to the vacuole 437

was seen in vps38 and ESCRT-related mutants (Fig. 7, F and G; Spitzer et al., 2009; 438

Gao et al., 2014), but not in retromer mutants (Jaillais et al., 2007). The difference 439

suggests that VPS38 is required for two separated PI3P-dependent processes, i.e., 440

vacuolar sorting of biosynthetic and endocytic cargo. 441

Another potential PI3P effector is ATG18a, which is involved in autophagy. 442

However, our data indicated that vps38 mutation did not block autophagy (Fig. 4, 443

Supplemental Fig. S5). It is possible that two Atg14-like proteins, At1g77890 and 444

At4g08540 (Fig. 1A), replace VPS38, as in the autophagy-specific PI 3-kinase complex 445

I in yeast and mammals (Kihara et al., 2001; Itakura et al., 2008). These proteins may 446

also be responsible for the sensitivity of vps38 mutants to Wm in both our autophagic 447

flux (Fig. 4C, Supplemental Fig. S5C) and PI3P biosensor assays (Fig. 3C). 448

Our data are consistent with recent findings that challenge direct involvement 449

of UVRAG/VPS38 in autophagy (Takats et al., 2014; Farre et al., 2010; Jiang et al., 450

2014). However, it is still possible that a role of VPS38 in autophagy is masked by its 451

greater impact on vacuolar protein sorting. For example, mutations in VPS38 may block 452

autophagic flux, but this effect would be canceled out if the mutant vacuole had weaker 453

proteolytic activity due to inefficient vacuolar sorting. 454

Clearly, the use of vps38 mutants provides a new tool to elucidate the in vivo 455

roles of PI3P in plant vacuolar/endosomal sorting pathways, complementing the 456

pharmacological approach of PI 3-kinase inhibitors, which are less specific. For 457

example, Wm has been reported to deplete TGN marker proteins and induce heterotypic 458

fusion of the TGN vesicles with the MVE (Takáč et al., 2012). Treatment with another 459

pan-PI3K inhibitor LY294002 also results in a slight increase in the size of the TGN 460



28

(Fujimoto et al., 2015). Our data that Wm, but not vps38 mutation, was associated with 461

an increase in the punctum size of a TGN marker (Fig. 6C) indicate that inhibition of a 462

non-VPS34 target by Wm and LY294002 is responsible for the apparent enlargement of 463

the TGN. Future investigation on vps38 mutants using pan-PI3K inhibitors and more 464

specific VPS34 inhibitors (Ronan et al., 2014; Dowdle et al., 2014; Bago et al., 2014) 465

may reveal additional major players in PI3P metabolism in plants. 466

467

MATERIALS AND METHODS 468

DNA Constructs and Transgenic Plants 469

The Arabidopsis Biological Resource Center (ABRC; Columbia, Ohio, USA) provided 470

cDNA entry clones for Arabidopsis thaliana VPS29 (ABRC stock # G20137), VPS38 471

(G82505), VPS34 (GC105027), ATG6 (G12843), and SH3P2 (G11736). We amplified 472

cDNA for VPS38(NS) by PCR using primers listed in Supplemental Table S2 and 473

cloned them into pENTR/D-TOPO (Invitrogen). 474

For yeast two-hybrid (Y2H) constructs, the entry clones were reacted with the 475

destination vectors pDEST22 and pDEST32 using LR Clonase (Invitrogen). For 476

bimolecular fluorescence complementation (BiFC), entry clones were recombined with 477

pSITE-nEYFP-C1 or with pSITE-cEYFP-C1 (Martin et al., 2009) via the LR Clonase 478

reaction. 479

For Pro35S::VPS38-GFP and Pro35S::mRFP-VPS38, entry clones for 480

VPS38(NS) and VPS38 were reacted with the destination vectors pMDC83 (Curtis and 481

Grossniklaus, 2003) and pSITE-4CA (Chakrabarty et al., 2007), respectively. 482

To generate stable transformants of Arabidopsis, expression clones were 483



29

introduced into Agrobacterium tumefaciens strain GV3101. Agrobacterium 484

transformants were used to infect Arabidopsis by floral dip method (Clough and Bent, 485

1998). Multiple T1 events were analyzed for initial analysis, and homozygous T3 486

populations from a representative line were used for quantitative analyses. 487

We used the fusion protein citrine-VSR2;1 as previously described (Saint-Jean 488

et al., 2010) except that the 35S promoter was replaced by the promoter of AtVSR2;1 489

(VSR4). The fluorescent tag was put in frame between the signal peptide of VSR2;1 and 490

the sequence of mature VSR2;1. The promoter region starting from -1397 to -3 bp 491

before the start codon was provided by Jan Zouhar (Zouhar et al., 2010). The citrine-492

VSR2;1 coding region was amplified using primers VSR2;1_F and VSR2;1_R and 493

inserted between XhoI and AscI of pENTR/D-TOPO behind the promoter. The final 494

construct was transferred by recombination into pGWB1. The citrine-VSR2;1 construct 495

was introduced into vsr2;1 mutant plants (SALK_094467) by floral dip method. 496

Selection was made using hygromycin plus kanamycin and homozygous T2 plants were 497

selected on the basis of fluorescent progeny. 498

499

Plant Materials and Growth 500

Mutant seeds of vps38-1 (SAIL_552_F02), vps38-2 (SAIL_164_D09), vps38-3 501

(SALK_094540C), vps29-4 (Jaillais et al., 2007), atg7-2 (Chung et al., 2010) and 502

transgenic seeds of ProUBQ10::YFP-ARA7, ProUBQ10::YFP-SYP32, 503

ProUBQ10::mCherry-RHA1 (Geldner et al., 2009), ProUBQ10::Citrine-2xFYVE 504

(Simon et al., 2014) and ProPIN1-PIN1-GFP (Benkova et al., 2003) were obtained from 505

the ABRC. ProVHA-a1::VHA-a1-GFP (Dettmer et al., 2006), ProPIN2::PIN2-GFP (Xu 506



30

and Scheres, 2005), ProBRI1::BRI1-GFP (Nam and Li, 2002) and ProUBQ10::GFP-507

ATG8a (Kim et al., 2013). were previously described. Seeds were germinated on solid 508

MS medium with 1% (w/v) sucrose and 0.25% (w/v) to 0.6% Phytagel (Sigma). For 509

liquid culture, seeds were germinated in 1 mL of liquid MS medium with 1% sucrose. 510

For nitrogen starvation, 7-day-old seedlings were washed and supplemented with liquid 511

MS-N with 1% sucrose (Chung et al., 2009). 512

513

Sequence Analysis 514

For phylogenetic analyses, putative VPS38 and ATG14-like protein sequences were 515

identified by DELTA-BLAST using Arabidopsis VPS38 amino acid sequence as a query. 516

Sequences of BLAST hits were aligned using MUSCLE (Edgar, 2004), and maximum 517

likelihood trees were generated by MEGA 6 (Tamura et al., 2013) using the 518

Jones/Taylor/Thornton matrix-based model, partial deletion of gaps, uniform rates 519

among sites, and 500 bootstrap replicates. Coiled coil regions were predicted by COILS 520

(www.ch.embnet.org/software/COILS_form.html) with more than 30% probability and 521

28 amino acid window width. 522

523

RNA Analysis 524

Seeds were germinated on the solid medium and total RNA was extracted from 10-day-525

old seedlings using Trizol (Invitrogen). Total RNA was treated with DNase I (NEB) and 526

used for cDNA synthesis by RevertAid H Minus reverse transcriptase (Thermo) with 527

oligo-dT primers. cDNA was amplified for 35 (for VPS38) or 26 cycles (for UBC9 as an 528

internal control). For real-time quantitative PCR, real-time PCR mix (SolGent) 529



31

including Evagreen was used. Amounts of transcripts were calculated using the 2-ΔΔCT 530

method (Livak and Schmittgen, 2001) normalizing against UBC9 expression according 531

to the Rotor Gene Q system (Qiagen). The primers used for Reverse transcriptase 532

polymerase chain reaction (RT-PCR) are presented in Supplemental Table S2. 533

534

Protein Interaction 535

An activation domain fusion construct and a DNA binding domain construct were 536

transformed into yeast strain MaV203 using the Yeastmarker Yeast Transformation 537

System 2 (Clontech). Y2H was performed with ProQuest (Invitrogen), using the 538

manufacturer’s instructions. Expression of both constructs was tested on medium 539

lacking Leu and Trp and protein interaction was identified on medium lacking Leu, Trp, 540

and His and containing 25 mM 3-amino-1,2,4-triazole. 541

For BiFC, transgenes were introduced into the Agrobacterium strain GV3101 542

and then used to infiltrate 6-week-old Nicotiana benthamiana leaves as described in 543

Martin et al. (2009). p19 genes were co-infiltrated to repress gene silencing (Voinnet et 544

al., 2003). Leaf epidermal cells were analyzed by confocal microscopy 36 to 48 h after 545

infiltration. 546

547

Immunoblot Analysis 548

For immunoblotting, samples were homogenized in Laemmli buffer and centrifuged at 549

16,000 × g for 10 min. The supernatants were analyzed by SDS-PAGE after boiling. 550

Western blotting was performed as described in Kim et al. (2013). Antibodies used were 551



32

as follows: Anti-GFP (Roche), anti-mCherry (Clontech) and anti-Catalase (Agrisera). 552

The antibodies against Arabidopsis 12S (Shimada et al., 2003), and 2S propeptides 553

(Otegui et al., 2006) were previously described. Band intensity was determined using 554

NIH ImageJ. 555

556

Transmission Electron Microscopy 557

Root tips from 5-day-old wild type Col-0, vps38-1, and vps38-2 seedlings were high-558

pressure frozen in a Baltec HP010, substituted overnight at -80ºC in acetone containing 559

2% (w/v) osmium tetroxide and embedded in Epon resin (Electron Microscopy 560

Sciences). Samples were sectioned, and stained with 2% uranyl acetate in 70% 561

methanol and lead citrate (2.6% lead nitrate and 3.5% sodium citrate, pH 12). For the 562

MVE morphometric analysis two independent roots for each genotype were analyzed 563

using FIJI. In total, we analyzed 46 (Col-0), 34 (vps38-1), and 38 (vps38-2) MVEs and 564

36 (Col-0), 42 (vps38-1), and 47 (vps38-2) ILVs. 565

566

Confocal Microscopy and Image Analysis 567

In most cases, images were acquired using a Zeiss 510 laser scanning confocal 568

microscope. For GFP, YFP, and citrine, a 488-nm laser and BP500-530IR emission filter 569

were used. For mRFP, mCherry and FM4-64, a 543-nm laser and BP565-615IR 570

emission filter were used. For colocalization of mRFP-VPS38 with YFP-ARA7 or with 571

citrine-2xFYVE, Zeiss 710 AxioObserver was used. mRFP-VPS38 was excited by a 572

594-nm laser and 599−638-nm fluorescence was collected. YFP-ARA7 and citrine-573

2xFYVE were excited by a 488-nm laser and 493-563-nm fluorescence was collected. 574



33

For each quantitative analysis, more than 12 regions of interest were analyzed by 575

ImageJ. The number and the size of puncta were measured by Analyze Particles. For the 576

quantification of plasma membrane (PM) and intracellular (IC) signals of PIN2-GFP 577

and BRI1-GFP, PM and IC regions per one cell were manually selected using Area 578

Selection Tools, and the mean brightness value was measured. To calculate the Pearson 579

correlation coefficient (r), the Coloc 2 Plug-in for ImageJ was used. 580

581

Inhibitors and Endocytic Tracer Analysis 582

Inhibitors were added to liquid medium in which seedlings were hydroponically grown 583

for 7 days. Wortmannin (Sigma), concanamycin A (Santa Cruz), brefeldin A (Molecular 584

probes), MG132 (Sigma), and cycloheximide (Sigma) were dissolved in DMSO. For 585

pulse-labeling with endocytic tracer FM4-64 (Molecular Probes), 7- day-old seedlings 586

grown on the MS liquid medium were incubated with cold 5 μM FM4-64 for 5 min. 587

Roots were then washed three times with the liquid MS medium at room temperature, 588

and observed at various times. To detect vacuolar membrane, roots were treated with 5 589

μM FM4-64 for 2 h, then washed and incubated in the liquid MS medium at room 590

temperature for 4 h. For the BFA washout experiments (Martins et al., 2015), roots 591

expressing PIN2-GFP were pre-incubated in liquid medium containing 50 μM 592

cycloheximide for 30 min, and subsequently incubated in medium with 50 μM brefeldin 593

A and 50 μM cycloheximide for 2 h, before being washed out with medium containing 594

50 μM cycloheximide. 595

596

Phosphoinositide Analysis 597



34

Five-d-old wild-type and vps38 seedlings were labelled overnight using [32P]PO43- as 598

detailed in Munnik and Zarza (2013). Next day, fresh label (5-10 µCi/sample) was 599

added for another 60 min, prior to lipid extraction. Extracts were separated by alkaline 600

thin layer chromatography (TLC) and the radioactivity visualized and quantified by 601

PImaging (Munnik and Zarza, 2013). The experiment was performed in triplicate and 3 602

seedlings were used per sample. To distinguish PI3P from PI4P, PIP spots were scraped 603

from the TLC, deacylated, desalted and the resulting GPIPs separated by HPLC using a 604

Parisil-SAX column and a gradient of NaH2PO4 pH 3.7 (Munnik, 2013; Munnik et al., 605

1994a, 1994b). The final results for the different PIP isomers were obtained by 606

quantifying the PIP spots from the TLC and normalizing the results with respect to the 607

ratios of PI3P to PI4P obtained from the HPLC analysis. 608

609

Accession Numbers 610

ATG6 (At3g61710), ATG7 (At5g45900), ATG8a (At4g21980), BRI1 (At4g39400), 611

PIN1 (At1g73590), PIN2 (At5g57090), RABF2b/ARA7 (At4g19640), RHA1 612

(At5g45130), SH3P2 (At4g34660), SYP32 (At3g24350), VHA-a1 (At2g28520), VPS29 613

(At3g47810), VPS34 (At1g60490), VPS38 (At2g32760), VSR2;1 (At2g14720), and 614

UBC9 (At4g27960). 615

616

Supplemental Data 617

Supplemental Figure S1. Alignment of amino acid sequences predicted from 33 618

proteins containing the ATG14 domain. 619

Supplemental Figure S2. A phylogenetic analysis of ATG14 and VPS38/UVRAG 620



35

homologues. 621

Supplemental Figure S3. VPS38 interactions and subcellular localization. 622

Supplemental Figure S4. Phenotypes of Arabidopsis vps38 mutants and 623

complementation tests in this study. 624

Supplemental Figure S5. vps38 mutants show reduced autophagic flux under nitrogen-625

sufficient (+N) conditions but retain sensitivity to Wm. 626

Supplemental Figure S6. vps38 cells have enlarged MVE and abnormal vacuoles. 627

Supplemental Figure S7. vps38 mutants show normal endocytic uptake but defective 628

trafficking of PM proteins into the vacuole. 629

Supplemental Figure S8. Immunoblots used for the quantification in Figure 4B. 630

Supplemental Figure S9. Immunoblots used for the quantification in Figure 4C. 631

Supplemental Table S1. Quantitative RT-PCR to estimate VPS38 transcript level in 632

vps38-3 633

Supplemental Table S2. Primers used for plasmid construction or RT-PCR 634

635

ACKNOWLEDGMENTS 636

We thank Karin Schumacher for providing VHA-a1-GFP; Ben Scheres for PIN2-GFP; 637

Kyoung Hee Nam for BRI1-GFP; and Ikuko Hara-Nishimura for anti-12S globulin 638

antiserum. 639

640

FIGURE LEGENDS 641



36

Figure 1. Conserved domains, protein interactions and subcellular localization of 642

Arabidopsis VPS38. A, Diagram showing conserved domains/motifs in VPS38/UVRAG 643

and ATG14/ATG14L homologs of yeast, human, and Arabidopsis. B to E, In planta 644

interaction assay using bimolecular fluorescence complementation (BiFC) in tobacco 645

leaf epidermis. BiFC combinations of NYFP-VPS38 and various CYFP fusions (B) and 646

of various NYFP fusions and CYFP-VPS38 (C) were tested, and fluorescence 647

quantified from the combinations is shown in D and E, respectively (mean ± SE; n = 6 648

leaf areas of inoculation or more). Background fluorescence from a control pair of 649

NYFP and CYFP was set to zero. Columns marked with asterisks represent significantly 650

different means (*, 0.01 < P < 0.05; **, P < 0.01; t-test). F and G, Colocalization of 651

mRFP-VPS38 with YFP-ARA7 (F) and citrine-2xFYVE (G) in guard cells of 652

Arabidopsis cotyledon epidermis. Arrowheads indicate small puncta of mRFP-VPS38 653

overlapping with larger YFP-ARA7 puncta. Pearson correlation coefficients (PCCs) 654

were calculated from 4 (F) and 8 (G) pairs of guard cells and presented as Mean ± SE. 655

Bars = 5 μm. 656

657

Figure 2. Arabidopsis vps38 mutants show phenotypic similarity to retromer mutants 658

but not to autophagy mutants. A, Diagram of the VPS38 gene. Exons (boxes) and 659

introns (connecting lines) are shown with T-DNA insertion sites (triangles). Grey boxes 660

illustrate untranslated regions, whereas colored boxes represent coding regions. Coding 661

sequences for coiled coil regions (CC) and a conserved C-terminal BARA2 domain 662

(CTD; see Supplemental Fig. S1) are indicated. B, Transcript analysis of vps38 mutants. 663

RT-PCR was performed to determine VPS38 transcript levels using three pairs of 664



37

primers (see arrows in the gene diagram for primer positions) and UBC9 transcript level 665

(internal control). Asterisks indicate vps38-1-specific RT-PCR products representing 666

two aberrant splice variants that either skip exon 2 (two asterisks) or contain additional 667

nucleotides derived from T-DNA vector sequence (one asterisk). C, Picture of 10-day-668

old seedlings with indicated genotypes. Bars = 10 mm. D, Lateral root density of 669

seedlings with indicated genotypes. Seedlings were vertically grown for 9 days. Each 670

bar represents the mean value ± S.E. from more than 16 seedlings. 671

672

Figure 3. vps38 affects the intracellular distribution of PI3P but not its total levels. A, 673

Root tip images of wild-type (WT) and vps38 expressing the PI3P biosensor, citrine-674

2xFYVE. Wild-type and vps38 seedlings expressing the sensor were incubated with 675

either 30 μM Wm or DMSO for 1 h prior to confocal imaging. Arrowheads indicate 676

ring-shaped compartments. Bars = 5 μm. B and C, Graphs illustrate area (B) and density 677

(C) of the citrine-2xFYVE puncta in DMSO- or Wm-treated WT and vps38-1 (mean ± 678

SE; n > 46 regions of interest; *, 0.01 < P < 0.05; **, P < 0.01; two-way ANOVA 679

followed by Tukey’s test). D, Autoradiograph of thin layer chromatography (TLC) of 680

32P-labelled lipid extracts, which were prepared from 3 biological replicates, each 681

consisting of 3 seedlings selected from 4 seed populations of wild type (WT #1, WT #2) 682

and two vps38 alleles that were 32Pi-labelled in vivo. CL, cardiolipin; PG, 683

phosphatidylglycerol; PE, phosphatidylethanolamine; PC, phosphatidylcholine; PI, 684

phosphatidylinositol. E to G, Levels of PI3P (E), PI4P (F), and PI(4,5)P2 (G), which 685

were quantified by phosphoimaging the phosphoinositide spots in D and determining 686

the ratios of PI3P to PI4P by HPLC analysis (see Materials and Methods). Columns 687



38

(Mean ± SD) marked with asterisks represent significantly different means (*, 0.01 < P 688

< 0.05; **, P < 0.01; one-way ANOVA followed by Tukey’s test). 689

690

Figure 4. Autophagy flux under nitrogen starvation (-N) is reduced but not fully 691

inhibited in vps38-1. A, Images of the autophagy marker line GFP-ATG8a in the genetic 692

backgrounds of wild type (WT), atg7-2, vps38-1, and vps38-3. Seven-day-old seedlings 693

were starved for nitrogen for 32 h, and subsequently treated with DMSO or 1 μM ConA 694

for 16 h. Bar = 5 μm. B and C, GFP-ATG8a processing assay of WT, atg7, vps38-1, and 695

vps38-3. Where applicable, seedlings were treated with N starvation (-N) for 2 d, 30 μM 696

Wm for 16 h or 1 μM ConA for 16 h prior to protein extraction. A protein band 697

indicated by an asterisk is an autophagy-independent cleavage product of GFP-ATG8a 698

(Shin et al., 2014). Graphs below illustrate the quantification of 27-kDa GFP band 699

intensities normalized by those of histone H3. Mean ± SE. n = 6 (B) and 5 (C). Columns 700

marked with different letters represent significantly different means according to two-701

way ANOVA followed by Tukey’s test (P < 0.01). 702

703

Figure 5. Vacuolar protein sorting is compromised in vps38 mutants. A, A seed protein 704

profile of the indicated mutants and transgenic plants. A protein blot stained with 705

Ponceau S is shown in the upper panel with seed storage protein species indicated by 706

arrowheads (precursors) and vertical bars (mature forms). The two immunoblots below 707

were generated with antibodies against 12S globulin (middle panel) and pro-2S albumin 708

(lower panel). Each lane contains the protein extract of five dry seeds. B, Confocal 709

microscopy images of Citrine-VSR2;1 transgenic plants with indicated genotypes. Root 710



39

tips of seedlings treated for 1 h with either DMSO or 30 μM Wm were observed. C and 711

D, Graphs illustrate the quantification of citrine-VSR2;1 puncta in wild-type (WT) and 712

vps38-1 mutant cells (mean ± SE; n > 11 regions of interest). E, Confocal images of 713

wild-type and vps38-1 root cells expressing both citrine-VSR2;1 and mCherry-RHA1. 714

Roots were treated with DMSO or Wm as in B. F, Quantification of colocalization using 715

images similar to one shown in E (mean ± SE; n > 23 regions of interest). Columns 716

marked with different letters represent significantly different means according to two-717

way ANOVA followed by Tukey’s test (C and D) or t-test (F) (P < 0.01). Bars = 5 μm. 718

719

Figure 6. MVE morphology is altered in vps38 mutants. A to C, Root tip images of 720

wild-type (WT) and vps38 expressing MVE marker, YFP-ARA7 (A), Golgi marker, 721

YFP-SYP32 (B), and TGN marker, VHA-a1-GFP (C). Wild-type seedlings expressing 722

each marker were incubated with either DMSO or 30 μM Wm for 1 h prior to 723

observation under confocal microscope. Arrowheads indicate ring-shaped compartments. 724

Graphs on the right illustrate the quantities of each marker in DMSO-treated WT and 725

vps38, and Wm-treated WT (mean ± SE; n > 11 regions of interest; *, 0.01 < P < 0.05; 726

**, P < 0.01 by t-test). D, Transmission electron micrograph showing MVEs and their 727

ILVs of WT, vps38-1, and vps38-2. Between 34 and 46 MVEs and between 36 and 47 728

ILVs from two independent roots were analyzed. Bars = 5 μm (A to C) or 500 nm (D). 729

730

Figure 7. Trafficking of endocytic cargo to the vacuole is hindered in vps38 mutants. A 731

to C, Confocal microscopic images of wild type (WT) and vps38 roots expressing PIN1-732

GFP (A), PIN2-GFP (B), or BRI1-GFP (C). Seedlings expressing each marker were 733



40

incubated with either DMSO or 30 μM Wm for 1 h prior to observation under confocal 734

microscope. D and E, Graphs illustrating the quantification of PIN2-GFP (D) and BRI1-735

GFP (E) signal intensities in the PM and intracellular region (mean ± SE; n > 11; *, 0.01 736

< P < 0.05; **, P < 0.01 by t-test). F, Images of wild-type and vps38 roots expressing 737

PIN2-GFP in the presence of the endocytic tracer FM4-64. Seven-day-old seedlings 738

were pulse-labeled with 5 μΜ FM4-64 for 2 h, washed 3 times, and incubated for 4 h 739

prior to observation. G, Images of dark- or ConA-treated WT or vps38 seedlings 740

expressing PIN2-GFP. Seedlings were incubated with either DMSO, 1 μM ConA, or 30 741

μM Wm for 12 h prior to observation. Dark treatment was performed by incubating 742

seedlings for 12 h in the dark. Bars = 5 μm. 743

744

745

746



Parsed CitationsAvila EL, Brown M, Pan S, Desikan R, Neill SJ, Girke T, Surpin M, Raikhel NV (2008) Expression analysis of Arabidopsis vacuolarsorting receptor 3 reveals a putative function in guard cells. J Exp Bot 59: 1149-1161

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Bago R, Malik N, Munson MJ, Prescott AR, Davies P, Sommer E, Shpiro N, Ward R, Cross D, Ganley IG, Alessi DR (2014)Characterization of VPS34-IN1, a selective inhibitor of Vps34, reveals that the phosphatidylinositol 3-phosphate-binding SGK3 proteinkinase is a downstream target of class III phosphoinositide 3-kinase. Biochem J 463: 413-427


Benkova E, Michniewicz M, Sauer M, Teichmann T, Seifertova D, Jurgens G, Friml J (2003) Local, efflux-dependent auxin gradients asa common module for plant organ formation. Cell 115: 591-602


Buono RA, Paez-Valencia J, Miller ND, Goodman K, Spitzer C, Spalding EP, Otegui MS (2016) Role of SKD1 regulators LIP5 and IST1-LIKE1 in endosomal sorting and plant development. Plant Physiol 171: 251-264


Chakrabarty R, Banerjee R, Chung SM, Farman M, Citovsky V, Hogenhout SA, Tzfira T, Goodin M (2007) PSITE vectors for stableintegration or transient expression of autofluorescent protein fusions in plants: probing Nicotiana benthamiana-virus interactions. MolPlant Microbe Interact 20: 740-750


Chung T, Phillips AR, Vierstra RD (2010) ATG8 lipidation and ATG8-mediated autophagy in Arabidopsis require ATG12 expressed fromthe differentially controlled ATG12A AND ATG12B loci. Plant J 62: 483-493


Chung T, Suttangkakul A, Vierstra RD (2009) The ATG autophagic conjugation system in maize: ATG transcripts and abundance of theATG8-lipid adduct are regulated by development and nutrient availability. Plant Physiol 149: 220-234


Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J16: 735-743


Curtis MD, Grossniklaus U (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol133: 462-469


daSilva LL, Taylor JP, Hadlington JL, Hanton SL, Snowden CJ, Fox SJ, Foresti O, Brandizzi F, Denecke J (2005) Receptor salvage fromthe prevacuolar compartment is essential for efficient vacuolar protein targeting. Plant Cell 17: 132-148


De Marcos Lousa C, Gershlick DC, Denecke J (2012) Mechanisms and concepts paving the way towards a complete transport cycle ofplant vacuolar sorting receptors. Plant Cell 24: 1714-1732


Dettmer J, Hong-Hermesdorf A, Stierhof YD, Schumacher K (2006) Vacuolar H+-ATPase activity is required for endocytic and secretorytrafficking in Arabidopsis. Plant Cell 18: 715-730

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http://www.ncbi.nlm.nih.gov/pubmed?term=Avila EL%2C Brown M%2C Pan S%2C Desikan R%2C Neill SJ%2C Girke T%2C Surpin M%2C Raikhel NV %282008%29 Expression analysis of Arabidopsis vacuolar sorting receptor 3 reveals a putative function in guard cells%2E J Exp Bot 59%3A 1149%2D1161&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Bago R%2C Malik N%2C Munson MJ%2C Prescott AR%2C Davies P%2C Sommer E%2C Shpiro N%2C Ward R%2C Cross D%2C Ganley IG%2C Alessi DR %282014%29 Characterization of VPS34%2DIN1%2C a selective inhibitor of Vps34%2C reveals that the phosphatidylinositol 3%2Dphosphate%2Dbinding SGK3 protein kinase is a downstream target of class III phosphoinositide 3%2Dkinase%2E Biochem J 463%3A 413%2D427&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Benkova E%2C Michniewicz M%2C Sauer M%2C Teichmann T%2C Seifertova D%2C Jurgens G%2C Friml J %282003%29 Local%2C efflux%2Ddependent auxin gradients as a common module for plant organ formation%2E Cell 115%3A 591%2D602&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Benkova E, Michniewicz M, Sauer M, Teichmann T, Seifertova D, Jurgens G, Friml J (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115: 591-602

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http://www.ncbi.nlm.nih.gov/pubmed?term=Buono RA%2C Paez%2DValencia J%2C Miller ND%2C Goodman K%2C Spitzer C%2C Spalding EP%2C Otegui MS %282016%29 Role of SKD1 regulators LIP5 and IST1%2DLIKE1 in endosomal sorting and plant development%2E Plant Physiol 171%3A 251%2D264&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Buono RA, Paez-Valencia J, Miller ND, Goodman K, Spitzer C, Spalding EP, Otegui MS (2016) Role of SKD1 regulators LIP5 and IST1-LIKE1 in endosomal sorting and plant development. Plant Physiol 171: 251-264

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http://www.ncbi.nlm.nih.gov/pubmed?term=Chakrabarty R%2C Banerjee R%2C Chung SM%2C Farman M%2C Citovsky V%2C Hogenhout SA%2C Tzfira T%2C Goodin M %282007%29 PSITE vectors for stable integration or transient expression of autofluorescent protein fusions in plants%3A probing Nicotiana benthamiana%2Dvirus interactions%2E Mol Plant Microbe Interact 20%3A 740%2D750&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Clough SJ%2C Bent AF %281998%29 Floral dip%3A a simplified method for Agrobacterium%2Dmediated transformation of Arabidopsis thaliana%2E Plant J 16%3A 735%2D743&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Diao J%2C Liu R%2C Rong Y%2C Zhao M%2C Zhang J%2C Lai Y%2C Zhou Q%2C Wilz LM%2C Li J%2C Vivona S%2C Pfuetzner RA%2C Brunger AT%2C Zhong Q %282015%29 ATG14 promotes membrane tethering and fusion of autophagosomes to endolysosomes%2E Nature 520%3A 563%2D566&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Jaillais Y%2C Fobis%2DLoisy I%2C Miege C%2C Rollin C%2C Gaude T %282006%29 AtSNX1 defines an endosome for auxin%2Dcarrier trafficking in Arabidopsis%2E Nature 443%3A 106%2D109&dopt=abstract

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Matsuoka K, Bassham DC, Raikhel NV, Nakamura K (1995) Different sensitivity to wortmannin of two vacuolar sorting signals indicatesthe presence of distinct sorting machineries in tobacco cells. J Cell Biol 130: 1307-1318


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http://scholar.google.com/scholar?as_q=Transient expression in Nicotiana benthamiana fluorescent marker lines provides enhanced definition of protein localization, movement and interactions in planta&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Martin&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Martins S%2C Dohmann EM%2C Cayrel A%2C Johnson A%2C Fischer W%2C Pojer F%2C Satiat%2DJeunemaitre B%2C Jaillais Y%2C Chory J%2C Geldner N%2C Vert G %282015%29 Internalization and vacuolar targeting of the brassinosteroid hormone receptor BRI1 are regulated by ubiquitination%2E Nat Commun 6%3A 6151&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Marty F %281999%29 Plant vacuoles%2E Plant Cell 11%3A 587%2D600&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Matsunaga K%2C Morita E%2C Saitoh T%2C Akira S%2C Ktistakis NT%2C Izumi T%2C Noda T%2C Yoshimori T %282010%29 Autophagy requires endoplasmic reticulum targeting of the PI3%2Dkinase complex via Atg14L%2E J Cell Biol 190%3A 511%2D521&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Matsuoka K%2C Bassham DC%2C Raikhel NV%2C Nakamura K %281995%29 Different sensitivity to wortmannin of two vacuolar sorting signals indicates the presence of distinct sorting machineries in tobacco cells%2E J Cell Biol 130%3A 1307%2D1318&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Matsuoka K%2C Higuchi T%2C Maeshima M%2C Nakamura K %281997%29 A vacuolar%2Dtype H%2B%2DATPase in a nonvacuolar organelle is required for the sorting of soluble vacuolar protein precursors in tobacco cells%2E Plant Cell 9%3A 533%2D546&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Munnik T %282013%29 Analysis of D3%2D%2C4%2D%2C5%2Dphosphorylated phosphoinositides using HPLC%2E Methods Mol Biol 1009%3A 17%2D24&dopt=abstract

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http://scholar.google.com/scholar?as_q=Analysis of D3-,4-,5-phosphorylated phosphoinositides using HPLC&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Munnik&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Munnik T%2C Irvine RF%2C Musgrave A %281994a%29 Rapid turnover of phosphatidylinositol 3%2Dphosphate in the green alga Chlamydomonas eugametos%3A signs of a phosphatidylinositide 3%2Dkinase signalling pathway in lower plants%3F Biochem J 298 %28 Pt 2%29%3A 269%2D273&dopt=abstract

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Naramoto S, Otegui MS, Kutsuna N, de Rycke R, Dainobu T, Karampelias M, Fujimoto M, Feraru E, Miki D, Fukuda H, Nakano A, Friml J(2014) Insights into the localization and function of the membrane trafficking regulator GNOM ARF-GEF at the Golgi apparatus inArabidopsis. Plant Cell 26: 3062-3076


Novakova P, Hirsch S, Feraru E, Tejos R, van Wijk R, Viaene T, Heilmann M, Lerche J, De Rycke R, Feraru MI, Grones P, Van MontaguM, Heilmann I, Munnik T, Friml J (2014) SAC phosphoinositide phosphatases at the tonoplast mediate vacuolar function in Arabidopsis.Proc Natl Acad Sci U S A 111: 2818-2823


Oliviusson P, Heinzerling O, Hillmer S, Hinz G, Tse YC, Jiang L, Robinson DG (2006) Plant retromer, localized to the prevacuolarcompartment and microvesicles in Arabidopsis, may interact with vacuolar sorting receptors. Plant Cell 18: 1239-1252


Otegui MS, Herder R, Schulze J, Jung R, Staehelin LA (2006) The proteolytic processing of seed storage proteins in Arabidopsisembryo cells starts in the multivesicular bodies. Plant Cell 18: 2567-2581


Phan NQ, Kim SJ, Bassham DC (2008) Overexpression of Arabidopsis sorting nexin AtSNX2b inhibits endocytic trafficking to thevacuole. Mol Plant 1: 961-976


Pourcher M, Santambrogio M, Thazar N, Thierry AM, Fobis-Loisy I, Miege C, Jaillais Y, Gaude T (2010) Analyses of sorting nexinsreveal distinct retromer-subcomplex functions in development and protein sorting in Arabidopsis thaliana. Plant Cell 22: 3980-3991


Reyes FC, Buono R, Otegui MS (2011) Plant endosomal trafficking pathways. Curr Opin Plant Biol 14: 666-673Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Ronan B, Flamand O, Vescovi L, Dureuil C, Durand L, Fassy F, Bachelot MF, Lamberton A, Mathieu M, Bertrand T, Marquette JP, El-Ahmad Y, Filoche-Romme B, Schio L, Garcia-Echeverria C, Goulaouic H, Pasquier B (2014) A highly potent and selective Vps34inhibitor alters vesicle trafficking and autophagy. Nat Chem Biol 10: 1013-1019


Rostislavleva K, Soler N, Ohashi Y, Zhang L, Pardon E, Burke JE, Masson GR, Johnson C, Steyaert J, Ktistakis NT, Williams RL (2015)Structure and flexibility of the endosomal Vps34 complex reveals the basis of its function on membranes. Science 350: aac7365


Rothman JH, Howald I, Stevens TH (1989) Characterization of genes required for protein sorting and vacuolar function in the yeastSaccharomyces cerevisiae. EMBO J 8: 2057-2065


Saint-Jean B, Seveno-Carpentier E, Alcon C, Neuhaus JM, Paris N (2010) The cytosolic tail dipeptide Ile-Met of the pea receptor BP80is required for recycling from the prevacuole and for endocytosis. Plant Cell 22: 2825-2837


Scheuring D, Viotti C, Kruger F, Kunzl F, Sturm S, Bubeck J, Hillmer S, Frigerio L, Robinson DG, Pimpl P, Schumacher K (2011)Multivesicular bodies mature from the trans-Golgi network/early endosome in Arabidopsis. Plant Cell 23: 3463-3481



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http://www.ncbi.nlm.nih.gov/pubmed?term=Naramoto S%2C Otegui MS%2C Kutsuna N%2C de Rycke R%2C Dainobu T%2C Karampelias M%2C Fujimoto M%2C Feraru E%2C Miki D%2C Fukuda H%2C Nakano A%2C Friml J %282014%29 Insights into the localization and function of the membrane trafficking regulator GNOM ARF%2DGEF at the Golgi apparatus in Arabidopsis%2E Plant Cell 26%3A 3062%2D3076&dopt=abstract

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http://scholar.google.com/scholar?as_q=Insights into the localization and function of the membrane trafficking regulator GNOM ARF-GEF at the Golgi apparatus in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Naramoto&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Novakova P%2C Hirsch S%2C Feraru E%2C Tejos R%2C van Wijk R%2C Viaene T%2C Heilmann M%2C Lerche J%2C De Rycke R%2C Feraru MI%2C Grones P%2C Van Montagu M%2C Heilmann I%2C Munnik T%2C Friml J %282014%29 SAC phosphoinositide phosphatases at the tonoplast mediate vacuolar function in Arabidopsis%2E Proc Natl Acad Sci U S A 111%3A 2818%2D2823&dopt=abstract

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http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Novakova&hl=en&c2coff=1

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http://www.ncbi.nlm.nih.gov/pubmed?term=Oliviusson P%2C Heinzerling O%2C Hillmer S%2C Hinz G%2C Tse YC%2C Jiang L%2C Robinson DG %282006%29 Plant retromer%2C localized to the prevacuolar compartment and microvesicles in Arabidopsis%2C may interact with vacuolar sorting receptors%2E Plant Cell 18%3A 1239%2D1252&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Otegui MS%2C Herder R%2C Schulze J%2C Jung R%2C Staehelin LA %282006%29 The proteolytic processing of seed storage proteins in Arabidopsis embryo cells starts in the multivesicular bodies%2E Plant Cell 18%3A 2567%2D2581&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Phan NQ%2C Kim SJ%2C Bassham DC %282008%29 Overexpression of Arabidopsis sorting nexin AtSNX2b inhibits endocytic trafficking to the vacuole%2E Mol Plant 1%3A 961%2D976&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Phan NQ, Kim SJ, Bassham DC (2008) Overexpression of Arabidopsis sorting nexin AtSNX2b inhibits endocytic trafficking to the vacuole. Mol Plant 1: 961-976

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http://www.ncbi.nlm.nih.gov/pubmed?term=Pourcher M%2C Santambrogio M%2C Thazar N%2C Thierry AM%2C Fobis%2DLoisy I%2C Miege C%2C Jaillais Y%2C Gaude T %282010%29 Analyses of sorting nexins reveal distinct retromer%2Dsubcomplex functions in development and protein sorting in Arabidopsis thaliana%2E Plant Cell 22%3A 3980%2D3991&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Reyes FC%2C Buono R%2C Otegui MS %282011%29 Plant endosomal trafficking pathways%2E Curr Opin Plant Biol 14%3A 666%2D673&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Ronan B%2C Flamand O%2C Vescovi L%2C Dureuil C%2C Durand L%2C Fassy F%2C Bachelot MF%2C Lamberton A%2C Mathieu M%2C Bertrand T%2C Marquette JP%2C El%2DAhmad Y%2C Filoche%2DRomme B%2C Schio L%2C Garcia%2DEcheverria C%2C Goulaouic H%2C Pasquier B %282014%29 A highly potent and selective Vps34 inhibitor alters vesicle trafficking and autophagy%2E Nat Chem Biol 10%3A 1013%2D1019&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Rostislavleva K%2C Soler N%2C Ohashi Y%2C Zhang L%2C Pardon E%2C Burke JE%2C Masson GR%2C Johnson C%2C Steyaert J%2C Ktistakis NT%2C Williams RL %282015%29 Structure and flexibility of the endosomal Vps34 complex reveals the basis of its function on membranes%2E Science 350%3A aac7365&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Rothman JH%2C Howald I%2C Stevens TH %281989%29 Characterization of genes required for protein sorting and vacuolar function in the yeast Saccharomyces cerevisiae%2E EMBO J 8%3A 2057%2D2065&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Saint%2DJean B%2C Seveno%2DCarpentier E%2C Alcon C%2C Neuhaus JM%2C Paris N %282010%29 The cytosolic tail dipeptide Ile%2DMet of the pea receptor BP80 is required for recycling from the prevacuole and for endocytosis%2E Plant Cell 22%3A 2825%2D2837&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Saint-Jean B, Seveno-Carpentier E, Alcon C, Neuhaus JM, Paris N (2010) The cytosolic tail dipeptide Ile-Met of the pea receptor BP80 is required for recycling from the prevacuole and for endocytosis. Plant Cell 22: 2825-2837

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http://www.ncbi.nlm.nih.gov/pubmed?term=Scheuring D%2C Viotti C%2C Kruger F%2C Kunzl F%2C Sturm S%2C Bubeck J%2C Hillmer S%2C Frigerio L%2C Robinson DG%2C Pimpl P%2C Schumacher K %282011%29 Multivesicular bodies mature from the trans%2DGolgi network%2Fearly endosome in Arabidopsis%2E Plant Cell 23%3A 3463%2D3481&dopt=abstract

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Shimada T, Yamada K, Kataoka M, Nakaune S, Koumoto Y, Kuroyanagi M, Tabata S, Kato T, Shinozaki K, Seki M, Kobayashi M, KondoM, Nishimura M, Hara-Nishimura I (2003) Vacuolar processing enzymes are essential for proper processing of seed storage proteins inArabidopsis thaliana. J Biol Chem 278: 32292-32299


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Simon ML, Platre MP, Assil S, van Wijk R, Chen WY, Chory J, Dreux M, Munnik T, Jaillais Y (2014) A multi-colour/multi-affinity marker setto visualize phosphoinositide dynamics in Arabidopsis. Plant J 77: 322-337


Singh MK, Kruger F, Beckmann H, Brumm S, Vermeer JE, Munnik T, Mayer U, Stierhof YD, Grefen C, Schumacher K, Jurgens G (2014)Protein delivery to vacuole requires SAND protein-dependent Rab GTPase conversion for MVB-vacuole fusion. Curr Biol 24: 1383-1389


Spitzer C, Reyes FC, Buono R, Sliwinski MK, Haas TJ, Otegui MS (2009) The ESCRT-related CHMP1A and B proteins mediatemultivesicular body sorting of auxin carriers in Arabidopsis and are required for plant development. Plant Cell 21: 749-766


Takáč T, Pechan T, Samajová O, Ovečka M, Richter H, Eck C, Niehaus K, Samaj J (2012) Wortmannin treatment induces changes inArabidopsis root proteome and post-Golgi compartments. J Proteome Res 11: 3127-3142


Takats S, Pircs K, Nagy P, Varga A, Karpati M, Hegedus K, Kramer H, Kovacs AL, Sass M, Juhasz G (2014) Interaction of the HOPScomplex with Syntaxin 17 mediates autophagosome clearance in Drosophila. Mol Biol Cell 25: 1338-1354


Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol BiolEvol 30: 2725-2729


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http://www.ncbi.nlm.nih.gov/pubmed?term=van Leeuwen W%2C Okresz L%2C Bogre L%2C Munnik T %282004%29 Learning the lipid language of plant signalling%2E Trends Plant Sci 9%3A 378%2D384&dopt=abstract

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http://scholar.google.com/scholar?as_q=Learning the lipid language of plant signalling&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=van&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Vermeer JE%2C van Leeuwen W%2C Tobena%2DSantamaria R%2C Laxalt AM%2C Jones DR%2C Divecha N%2C Gadella TW%2CJr%2C Munnik T %282006%29 Visualization of PtdIns3P dynamics in living plant cells%2E Plant J 47%3A 687%2D700&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Viotti C%2C Bubeck J%2C Stierhof YD%2C Krebs M%2C Langhans M%2C van den Berg W%2C van Dongen W%2C Richter S%2C Geldner N%2C Takano J%2C Jurgens G%2C de Vries SC%2C Robinson DG%2C Schumacher K %282010%29 Endocytic and secretory traffic in Arabidopsis merge in the trans%2DGolgi network%2Fearly endosome%2C an independent and highly dynamic organelle%2E Plant Cell 22%3A 1344%2D1357&dopt=abstract

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arabidopsis vps38 is required for vacuolar trafficking but ...37 1this work was supported by grants...

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