Genetics, Development and Biology Genetics, Development and Publications

2012 Structure and function of endosomes in plant cells Anthony L. Contento Iowa State University

Diane C. Bassham Iowa State University, [email protected]

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Journal of Cell Science ora fCl cec 2,3511–3518 USA 125, Science 50011, Cell IA of Ames, Journal University, State Iowa ( Biology, correspondence Cell for and *Author cells Bassham* Development Genetics, C. of plant Diane Department and in Contento L. endosomes Anthony of function and Structure Commentary 08.Hwvr h raiaino h nooa ytmin system endosomal the of the Spitzer, organization and in the (Otegui compartment However, the intermediate 2008). to an macromolecules of and transport materials the for external point other entry in of an as vacuole plants, as central In serve 2004). endosomes the al., organisms, of et (Saint-Jore-Dupas maintenance wall proper cell degradative the and for at essential proteins for large is defense of sorting some a TGN responsible Appropriate and as 1999). ions acts (Marty, is water, also compounds proteins, and for vacuole , compartment with storage The common in 2011). functions, (Takatsuka -like cells al., some that in vacuole evidence et the with is co-exist can there although and vacuole, Otegui cell central 2011; the Helenius, within and Huotari target 2008). 2010; designated Spitzer, al., a et to provide (Anitei sent Endosomes sorted stored, or then Golgi. be vacuole, and the can or materials to where lysosome compartments lysosomes the internalize intermediate from to to return Golgi of used the their transport from the are in either involved of which materials also are point vesicles, They the first materials. endocytic extracellular within the or are function for organelles sorting lysosomes fusion These core and system. a endomembrane and endosomes, have complex Endosomes (TGN), Golgi . endomembrane the network reticulum, the endoplasmic of trans-Golgi the organelles are main of membrane-bound system series The a of through vesicles. variety or directly a transport either of connected are composed that the is organelles within system macromolecules The of cell. degradation and synthesis, the delivery in sorting, functions system endomembrane eukaryotic The Introduction other growth, of plant those in from pathways. role differences signaling essential their and and an polarity endosomes cell playing plant in words: thus of of organelles Key platform, endocytosis these features signaling After of key responses. role a the the defense describe as discuss activate we act and that Here hormone endosomes organisms the responses. elicitors of membrane, by defense localization pathogen exemplified plasma basic polar and for are to by the development functions receptors with addition polarity from signaling by In cell These endosome), receptors cargo. and of receptors. its late these maintenance ligand-bound release of in hormone the to internalization function brassinosteroid vacuole to after to the BRI1 pathways which known (equivalent with signaling in are fuses in proposed body cells then and been plant which multivesicular transporters has cells, in body, model the plant endosomes A multivesicular an in possibility. functions, a and with a studied into trafficking features, also endosome) been matures unique compartment) have network early prevacuolar some compartments trans-Golgi late have cell endosomal the the endosome, endosomes the defined (recycling to Plant clearly from types vacuole. Two material endosome (equivalent or cells. additional internalized lysosome network animal of the or delivery trans-Golgi to yeast and Golgi of the sorting the that the from from in materials distinct function of organization that transport organelles the of and collection surface heterogeneous a are Endosomes Summary 10.1242/jcs.093559 doi: ß 02 ulse yTeCmayo ilgssLtd Biologists of Company The by Published 2012. npat,lssmsaegnrlyasn nfvro large a of favor in absent generally are lysosomes plants, In Endosome, [email protected] Arabidopsis Endocytosis , ) ta. 06.Hr,w ecietecasfcto n tutr of structure and classification the Robatzek describe 2010; we al., Here, et 2006). Kang (Bar 2007; al., al., et pathways et signaling Geldner several 2009; have of Avni, Endosomes Jackson, require activation and 2009). to al., wall and linked et been Toyooka cell (Bonifacino also 2008; al., and function et Chow membrane sorting 2003; composition plasma The endosomal the 2012). al., proper (S of et tubes structure Richter pollen 2010; and al., as et such Wang the cells including 2006; growth, specialized cell of for in and growth vacuole important the are of endosomes maintenance the Plant biosynthesis. and endocytosis criteria. same the using classified be cannot they plants, transport in and a sorting cargo by major of or functions Although surface similar 2010). third perform cell Prekeris, endosomes and the (Hsu A to TGN back the 2004). to it pathway directs retrograde al., and EE et the from and Tse material internalized receives (RE), yeast 2000; endosome recycling both the al., type, endosome in et (PVC) (Gerrard compartment plants also prevacuolar often the therefore is termed and meet, and endocytic trafficking which vacuolar at biosynthetic point the be The to 2009). considered (MVB), (Spang, generally degradation is for MVB body often transport vacuole, multivesicular for or be lysosome (LE), a a endosome uponto late enter or then intermediate might an components to as or designated recycling might surface, subsequent internalized for cell components endosome the of recycling a internalized to deposition transported The of endocytosis. site according the classified are first (EEs) endosomes be Early endocytosis. during can function their that to identified in been that have endosomes with compared when features cells. unique animal some has plants nooe ev ucin eodtesrigo ag from cargo of sorting the beyond functions serve Endosomes of types different of array an cells, yeast and animal In ˇ mje al., et amaj 3511 Journal of Cell Science rmteTNt Vsi eintdb lc ro.Rtord rnpr rmteVCt h V srpeetdb uvdbakarrows. black curved by represented is MVB the to VAC al. the et from Spitzer 2003; transport al., Retrograde et arrow. Sohn 1999; black al., a et Sanderfoot by des 1998; designated Conceic al., materials Silva et is cellular Sanderfoot da MVBs 2002; as Moore, 2012; to well and al., TGN Rutherford as 1997; et the components, al., (Bottanelli 2006; from vacuolar et shown al., synthesized Paris et are 2002; newly Preuss al., co MVBs 2009; for et membrane with al., Li plasma (4) et associated 2004; which pathway (Geldner Proteins by In shown transport are vacuole. (3), 2008; are the they pathway the RE al., recycling designate as the in et a arrows with ovals) degradation represent Chow associated orange (red arrows Proteins 2000; The red components RE. al., specialized thick, 2002). membrane et a The Moore, plasma (Bassham through 1996). and membrane by listed al., plasma taken are et the Ueda TGN is to 2001; returned the that al., be with (2) et membranmight associated Sanderfoot pathway plasma Proteins 2007; a the TGN. al., shows et the to arrow Lam through route 2002; blue move transport and The biosynthetic vesicles MVB. the endocytic the 1, into sometimes pathway internalized indicate and arrows TGN mult green the or T The through (LE) (RE). endosome organelles. endosome passes recycling tonoplast, between late e the (EE), in traffic by involved endosome surrounded potential organelles vacuole early designate (LPVC), the compartment or arrows displays prevacuolar (TGN) late diagram (PVC), network This compartment trans-Golgi pathways. prevacuolar or (GC), three (MVB) these complex body for Golgi organization (ER), of reticulum point endoplasmic the nucleus, as trafficking: act endosomes early plants. and in network pathway trans-Golgi endocytic The 1. Fig. 2006). into EE al., an of et maturation example, for (Russell endosomes, of through degradation maturation occurs a general for plasma in system endosomal lysosome deliver the the through or Transport the TGN late to the to whereas to late components endosome, them back recycle and recycling either contents can a and early endosomes their by receptors, Both potentially recycle membrane, 6-phosphate RAB11. can be mannose contain endosomes or might endosomes endosomes late RAB7 endosomes recycling RAB5, and contain early RAB4 of can example, presence the of by For detectable presence and (Huotari 2011). the GTPases by Helenius, particular in distinguished proteins, be marker specific can compartments These 2011). 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LE be experimental or might further MVB endosomes and potentially of EE or types appear proteins in TGN compartments there the endosomal date, cells, of studied To and plant defined 1). clearly analysis Table two be (see to the pathways these of and in dissection involved uptake. and the routes endocytic of allowed the have trafficking course in pathways time steps sequentially trafficking distinct a endosomal therefore block during that are inhibitors dye Various route fluorescent 2004). endocytic with al., et labeled the (Bolte on membrane vacuolar Organelles and the compartments by reaches up endosomal eventually taken through is cells, transported intact to endocytosis, the labels addition 1). it upon using Fig. membrane compounds); cells plasma related the (see (and plant FM4-64 in features dye traced styryl fluorescent distinct been commonly some has endosomal has Endocytosis the is of pathways organization the cells, trafficking which animal in those components, to similar the EE-specific of structure 2011). of the Helenius, and in (Huotari removal changes endosome morphological by by accompanied LE a al endosomes Early eyrpdyb M-4(ot ta. 04.Teei o strong now is There 2004). labeled al., are et and (Bolte surface, FM4-64 by cell endocytic rapidly the receive very from that internalization compartments first after the cargo as defined are EEs lhuhtegnrlfntoso nooe npatclsare cells plant in endosomes of functions general the Although 4 LPVC ¸a oe l,19;JagadRgr,19;Lee al., et Lee 1998; Rogers, and Jiang 1997; al., et ˜o Vacuole 09.Transport 2009). , ndomembrane that e Rutherford ie for tined ecolored he mponents ivesicular b tal., et aba Journal of Cell Science ypotnA3Ihbt ltrnmdae noyoi Fjmt ta. 00 ri-aae ta. 2006) al., et Ortiz-Zapater 2010; al., et (Fujimoto aggregates endosomal of formation Causes sterols membrane plasma Binds endocytosis -mediated Inhibits Endosidin1 A23 Tyrphostin ATPase Filipin vacuolar Inhibits A Concanamycin otannIhbt PI3K Inhibits Wortmannin niio feto ln el References cells plant on Effect membrane plasma to endosomes from trafficking Blocks A Brefeldin Inhibitor ail fe diino h y,ahlmr fa E Inhibition EE. very an of FM4-64 hallmark with a dye, colocalize the to of the addition shown Surprisingly, after 2006). also rapidly al., was et marker (Dettmer TGN same the endocytosed fluorescent VHA- to subunit and localizes of proton–ATPase a1 vacuolar microscopy delivery the that electron showed for colleagues, labeling, immunogold and site Dettmer using by first proposed who, early initially an the was of This in function is material. as the on organelle and takes separate TGN endosome the a plants, as in existing cells, animal than rather that, evidence niisendocytosis Inhibits degradation vacuolar TGN/EE Prevents of out transport Blocks lcsedctctrafficking endocytic Blocks asselre PVC/MVB enlarged Causes assrdsrbto fGlipoen oER to proteins Golgi compartment) of (BFA redistribution aggregates Causes endosomal of formation Causes al .Eape fihbtr sdt td nooa rfikn nplants in trafficking endosomal study to used inhibitors of Examples 1. Table banduigtesceoycrirmmrn rti 1 protein membrane carrier secretory were results the Similar TGN/EE. the using merged termed pathways often obtained two TGN now secretory these same site, that the this suggesting in at proteins, 2010), found al., be et membrane all al., (Viotti can et polysaccharides (Dettmer plasma and TGN proteins the Endocytosed at cargo of accumulation 2006). endocytic the which and causes 1), trafficking, secretory vesicle (Table both in A block concanamycin a to with leads ATPase vacuolar the of SAP)poenfo ie hc lolclzdt h TGN the to localized also which rice, from protein (SCAMP1) Rbr ta. 2008) al., et (Robert 2006) al., et Kleine-Vehn 2003; al., et (Grebe 1997) al., et Matsuoka 2006; al., et (Dettmer Jili ta. 06 aa ta. 01 asoae l,19;Miao 1995; al., et Matsuoka 2011; al., et Kasai 2006; al., et (Jaillais Glnre l,20;Nebenfu 2003; al., et (Geldner ta. 06 s ta. 04 eme ta. 2006) al., et Vermeer 2004; al., et Tse 2006; al., et oisne l,20b e n or,20;Tee l,2006) al., et Tse 2007; Moore, and Teh 2008b; al., et Robinson tgie l Oeu ta. 2006) al., permission. et with (Otegui from al. reprinted et Figure Otegui nm. 100 (CC). bars: CCVs Scale and (arrows) of aggregates formation protein also the view of top-down visualization This each allows B. for in colors as The are TGN). 2, 2, medial trans 1, 3, medial medial 2, cis cis1, cisternae indicated: top, (from are Golgi bottom to the top of from dissection stack, virtual tomography the electron for 3D allows stack. Golgi the of ( attached TGN. bodies the white to as visible clearly are also MVBs (CCVs). vesicles and a clathrin-coated non-coated as associated well with as TGN stack, distinct Golgi the the of displaying divisions image, three-dimensional visualized a are as A in seen cisternae trans-Golgi lolbld ( are labeled. (MVB) also body multivesicular a and vesicle (NCV) non-coated distinguish A help cisternae. to different used be can techniques labeling Specialized (TGN). trans-Golgi network the and to (trans) from (med) trans-Golgi stack medial-Golgi Golgi to the (cis) of cis-Golgi division the of Take note Golgi . the surrounding of and region complex a through thick) mm slice (4.3 tomographic prepared a of image (TEM) system. ( endomembrane the of regions different distinguish electron to three-dimensional tomography of Use 2. Fig. A nooe npat 3513 plants in Endosomes rnmsineeto microscopy electron Transmission ) h ta. 02 ihe ta. 2007; al., et Richter 2002; al., et ¨hr C B o-ono aeo views face-on or Top-down ) ee i- eil and medial- cis-, Here, ) Journal of Cell Science hs raelsaeo h noyi aha Tee l,2004). al., et (Tse pathway that endocytic labeling, the FM4-64 on the by are by organelles culture, provided these cell was plants tobacco in in LEs demonstration as act would microscopy, recycling electron by 2011). for (Babst, membrane destined outer those limiting the are whereas on internal that remain the LEs, into proteins of concentrated membrane be It vesicles the would that vesicles. degradation of internal predicted for lumen the destined been the in therefore degradation to for has and vacuole membrane with or membrane vacuolar lysosome endosomal or vacuolar external or lysosomal the lysosomal the of the fusion both buds structure by to this endosome membrane membrane Functionally, of the vesicles. in delivery of internal allows structure, membrane produce or multivesicular to limiting secretory plasma LE, a inward external the a the have the into of LEs to which matures compartments EEs, back it Unlike earlier recycled as pathway. to be EE transported might after the possibly It in destinations maintained EE. possible membrane, an several at has arriving material Endocytosed unknown. endosomes Late is 2009) al., et mobile by (Toyooka described these co-workers clusters of and secretory some the Toyooka Whether to 2010). correspond not different rather, structures al., a TGN et with that is (Viotti reassociate dissociate stack even but can TGN and Golgi and Golgi stack, cell associated the the their Golgi within from rapidly 2011). that a move TGNs al., with demonstrated individual et associated has (Ebine by permanently followed imaging ARA6 markers fluorescent with GTPase live-cell TGN and Rab possibly Golgi contents that of the process Tagging its a in releases involves 2009), al., and et also fuses (Toyooka wall it cell the to where into moves membrane, Golgi, plasma the and from the protein separates derived including cluster vesicles cargo, was This secretory of polysaccharides. al., contain cluster which that et a TGN (Toyooka in the FM4- route TGN, found from with endocytic subsequently the labeled the was a on It be was 2009). at could as it also that seen and SCAMP2 indicating 64, Golgi be protein the with secreted could associated by the analyzed SCAMP2 Electron further using marker. was imaging 2011). differentiation not This is live-cell Kang, regions clear. al., and specialized entirely functionally Staehelin to yet early 2011; et relate al., into these et two how differentiated (Gendre 2008); (Kang is these compartments TGN TGN late the of and that the separation indicates not tomography a of but secretory indicating in functions defective trafficking, is that endocytic described to suggesting division. was cell contributes component possibly during an EE that 2008), or TGN Recently, al., organelle the of et an differentiation functional (Chow cytokinesis, label during processes plate they secretory cell the that VHA- at marker found suggesting TGN are the GTPases an unlike as these However, acts a1, 2008). also partially al., TGN that et organelle GTPases same an (Chow Using at Rab-A3 EE the marker and TGN of a Rab-A2 domains with functions. 2000). co-localize separate al., have to et proteins localize distinct (Bassham to marker shown TGN with been microscopy, electron subdomains immunogold specialized al., et on used. (Lam dependent marker points not TGN are time findings the previous early the at that confirming FM4-64 2007), with colocalized and 3514 vdneta Vs hc eeietfe morphologically identified were which MVBs, that Evidence contain might plants in TGN the that exists Evidence ora fCl cec 2 (15) 125 Science Cell of Journal Arabidopsis uatlcigaTGN-localized a lacking mutant noteevsce Hnee l,21) lhuhms fthe of in conserved most are Although animals and 2011). yeast al., in identified et proteins proteins (Henne ESCRT membrane vesicles plasma the these vacuole-destined of into of invagination formed, targeting vesicles the in the in of and release function and membrane that (ESCRT) endosomal -III) limiting transport -II, complexes protein -I, for several (ESCRT-0, of consists required machinery This complex machinery. plasma sorting the 2010). endosomal al., the et to either (Viotti the compartment, RE recycling to separate earlier a that an route or from TGN en and occur are must the degradation from membrane they absent for that are and vacuole indicating MVBs PVC of membrane, proteins a vesicles membrane limiting internal Plasma and 2008). in LE al., found et a are Miao 2007; both an al., not electron et to by but (Haas functionally observed marker, MVBs PVC correspond that a confirming microscopy with marker, colocalize TGN localize or to also shown EE to al., were 2001) et and al., (Ebine MVBs et GTPases Ueda to Rab 2004; vacuole Several al., Mo 2004). et 2008; Ueda al., al., the 2011; et et Miao Tse to 2008; 2006; al., al., trafficking et et Jaillais are vacuolar 2011; biosynthetic they al., that et and in suggesting (Bottanelli vacuole, receptors intermediates the to sorting route also en vacuolar are that contain proteins also MVBs 02 oet ta. 00.Teesrcue r therefore are late the structures termed These compartment, intermediate 2010). an al., be al., contains to et et (Bottanelli which suggested GTPases Foresti small structures, of family these 2012; vacuolar Rab5 soluble in the A of the accumulates members 2010). from al., also distinct et (Foresti is marker is MVB that and receptor compartment TGN a vacuolar-sorting Golgi, in mutant accumulate a to which shown in colleagues, and (Scheuring leads 2011). markers maturation al., MVB their endosome and et TGN of of of disruption colocalization as support increased and TGN to MVBs, In the on on TGN. as distributed found well the are components to from ESCRT correspond model, derived to hypothesized MVBs are they MVBs that immature which MVBs does capture tubules, imaged step al., also to to transport They connected et able this trafficking. that vesicle (Scheuring were involve suggesting study cargo not vacuole, this its the with of release fusing authors to then The which vacuole cargo MVB, 2011). the a moving into with transport matures fuses vesicle TGN the of endosomes, instead between which, in proposed, details), exist. more ESCRT for probably recently 1 the examples Box has (see additional by 2005) conditions and al., et environmental sorted (Takano described to and been response internalized in is complex 2012; in transporter, transport al., BOR1 regulated the boron et protein, of al., plasma-membrane-localized example et Ibl normally An for Shahriari a 2009). 2007; which 2011; al., proteins al., al., et probably et cargo Spitzer et Scheuring 2011; 2011; of proteins (Haas al., sorting et 3) ESCRT Katsiarimpa Fig. and protein the (see maturation of plant degradation LE plants, the basis of in in few the function a in proteins, On mutants of 2011). 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Some signaling the in involve 2008). function that can Robatzek, and receptor repeat (Geldner now rich are plants endosomes in involve at that known several pathways In initiated signaling signaling receptors, are of 2008). membrane-localized for that examples by platforms cascades Robatzek, membrane signaling plasma as and typical the endosomes more Geldner to of 2004; addition role (Geldner, the pathways as receptors, membrane well plasma as of internalization and polarity. and maintenance growth cell plant in for which, essential recycling, is and turn, endocytosis through membrane plasma 3516 nuuulptwyfriiito fsgaighsbeen has signaling of initiation for pathway unusual An noyoi n inln r ikdtruhtene for need the through linked are signaling and Endocytosis ora fCl cec 2 (15) 125 Science Cell of Journal ´ mez-Go ´ e and mez u . u . ag .adCog K. Chong, and Y. Wang, Y., Xu, C., Du, K. Chong, and C. Du, L. C. Jackson, and S. J. Bonifacino, hnkh,P,Aino . wn,I,Rbno,D . rvc . tehf .D. Y. Stierhof, J., Mravec, G., D. Robinson, I., Hwang, F., K. Aniento, Schumacher, P., Dhonukshe, and D. Y. Stierhof, A., Hong-Hermesdorf, J., Dettmer, Conceic Silva da B. Satiat-Jeunemaitre, and D. N. V. Read, O., N. Catrice, Raikhel, Y., Boutte, and C., Talbot, H. S., Zheng, Bolte, V., Kovaleva, A., A. Sanderfoot, C., D. A. Bassham, Avni, and S. Schuster, M., Sharfman, M., Bar, hw .M,Nt,H,Fuat .adMoe I. Moore, and C. Foucart, H., Neto, M., C. Chow, J. Denecke, and C. D. Gershlick, F., Bottanelli, J. Denecke, and S. Hanton, O., Foresti, F., Bottanelli, A. Avni, and M. Bar, as,M. Babst, al o xmls,nwaeuso eerhmgtbe might research of organelles avenues expand. important these greatly of (see new will understanding trafficking our examples), and and the illuminated, for for function available over structure, 1 becoming Table grow are endosomal tools will of new platforms As is analysis years. signaling it few 2010); as the next of the al., endosomes understanding and our et of and (Geldner Kang increase function will plants still 2011; number in Innes, this is that examples and pathways likely of Gu signaling number 2008; in small Robatzek, a endosomes al., et to 2010b; of Robinson limited 2010; role al., al., The for et et Pourcher required 2008a). (Niemes 2008; are plasma Spitzer, al., maturation and that et Otegui the and proteins Richter 2009; of trafficking to al., analysis endosomal et functional endosomes Pan and 2008; 2012) from al., et (Jaillais recycling the and membrane include pathways for will the Wang and of research 2011; characterization components of maturation further al., 2010), avenues and et important clarification and the Future Shahriari al., and 2010). 2010; transport al., al., ESCRT et et in et as (Pourcher involved Viotti such pathways components proteins 2011; endosomal retromer al., of characterization et Scheuring nti . ase,T,Sag,C n olc,B. Hoflack, and C. Stange, T., Wassmer, M., Anitei, Acknowledgements lebc,D n oazk S. Robatzek, and D. Altenbach, Aeronautics References D.C.B. National to the NNX09AK78G] from number grant [grant a Administration Space by and supported was work This Funding 2. Fig. providing for Otegui Marisa thank We atrGPs-ciaigpoensiuae h rnpr fAX nooe which endosome, AUX1 of transport the stimulates protein factor-GTPase-activating are U1eryedsm rfikn orglt ui eedn plant dependent auxin regulate to trafficking endosome early development. AUX1 carrier Arabidopsis. in carriers J. Friml, and plants. in compartment post-Golgi V. N. late Raikhel, and F. 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Vicia K-channel GFP-tagged of and cells membrane plasma guard labelled intact turgor: disorders. otn ei tN2 niisedctctafcigt h vacuole. the to trafficking endocytic inhibits 961-976. AtSNX2b sorting oyECTmciey eeto costeekroi lineage. eukaryotic the across retention machinery; ESCRT body ermrsbope ucin ndvlpetadpoensrigi Arabidopsis in sorting protein and development thaliana. T. in Gaude, functions and retromer-subcomplex Y. Jaillais, C., 1598. A. brefeldin and A23 tyrphostin of effects F. Aniento, receptors. sorting vacuolar with interact Cell may Arabidopsis, in wall and cell G. D. cross-linked Robinson, borate a of function polysaccharide. and pectic structure II: Rhamnogalacturonan boron. of level high a T. requires Fujiwara, and M. Chino, H., ooosra n r7lclz otepeaulrcompartment. prevacuolar the to 45 localize ara7 and rha1 homologs ln aulrsrigreceptor. sorting vacuolar efflux plant auxin C. J. the of Rogers, of regulation accumulation auxin thaliana. in membrane Arabidopsis roles in plasma PIN2 key transporter and play sterols recycling, membrane endocytosis, and SCFTIR1/AFB in ligase starts cells embryo Arabidopsis in bodies. proteins multivesicular storage the seed of processing proteolytic network. P. trans-Golgi Pimpl, the and from G. receptors D. sorting Robinson, S., Hillmer, tutrsa neryedsm ntbcoB- cells. BY-2 tobacco in endosome tubular-vesicular early trans-golgi-located an clathrin-coated, as defines structures SCAMP1 Rice (2007). resistance. disease plant targeting. vacuolar dependent J. Friml, nteER. the P. in Pimpl, and G. D. Robinson, uclua rfikn fteAaiossaxnifu are U1ue novel a uses AUX1 carrier influx PIN1. auxin from Arabidopsis distinct the pathway of trafficking Subcellular localization. their regulates and 23 subunits ESCRT-III with interacts AMSH3 824-839. , 1211-1220. , 3026-3040. , 18 h,A,Rtetae,C n oisn .G. D. Robinson, and C. 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