Skip to main content
Log in

Adaptor proteins in protein trafficking between endomembrane compartments in plants

  • Review Article
  • Published:
Journal of Plant Biology Aims and scope Submit manuscript

Abstract

Clathrin is a highly conserved coat protein that plays a critical role in lipid vesicle-mediated trafficking at multiple routes in various post-Golgi compartments. It consists of large and small subunits, and exists in the cytosol as triskelions composed of three pairs of small and large subunits. For vesicle formation, the triskelions are recruited to the membrane of specific compartments where they undergo self-polymerization to produce coats for lipid vesicles. However, clathrin has no ability to bind directly to lipid membranes. Therefore, accessory proteins are necessary for its recruitment to the donor compartment where vesicles are formed. A large number of accessory proteins, called adaptor proteins, have been identified and characterized extensively at the molecular and cellular levels in animal cells and yeast. Recently, the roles of many adaptor proteins have been elucidated in plant cells. As expected from the conserved nature of lipidmediated trafficking in eukaryotic cells, these plant adaptor proteins for clathrin show a high degree of functional conservation with those found in animal cells and yeast. At the same time, they are also involved in plant-specific processes such as the transition from the PSV to the lytic vacuole and cell-plate formation. Here, we summarize recent advances in the physiological roles of adaptor proteins in plant cells.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Abas L, Benjamins R, Malenica N, Paciorek T, Wisniewska J, Moulinier-Anzola JC, Sieberer T, Friml J, Luschnig C (2006) Intracellular trafficking and proteolysis of the Arabidopsis auxin-efflux facilitator PIN2 are involved in root gravitropism. Nat Cell Biol 8:249–256

    Article  PubMed  CAS  Google Scholar 

  • Andersson ER (2012) The role of endocytosis in activating and regulating signal transduction. Cell Mol Life Sci 69:1755–1771

    Article  PubMed  CAS  Google Scholar 

  • Aguilar RC, Watson HA, Wendland B (2003) The yeast Epsin Ent1 is recruited to membranes through multiple independent interactions. J Cell Biol 152:531–543

    Google Scholar 

  • Aniento F, Robinson DG (2005) Testing for endocytosis in plants. Protoplasma 226:3–11

    Article  PubMed  CAS  Google Scholar 

  • Bannykh SI, Balch WF (1998) Selective transport of cargo between the endoplasmic reticulum and Golgi compartments. Histochem Cell Biol 109:463–475

    Article  PubMed  CAS  Google Scholar 

  • Bar M, Sharfman M, Schuster S, Avni A (2009a) The coiled-coil domain of EHD2 mediates inhibition of LeEix2 endocytosis and signaling. PLoS ONE 4:e7973

    Article  Google Scholar 

  • Bar M, Avni A (2009b) EHD2 inhibits ligand-induced endocytosis and signaling of the leucine rich repeat receptor-like protein LeEix2. Plant J 59:600–611

    Article  PubMed  CAS  Google Scholar 

  • Barberon M, Zelazny E, Robert S, Conejero G, Curie C, Friml J, Vert G (2011) Monoubiquitin-dependent endocytosis of the IRONREQULATED TRANSPORTER 1(IRT1) transporter controls iron uptake in plants. Proc Natl Acad Sci USA 108:12985–12986

    Article  CAS  Google Scholar 

  • Barlowe C, Orici L, Yeong T, Hosobuchi M, Hamamoto S, Salama N, Rexach MF, Ravaxxola M, Amherdt M, Schekman R (1994) COPII: A membrane coat formed by sec proteins that drives vesicle budding form the endoplasmic reticulum. Cell 77:895–907

    Article  PubMed  CAS  Google Scholar 

  • Barth M, Holstein SE (2004) Identification and functional characterization of Arabidopsis AP180, a binding partner of plant aC-adaptin. J Cell Sci 117:2051–2062

    Article  PubMed  CAS  Google Scholar 

  • Bashline L, Li S, Anderson C.T, Lei L, Gu Y (2013) The endocytosis of cellulose synthase in Arabidopsis is dependent on µ2, a clathrin-mediated endocytosis adaptin. Plant Physiol 163:150–160

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Bassham DC, Brandizzi F, Otegui MS, Sanderfoot AA (2008) The secretion system of Arabidopsis. The Arabidopsis book 6:e0116

    Article  Google Scholar 

  • Boehm M, Bonifacino JS (2001) Adaptins: the final recount. Mol Biol Cell 12:2907–2920

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Bonifacino JS, Dell’Angelica EC (1999) Molecular bases for the recognition of tyrosine-based sorting signals. J Cell Biol 145:923–926

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Bonifacino JS, Lippincott-Schwartz J (2003a) Coat proteins: shaping membrane transport. Mol Cell Biol 4:409–414

    CAS  Google Scholar 

  • Bonifacino JS, Traub LM (2003b) Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu Rev Biochem 72:395–447

    Article  PubMed  CAS  Google Scholar 

  • Brodsky FM, Chen CY, Knuehl C, Towler MC, Wakeham DE (2001) Biological basket weaving: formation and function of clathrincoated vesicles. Annu Rev Cell Dev Biol 17:517–568

    Article  PubMed  CAS  Google Scholar 

  • Chen H, Fre S, Slepnev VI, Capua MR, Takei K, Butler MH, Di Fiore PP, De Camilli P (1998) Epsin is an EH-domain-binding protein implicated in clathrin-mediated endocytosis. Nature 394:793–797

    Article  PubMed  CAS  Google Scholar 

  • Chen X, Irani NG, Friml J (2011) Clathrin-mediated endocytosis: the gateway into plant cells. Curr Opin in Plant Biol 14:674–682

    Article  CAS  Google Scholar 

  • Chidambaram S, Mullers N, Wiederhold K, Haucke V, von Mollard GF (2004) Specific interaction between SNAREs and Epsin Nterminal homology (ENTH) domains of epsin-related proteins in trans-Golgi network to endosome transport. J Biol Chem 279:4175–4179

    Article  PubMed  CAS  Google Scholar 

  • Collins BM, McCoy AJ, Kent HM, Evans PR, Owen DJ (2002) Molecular architecture and functional model of the endocytic AP2 complex. Cell 109:523–535

    Article  PubMed  CAS  Google Scholar 

  • DaSilva LP, Foresti O, Denecke J (2006) Targeting of the plant vacuolar sorting receptor BP80 is dependent on multiple sorting signals in the cytosolic tail. Plant Cell 18:1477–1497

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Dell’Angelica EC, Puertollano R, Mullins C, Aguilar RC, Vargas JD, Hartnell LM, Bonifacino JS (2000) GGAs: a family of ADP ribosylation factor-binding proteins related to adaptors and associated with the Golgi complex. J Cell Biol 149:81–83

    Article  PubMed  PubMed Central  Google Scholar 

  • Dhonukshe P, Aniento F, Hwang I, Robinson DG, Mravec J, Stierhof YD, Friml J (2007) Clatrin-mediated constitutive endocytosis of PIN auxin efflux carriers in Arabidopsis. Curr Biol 17:520–527

    Article  PubMed  CAS  Google Scholar 

  • Fan L, Hao H, Xue Y, Zhang L, Song K, Ding Z, Botella MA, Wang H, Lin J (2013) Dynamic analysis of Arabidopsis AP2 s subunit reveals a key role in clathrin-mediated endocytosis and plant development. Development 140:3826–3837

    Article  PubMed  CAS  Google Scholar 

  • Feraru E, Paciorek T, Feraru MI, Zwiewka M, De Groodt R, De Rycke R, Kleine-Vehn J, Friml J (2010) The AP-3 β adaptin mediates the biogenesis and function of lytic vacuoles in Arabidopsis. Plant Cell 22:2812–2824

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Fischer JA, Eun SH, Doolan BT (2006) Endocytosis, endosome trafficking, and the regulation of Drosophila development. Annu Rev Cell Dev Biol 22:181–206

    Article  PubMed  CAS  Google Scholar 

  • Freidit Frey N, Robatzek S (2009) Trafficking vesicles: pro or contra pathogens? Curr Opin Plant Biol 12:P437–443

    Article  CAS  Google Scholar 

  • Goodman OB, Keen JH (1995) The a chain of the AP-2 adaptor is a clathrin binding subunit. J Biol Chem 270:23768–23773

    Article  PubMed  CAS  Google Scholar 

  • Happel N, Höning S, Neuhaus J.M, Paris N, Robinson DG, Holstein SE (2004) Arabidopsis µA-adaptin interacts with the tyrosine motif of the vacuolar sorting receptor VSR-PS1. Plant J 37:678–693

    Article  PubMed  CAS  Google Scholar 

  • Hawes CR, Brandizzi F, Andreeva AV (1999) Endomembranes and vesicle trafficking. Curr Opin in Plant Biol 2:451–461

    Article  Google Scholar 

  • Hinners I, Tooze SA (2003) Changing directions: clathrin-mediated transport between the Golgi and endosomes. J Cell Sci 116:763–771

    Article  PubMed  CAS  Google Scholar 

  • Hirst J, Robinson MS (1998) Clathrin and adaptors. Biochim Biophys Acta 1401:173–193

    Article  Google Scholar 

  • Hirst J, Lui WW, Bright NA, Totty N, Seaman MN, Robinson MS (2000) A family of proteins with ?-adaptin and VHS domains that facilitate trafficking between the TGN and the vacuole/lysosome. J Cell Biol 149:81–93

    Article  Google Scholar 

  • Hirst J, Barlow LD, Francisco GC, Sahlender DA, Seaman MN, Dacks JB, Robinson MS (2011) The fifth adaptor protein complex. PLoS Biol 9:e1001170

    Article  Google Scholar 

  • Hirst J, Irving C, Borner GH (2013) Adaptor protein complexes AP-4 and AP-5: new players in endosomal trafficking and progressive spastic paraplegia. Traffic 14:153–164

    Article  PubMed  CAS  Google Scholar 

  • Holstein SE (2002) Clathrin and plant endocytosis. Traffic 3:614–620

    Article  PubMed  CAS  Google Scholar 

  • Holstein SE, Oliviusson P (2005) Sequence analysis of Arabidopsis thaliana E/ANTH-domain-containing proteins: membrane tethers of the clathrin-dependent vesicle budding machinery. Protoplasma 226:13–21

    Article  PubMed  CAS  Google Scholar 

  • Hwang I, Robinson DG (2009) Transport vesicle formation in plant cells. Curr Opin Plant Biol 12:660–669

    Article  PubMed  CAS  Google Scholar 

  • Jackson T (1998) Transport vesicles: Coats of many colours. Curr Biol 8:R609–R612

    Article  PubMed  CAS  Google Scholar 

  • Kalthoff C, Groos S, Kohl R, Mahrhold S, Ungewickell EJ (2002) Clint: a novel clathrin-binding ENTH-domain protein at the Golgi. Mol Biol Cell 13:4060–4076

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kasai K, Takano K, Miwa K, Toyoya A, Fujiwara T (2011) High boron-induced ubiquitination regulates vacuolar sorting of the BOR1 borate transporter in Arabidopsis thaliana. J Biol Chem 286:6175–6183

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kim H, Park M, Kim SJ, Hwang I (2005) Actin filaments play a critical role in vacuolar trafficking at the Golgi complex in plant cells. Plant Cell 17:888–902

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kim H, Kang H, Jang M, Chang JH, Miao Y, Jiang L, Hwang I (2010) Homomeric interaction of AtVSR1 is essential for its function as a vacuolar sorting receptor. Plant Physiol 154:134–148

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kim SY, Xu Z-I, Song K, Kim DH, Kang HJ, Reichardt I, Sohn EJ, Friml J, Juergens G, Hwang I (2013) Adaptor protein complex 2-mediated endocytosis is crucial for male reproductive organ development in Arabidopsis. Plant Cell 25:2970–2985

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kirchhausen T, Bonifacino JS, Riezman H (1997) Linking cargo to vesicle formation: receptor tail interactions with coat proteins. Curr Opin Cell Biol 9:488–495

    Article  PubMed  CAS  Google Scholar 

  • ai]Kirchhausen T (2000) Three ways to make a vesicle. Nate Rev Mol Cell Biol 1:187–198

    Article  Google Scholar 

  • ai]Kitakura S, Vanneste S, Robert S, Lofke C, Teichmann T, Tanaka H, Friml J (2011) Clathrin mediates endocytosis and polar distribution of PIN auxin transporters in Arabidopsis. Plant Cell 23:1920–1931

    Article  Google Scholar 

  • ai]Lee G-J, Sohn EJ, Lee MH, Hwang I (2004) The Arabidopsis Rab5 homologs Rha1 and Ara7 localize to the prevacuolar compartment. Plant Cell Physiol 45:1211–1220

    Article  Google Scholar 

  • ai]Lee GJ, Kim H, Kang H, Jang M, Lee DW, Lee S, Hwang I (2007) EpsinR2 interacts with clathrin, Adaptor protin-3, AtVTI12, and phosphatidylinositol-3-phosphate. Implications for EpsinR2 function in protein trafficking in plants cells. Plant Physiol 143:1561–1575

    Google Scholar 

  • Lee HK, Cho SK, Son O, Xu Z, Hwang I, Kim WT (2009) Drought stress-induced RamH1, a RING membrane-anchor E3 ubiquitin ligase homolog, regulates aquaporin levels via ubiquitination in transgenic Arabidopsis plants. Plant Cell 21:622–641

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Legendre-Guillemin V, Wasiak S, Hussain NK, Angers A, McPherson PS (2004) ENTH/ANTH proteins and clathrin-mediated membrane budding. J Cell Sci 117:9–18

    Article  PubMed  CAS  Google Scholar 

  • Lu D, Lin W, Gao X, Wu S, Cheng C, Avila J, Heese A, Devarenne TP, He P, Shan L (2011) Direct ubiquitination of pattern recognition receptor FLS2 attenuates plant innate immunity. Science 332:1439–1442

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Mao YX, Chen J, Maynard JA, Zhang B, Quiocho FA (2001) A novel all helix fold of the AP180 amino-terminal domain for phosphoinositide binding and clathrin assembly in synaptic vesicle endocytosis. Cell 104:433–440

    Article  PubMed  CAS  Google Scholar 

  • McMahon HT, Mills IG (2004) COP and clathrin-coated vesicle budding: different pathways, common approaches. Curr Opin Cell Biol 16:379–391

    Article  PubMed  CAS  Google Scholar 

  • McMahon HT, Boucrot E (2011) Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat Rev Mol Cell 12:517–533

    Article  CAS  Google Scholar 

  • Morgan JR, Prasad K, Hao W, Augustine GJ, Lafer EM (2000) A conserved clathrin assembly motif essential for synaptic vesicle endocytosis. J Neurosci 20:8667–8676

    PubMed  CAS  Google Scholar 

  • Niihama M, Takemoto N, Hashiguchi Y, Tasaka M, Morita MT (2009) ZIP genes encode proteins involved in membrane trafficking of the TGN-PVC/vacuoles. Plant Cell Physiol 50:2057–2068

    Article  PubMed  CAS  Google Scholar 

  • Ninoles R, Rubio L, Garca-Snchez MJ, Fern ndez JA, Bueso E, Alejandro S, Serrano R (2013) A dominant-negative form of Arabidopsis AP-3 β-adaptin improves intracellular pH homeostasis. Plant J 74:557–568

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Owen DJ, Vallis Y, Pearse BM, McMahon HT, Evans PR (2000) The structure and function of the ß2-adaptin appendage domain. EMBO J 19:4216–4227

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • ai]Paolini L, Radeghien A, Civini S, Caimi L, Ricotta D (2011) The epsilon hinge-ear region regulates membrane localization of the AP-4 complex. Traffic 12:1604–1619

    Article  Google Scholar 

  • Park M, Song K, Reichardt I, Kim H, Mayer U, Stierhof Y-D, Hwang I, Jurgens G (2013) Arabidopsis m-adaptin subunit AP1M of adaptor protein complex 1 mediates late secretory and vacuolar traffic and is required for growth. Proc Natl Acad Sci 110:10318–10323

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Robinson MS (1994) The role of clathrin, adaptors and dynamin in endocytosis. Curr Opin Cell Biol 6:538–544

    Article  PubMed  CAS  Google Scholar 

  • Robinson DG, Pimpl P (2014) Clathrin and post-Golgi trafficking: a very complicated issue. Trends Plant Sci 19:134–139

    Article  PubMed  CAS  Google Scholar 

  • Rothman JE, Wieand FT (1996) Protein sorting by transport vesicles. Science 272:227–234

    Article  PubMed  CAS  Google Scholar 

  • Rubbo SD, Irani NG, Kim SY, Xu ZY, Gadeyne A, Dejonghe W, Banhoutte I, Persiau G, Eeckhout D, Simon S, Song K, Kleine-Vehn J, Friml J, Jaeger GD, Damme DV, Hwang I, Russinova E (2013) The clathrin adaptor complex AP-2 mediates endocytosis of Brassinosteroid insensitive1 in Arabidopsis. Plant Cell 25:2986–2997

    Article  PubMed  PubMed Central  Google Scholar 

  • Sanmartin M, Ordones A, Sohn EJ, Robert S, Sanchez-Serrano JJ, Surpin MA, Raikhel NV, Rojo E (2007) Divergent functions of VTI12 and VTI11 in trafficking to storage and lytic vacuoles in Arabidopsis. Proc Natl Acad Sci USA 104:3645–3650

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Schekman R, Orci L (1996) Coat proteins and vesicle budding. Science 271:1526–1533

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Shiba T, Kawasaki M, Takatsu H, Nogi T, Matsugaki N, Igarashi N, Suzuki M, Kato R, Nakayama K, Wakatsuki S (2003) Molecular mechanism of membrane recruitment of GGA by ARF in lysosomal protein transport. Nat Struct Biol 10:386–393

    Article  PubMed  CAS  Google Scholar 

  • Simmen T, Honing S, Icking A, Tikkanen R, Hunziker W (2002) AP-4 binds baolateral signals and participates in basolateral sorting epithelial MDCK cells. Nat Cell Biol 4:154–159

    Article  PubMed  CAS  Google Scholar 

  • Simpson F, Bright NA, West MA, Newman LS, Darnell RB, Robinson MS (1996) A novel adaptor-related protein complex. J Cell Biol 133:749–760

    Article  PubMed  CAS  Google Scholar 

  • Sohn EJ, Rojas-Pierce M, Pan S, Carter C, Serrano-Mislata A, Madueno F, Rojo E, Surpin M, Raikhel NV (2007) The shoot meristem identity gene TFL1 is involved in flower development a trafficking to the protein storage vacuole. Proc Natl Acad Sci USA 104:18801–18806

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Song J, Lee MH, Lee GJ, Yoo CM, Hwang I (2006) Arabidopsis EPSIN1 plays an important role in vacuolar trafficking of soluble cargo proteins in plant cells via interaction with clathrin, AP-1, VTI11, and VSR1. Plant Cell 18:2258–2274

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Song K, Jang M, Kim SY, Lee G, Lee G-J, Kim DH, Lee Y, Cho W, Hwang I (2012) An A/ENTH domain-containing protein functions as an adaptor for clathrin-coated vesicles on the growing cell plate in Arabidopsis root cells. Plant Physiol 159:1013–1025

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Stoorvogel, W, Oorschot V, Geuze HJ (1996) A novel class of clathrincoated vesicles budding from endosomes. J Cell Biol 132:21–33

    Article  PubMed  CAS  Google Scholar 

  • Surpin M, Zheng H, Morita MT, Saito C, Avila E, Blakeslee JJ, Bandopadhyay A, Kovaleva, V, Carter D, Murphy A, Taasaka M, Rakhel N (2003) The VTI family of SNARE proteins is necessary for plant viability and mediates different protein transport pathways. Plant Cell 15:2885–2899

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Takano J, Tanaka M, Toyoda A, Miwa K, Kasai K, Fuji K, Onouchi H, Naito S, Fujiwara T (2010) Polar localization and degradation of Arabidopsis boron transporters through distinct trafficking pathways. Proc Natl Acad Sci USA 107:5220–5225

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Teh O-K, Shimono Y, Shirakawa M, Fukao Y, Tamura K, Shimada T, Hara-Nishimura I (2013) The AP-1 µ adaptin is required for KNOLLE localization at the cell plate to mediate cytokinesis in Arabidopsis. Plant Cell Physiol 54:838–847

    Article  PubMed  CAS  Google Scholar 

  • Van Damme D, Gadeyne A, Vanstraelen M, Inze D, Van Montagu MC, De Jaeger G, Russinova E, Geelen D (2011) Adaptin-like protein TPLATE and clathrin recruitment during plant somatic cytokinesis occurs via two distinct pathways. Proc Natl Acad Sci USA 108:615–620

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang J-G, Li S, Zhao X-Y, Zhou L-Z, Huang G-Q, Feng C, Zhang Y (2013) HAPLESS13, the Arabidopsis µ1 adaptin, is essential for protein sorting at the trans-Golgi network/early Endosome. Plant Physiol 162:1897–1910

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Yamaoka S, Shimono Y, Shirakawa M, Fukao Y, Kawase T, Hatsugai N, Tamura K, Shimada T, Hara-Nishimura I (2013) Identification and dynamics of Arabidopsis adaptor protien-2 complex and its involvement in floral organ development. Plant Cell 25:2958–2969

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Zhu Y, Drake MT, Kornfeld S (2001) Adaptor protein 1-dependent clathrin coat assembly on synthetic liposomes and Golgi membranes. Methods Enzymol 329:379–387

    Article  PubMed  CAS  Google Scholar 

  • Zwiewka M, Feraru E, Moller B, Hwang I, Feraru M, Kleine-Vehn J, Weijers D, Friml J (2011) The AP-3 adaptor complex is required for vacuolar function in Arabidopsis. Cell Res 21:1711–1722

    Article  PubMed  CAS  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Inhwan Hwang.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lee, M.H., Hwang, I. Adaptor proteins in protein trafficking between endomembrane compartments in plants. J. Plant Biol. 57, 265–273 (2014). https://doi.org/10.1007/s12374-014-0314-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12374-014-0314-8

Keywords

Navigation