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• W1900516175 abstract "Over the last 15 years endocytosis has moved from being a process of only minor importance to plant physiologists to being one of the most exciting research areas in plant cell biology. These days, nobody doubts the operation of clathrin-mediated endocytosis as a mechanism for the internalization of a range of physiologically important transmembrane protein complexes at the plasma membrane (PM) of plant cells. These include both receptors and transporters. As in animal cells, most of these proteins are constitutively recycled back to the PM from an early endosome (EE). However, some are destined for degradation and proceed further downstream in the endocytic pathway to late endosomes (LE), where they are internalized into the intraluminal vesicles of the LE. Fusion of the LE with the lysosome/vacuole releases the vesicles leading to their degradation. The signal that marks PM proteins for degradation has been known in mammalian and yeast cells for quite some time and is polyubiquitination (Mukhopadhyay and Riezman, 2007Mukhopadhyay D. Riezman H. Proteasome-independent functions of ubiquitin in endocytosis and signaling.Science. 2007; 315: 201-205Crossref PubMed Scopus (956) Google Scholar). In their Spotlight article, Zelazny and Vert, 2015Zelazny E. Vert G. Regulation of iron uptake by IRT1: endocytosis pulls the trigger.Mol. Plant. 2015; 8: 977-979Abstract Full Text Full Text PDF PubMed Scopus (13) Google Scholar highlight recent publications from the plant field that also demonstrate a key role for multiple monoubiquitination in the endocytosis of the metal transporters IRT1 (Barberon et al., 2011Barberon M. Zelazny E. Robert S. Conejero G. Curie C. Friml J. Vert G. Monoubiquitin-dependent endocytosis of the iron-regulated transporter 1 (IRT1) controls iron uptake in plants.Proc. Natl. Acad. Sci. USA. 2011; 108: E450-E458Crossref PubMed Scopus (332) Google Scholar), BOR1 (Kasai et al., 2011Kasai K. Takano J. Miwa K. Toyoda A. Fujiwara T. High boron-induced ubiquitination regulates vacuolar sorting of the BOR1 borate transporter in Arabidopsis thaliana.J. Biol. Chem. 2011; 286: 6175-6183Crossref PubMed Scopus (154) Google Scholar), as well as lysine63-linked polyubiquitination in vacuolar sorting of the auxin transporter PIN2 (Leitner et al., 2012Leitner J. Petrasek J. Tomanov K. Retzer K. Parezova M. Korbei B. Bachmair A. Zazimalova E. Luschnig C. Lysine63-linked ubiquitylation of PIN2 auxin carrier protein governs hormonally controlled adaptation of Arabidopsis root growth.Proc. Natl. Acad. Sci. USA. 2012; 109: 8322-8327Crossref PubMed Scopus (146) Google Scholar). They also draw attention to the discovery of a ubiquitin-binding protein (FREE1; also termed FYVE1 by Barberon et al., 2014Barberon M. Dubeaux G. Kolb C. Isono E. Zelazny E. Vert G. Polarization of IRON-REGULATED TRANSPORTER 1 (IRT1) to the plant-soil interface plays crucial role in metal homeostasis.Proc. Natl. Acad. Sci. USA. 2014; 111: 8293-8298Crossref PubMed Scopus (173) Google Scholar) which locates to the LE in plant cells and is part of the ESCRT-I (endosomal sorting complex for transport) complex (Gao et al., 2014Gao C. Luo M. Zhao Q. Yang R. Cui Y. Zeng Y. Xia J. Jiang L. A unique plant ESCRT component, FREE1, regulates multivesicular body protein sorting and plant growth.Curr. Biol. 2014; 24: 2556-2563Abstract Full Text Full Text PDF PubMed Scopus (145) Google Scholar). This complex sequesters ubiquitinated membrane cargo proteins and internalizes them. Finally, Zelazny and Vert draw attention to the work of Ivanov et al., 2014Ivanov R. Brumbarova T. Blum A. Jantke A.M. Finke-Straube C. Bauer P. SORTING NEXIN 1 is required for modulating the trafficking and stability of the Arabidopsis IRON-REGULATED TRANSPORTER 1.Plant Cell. 2014; 26: 1294-1307Crossref PubMed Scopus (72) Google Scholar in showing an increase in IRT1 degradation and iron deficiency in SNX1 mutants. So far so good, but Zelazny and Vert go on to conclude that a portion of the internalized IRT1 molecules that reach the LE are recycled back to the EE, a process that they consider to be mediated by sorting nexin 1 (SNX1), a retromer protein. I question the soundness of this scenario. My first line of critique centers on the nature of the IRT1 molecules that are present in the LE and their physiological significance. Both Barberon et al., 2011Barberon M. Zelazny E. Robert S. Conejero G. Curie C. Friml J. Vert G. Monoubiquitin-dependent endocytosis of the iron-regulated transporter 1 (IRT1) controls iron uptake in plants.Proc. Natl. Acad. Sci. USA. 2011; 108: E450-E458Crossref PubMed Scopus (332) Google Scholar and Ivanov et al., 2014Ivanov R. Brumbarova T. Blum A. Jantke A.M. Finke-Straube C. Bauer P. SORTING NEXIN 1 is required for modulating the trafficking and stability of the Arabidopsis IRON-REGULATED TRANSPORTER 1.Plant Cell. 2014; 26: 1294-1307Crossref PubMed Scopus (72) Google Scholar have documented that around 90% of visualizable IRT1 localizes to the EE (in plants the trans Golgi network [TGN]). Its accumulation at this site is a result of rapid endocytosis at the PM and slow recycling to the PM (Barberon et al., 2014Barberon M. Dubeaux G. Kolb C. Isono E. Zelazny E. Vert G. Polarization of IRON-REGULATED TRANSPORTER 1 (IRT1) to the plant-soil interface plays crucial role in metal homeostasis.Proc. Natl. Acad. Sci. USA. 2014; 111: 8293-8298Crossref PubMed Scopus (173) Google Scholar). However, wild-type IRT1 is monoubiquitinated at at least two lysines in the cytosolic loop of this transporter, and gets transported to the vacuole irrespective of the status of iron nutrition. Its detection in the vacuole is only possible when proteolysis is inhibited through concanamycin A treatment (Barberon et al., 2011Barberon M. Zelazny E. Robert S. Conejero G. Curie C. Friml J. Vert G. Monoubiquitin-dependent endocytosis of the iron-regulated transporter 1 (IRT1) controls iron uptake in plants.Proc. Natl. Acad. Sci. USA. 2011; 108: E450-E458Crossref PubMed Scopus (332) Google Scholar). Thus, it would seem that once internalized, IRT1 molecules get caught up in a cycling loop between the EE and PM before being allowed to proceed further downstream to the LE and then the vacuole. The reason for this is not clear. It could be that some of the incoming IRT1 molecules are de-ubiquinated and later reubiquitinated. It could also be, as suggested by Barberon et al., 2011Barberon M. Zelazny E. Robert S. Conejero G. Curie C. Friml J. Vert G. Monoubiquitin-dependent endocytosis of the iron-regulated transporter 1 (IRT1) controls iron uptake in plants.Proc. Natl. Acad. Sci. USA. 2011; 108: E450-E458Crossref PubMed Scopus (332) Google Scholar, that the degree of ubiquitination is a decisive factor, with single monoubiquitination being sufficient for the internalization step at the PM but multiple monoubiquitinations or lysine63-linked polyubiquitination being required for further downstream trafficking. Support for the notion that entry into the late endocytic pathway requires that a certain threshold level of ubiquitination be reached on a membrane protein destined for degradation, comes from the studies of Leitner et al., 2012Leitner J. Petrasek J. Tomanov K. Retzer K. Parezova M. Korbei B. Bachmair A. Zazimalova E. Luschnig C. Lysine63-linked ubiquitylation of PIN2 auxin carrier protein governs hormonally controlled adaptation of Arabidopsis root growth.Proc. Natl. Acad. Sci. USA. 2012; 109: 8322-8327Crossref PubMed Scopus (146) Google Scholar on PIN2 and Martins et al., 2015Martins S. Dohmann E.M. Cayrel A. Johnson A. Fischer W. Pojer F. Satiat-Jeunemaitre B. Jaillais Y. Chory J. Geldner N. et al.Internalization and vacuolar targeting of the brassinosteroid hormone receptor BRI1 are regulated by ubiquitination.Nat. Commun. 2015; 6: 6151Crossref PubMed Scopus (111) Google Scholar on the brassinosteroid hormone receptor BRI1. The former authors compared sorting of a ubiquitination-deficient PIN2-17KR allele with a constitutively endocytosed PIN2-ubiquitin fusion protein and PIN2-17KR-ubiquitin. They noted that PIN2-17KR-ubiquitin, while still being endocytosed, was no longer efficiently targeted to the vacuole. This suggests that extra ubiquitination is necessary for further downstream transport of the reporter protein to the vacuole. In contrast to IRT1, BRI1 is polyubiquitinated with lysine63-linked chains at residue K866 if not at some of the other 29 lysine residues in BRI1 (Martins et al., 2015Martins S. Dohmann E.M. Cayrel A. Johnson A. Fischer W. Pojer F. Satiat-Jeunemaitre B. Jaillais Y. Chory J. Geldner N. et al.Internalization and vacuolar targeting of the brassinosteroid hormone receptor BRI1 are regulated by ubiquitination.Nat. Commun. 2015; 6: 6151Crossref PubMed Scopus (111) Google Scholar). Interestingly, a BRI1 mutant in which 25 of the lysine residues were changed to arginine (essentially a ubiquitin-defective mutant) still retained kinase activity but, unlike the wild-type, the BRI125KR mutant was mostly present at the PM. Nevertheless, after application of brefeldin A (BFA), it was seen to enter BFA bodies, indicating that the ubiquitin-defective mutant could nevertheless be internalized. However, total internal reflection fluorescence microscopy imaging of mCitrine-tagged wild-type BRI1 and the BRI125KR mutant showed that the mutant had a four-fold longer residency period (28 s) at the PM. Moreover, in contrast to the wild-type, BRI125KR-mCitrine was not detectable in the vacuole. These data suggest that while the ubiquitin-defective BRI1 mutant was internalized, it failed to gain access to the late endosomal pathway and instead underwent enhanced recycling to the PM from the EE. Zelazny and Vert draw on the results published by Ivanov et al., 2014Ivanov R. Brumbarova T. Blum A. Jantke A.M. Finke-Straube C. Bauer P. SORTING NEXIN 1 is required for modulating the trafficking and stability of the Arabidopsis IRON-REGULATED TRANSPORTER 1.Plant Cell. 2014; 26: 1294-1307Crossref PubMed Scopus (72) Google Scholar, for their claim that SNX1 mediated the recycling of IRT1 from an LE compartment, but care is needed. Ivanov et al., 2014Ivanov R. Brumbarova T. Blum A. Jantke A.M. Finke-Straube C. Bauer P. SORTING NEXIN 1 is required for modulating the trafficking and stability of the Arabidopsis IRON-REGULATED TRANSPORTER 1.Plant Cell. 2014; 26: 1294-1307Crossref PubMed Scopus (72) Google Scholar state that “…unlike IRT1, SNX1 was mainly localized in ARA7-positive compartments”, and that “…29% of the SNX1-positive compartments had no RFP-ARA7 signal showing that part of the SNX1 population is located in different endosomes…”. Thus, from this paper, one can only say at best that a portion of the IRT1 colocalizes with SNX1, but with which SNX1-positive compartment remains unclear. This situation is due to the use of Rab5 GTPase ARA7 as a marker for the LE. As shown in several papers, while ARA7 labels principally the LE, it has also been detected at the EE (Stierhof and El Kasmi, 2010Stierhof Y.D. El Kasmi F. Strategies to improve the antigenicity, ultrastructure preservation and visibility of trafficking compartments in Arabidopsis tissue.Eur. J. Cell Biol. 2010; 89: 285-297Crossref PubMed Scopus (53) Google Scholar, Scheuring et al., 2011Scheuring D. Viotti C. Kruger F. Kunzl F. Sturm S. Bubeck J. Hillmer S. Frigerio L. Robinson D.G. Pimpl P. et al.Multivesicular bodies mature from the trans-Golgi network/early endosome in Arabidopsis.Plant Cell. 2011; 23: 3463-3481Crossref PubMed Scopus (196) Google Scholar, Singh et al., 2014Singh M.K. Krüger F. Beckmann H. Brumm S. Vermeer J.E.M. Munnik T. Mayer U. Stierhof Y.D. Grefen C. Schumacher K. et al.Protein delivery to vacuole requires SAND protein-dependent Rab GTPase conversion for MVB-vacuole fusion.Curr. Biol. 2014; 24: 1383-13899Abstract Full Text Full Text PDF PubMed Scopus (104) Google Scholar). Since ARA7 is not exclusively a marker for LEs, the conclusion that SNX1 resides at or even recycles IRT1 from LEs is not justified. Although two papers from the Gaude group (Jaillais et al., 2006Jaillais Y. Fobis-Loisy I. Miege C. Rollin C. Gaude T. AtSNX1 defines an endosome for auxin-carrier trafficking in Arabidopsis.Nature. 2006; 443: 106-109Crossref PubMed Scopus (279) Google Scholar, Jaillais et al., 2008Jaillais Y. Fobis-Losy L. Miege C. Gaude T. Evidence for a sorting endosome in Arabidopsis root cells.Plant J. 2008; 53: 237-247Crossref PubMed Scopus (123) Google Scholar) have claimed that SNX1 locates to a prevacuolar/late endosomal compartment (PVC), the validity of these results has been questioned (Robinson et al., 2012Robinson D.G. Pimpl P. Scheuring D. Stierhof Y.-D. Sturm S. Viotti C. Trying to make sense of retromer.Trends Plant Sci. 2012; 17: 431-439Abstract Full Text Full Text PDF PubMed Scopus (43) Google Scholar). Moreover, immunogold electron microscopy, which allows for unequivocal identification of endosomal organelles, has conclusively demonstrated the majority of SNX1 (and SNX2a) at the TGN/EE (Niemes et al., 2010Niemes S. Langhans M. Viotti C. Scheuring D. Yan M.S.W. Jiang L. Hillmer S. Robinson D.G. Pimpl P. Retromer recycles vacuolar sorting receptors from the trans-Golgi network.Plant J. 2010; 61: 107-121Crossref PubMed Scopus (99) Google Scholar, Stierhof et al., 2013Stierhof Y.D. Viotti C. Scheuring D. Sturm S. Robinson D.G. Sorting nexins 1 and 2a locate mainly to the TGN.Protoplasma. 2013; 250: 235-240Crossref PubMed Scopus (30) Google Scholar). A function for SNXs at the TGN/EE remains unclear, but SNX1 mutants do not appear to prevent downstream traffic to the vacuole. This has been seen for both IRT1 and PIN2 (Kleine-Vehn et al., 2008Kleine-Vehn J. Leitner J. Zwiewka M. Sauer M. Abas L. Luschnig C. Friml J. Differential degradation of PIN2 auxin efflux carrier by retromer-dependent vacuolar targeting.Proc. Natl. Acad. Sci. USA. 2008; 105: 17812-17817Crossref PubMed Scopus (310) Google Scholar, Ivanov et al., 2014Ivanov R. Brumbarova T. Blum A. Jantke A.M. Finke-Straube C. Bauer P. SORTING NEXIN 1 is required for modulating the trafficking and stability of the Arabidopsis IRON-REGULATED TRANSPORTER 1.Plant Cell. 2014; 26: 1294-1307Crossref PubMed Scopus (72) Google Scholar). Arabidopsis root cells of SNX1 mutants show reduced levels of both proteins at the PM and their increased degradation in the vacuole. Similarly, the transient expression of SNX1 and SNX2a mutants in tobacco mesophyll protoplasts is without effect on soluble vacuolar protein transport (Niemes et al., 2010Niemes S. Langhans M. Viotti C. Scheuring D. Yan M.S.W. Jiang L. Hillmer S. Robinson D.G. Pimpl P. Retromer recycles vacuolar sorting receptors from the trans-Golgi network.Plant J. 2010; 61: 107-121Crossref PubMed Scopus (99) Google Scholar). These observations seem to suggest that the SNXs are more involved in recycling to the PM than in sorting to the vacuole. Unfortunately, many of the papers in which claims for recycling from the LE of plants (morphologically the multivesicular body) have been made depict the EE (in plants the TGN) and LE as static long-lived organelles. Such a situation is not supported by recent research, which instead points to the continual production and maturation of a LE from the EE (Scheuring et al., 2011Scheuring D. Viotti C. Kruger F. Kunzl F. Sturm S. Bubeck J. Hillmer S. Frigerio L. Robinson D.G. Pimpl P. et al.Multivesicular bodies mature from the trans-Golgi network/early endosome in Arabidopsis.Plant Cell. 2011; 23: 3463-3481Crossref PubMed Scopus (196) Google Scholar, Singh et al., 2014Singh M.K. Krüger F. Beckmann H. Brumm S. Vermeer J.E.M. Munnik T. Mayer U. Stierhof Y.D. Grefen C. Schumacher K. et al.Protein delivery to vacuole requires SAND protein-dependent Rab GTPase conversion for MVB-vacuole fusion.Curr. Biol. 2014; 24: 1383-13899Abstract Full Text Full Text PDF PubMed Scopus (104) Google Scholar). Presumably, protein sorting continues during this process, so that depending on the state of transition, one would find different levels of IRT1 (or other PM proteins that are destined for degradation) and different degrees of colocalization between SNX1 and ARA7. If the plant cell goes to such lengths to ensure that only highly ubiquitinated IRT1, BOR1, BRI1, and PIN2 molecules are allowed to enter the late endocytic pathway, it is difficult to understand why such molecules should be retrieved from LEs. What purpose would they fulfill when re-entering an EE? I feel it is time that the plant community re-defines the LE as a compartment from which there is no recycling. The paper of Jaillais et al., 2008Jaillais Y. Fobis-Losy L. Miege C. Gaude T. Evidence for a sorting endosome in Arabidopsis root cells.Plant J. 2008; 53: 237-247Crossref PubMed Scopus (123) Google Scholar has been seminal in propagating the notion that recycling occurs from the LE. However, their statement that the “The PVC, MVB is a crossroads between the secretory and endocytic pathways in Arabidopsis root cells” is not supported by current opinions which deem the two pathways merging at the TGN/EE (Contento and Bassham, 2012Contento A.L. Bassham D.C. Structure and function of endosomes in plant cells.J. Cell Sci. 2012; 125: 3511-3518Crossref PubMed Scopus (68) Google Scholar). An underlying reason for this confusion lies I think in an inadequate appreciation of what EE and LE are in mammalian versus plant cells. Recycling of the mannosyl-6-P receptor (MPR) from the EE to the TGN in mammalian cells is a consequence of a TGN-based, receptor-mediated sorting mechanism for acid hydrolases, which has now become a paradigm for protein sorting in all textbooks. Retromer-mediated recycling of MPRs may still occur as the EE matures into an LE, but there is no evidence for recycling from the LE in mammalian cells (Bulankina et al., 2009Bulankina A.V. Deggerich A. Wenzel D. Mutenda K. Wittmann J.G. Rudolph M.G. Burger K.N.J. Höning S. TIP47 functions in the biogenesis of lipid droplets.J. Cell Biol. 2009; 185: 641-655Crossref PubMed Scopus (190) Google Scholar). The problem is that, whereas both EE and LE in mammals are multivesiculate structures, in plants only the LE is multivesiculate (hence is called a multivesicular body [MVB]). Plants also have receptors for segregating lytic enzymes from secretory proteins, known as vacuolar sorting receptors (VSRs). However, it is currently a subject of great debate as to where in the plant endomembrane system VSRs connect with and release their ligands. In addition, the localization of plant retromer and the nature of its cargo are also a matter of controversy (for a discussion on these topics see Robinson, 2014Robinson D.G. Trafficking of vacuolar sorting receptors: new data and new problems.Plant Physiol. 2014; 165: 1417-1423Crossref PubMed Scopus (14) Google Scholar). Nevertheless, in this regard I would like to point to the discovery of the so-called late prevacuolar compartment (LPVC). According to Foresti et al., 2010Foresti O. Gerschlick D.C. Bottanelli F. Hummel E. Hawes C. Denecke J. A recycling-defective vacuolar sorting receptor reveals an intermediate compartment situated between prevacuoles and vacuoles in tobacco.Plant Cell. 2010; 22: 3992-4008Crossref PubMed Scopus (68) Google Scholar, this compartment lacks VSRs and is the last endocytic compartment to fuse with the vacuole. Unfortunately, these authors did not provide electron microscopy images of their LPVC, but they are most certainly MVB. The budding of vesicles to the outside of plant MVBs has rarely been captured in electron microscopy (the only known example to my knowledge is Figure 1D in Stierhof et al., 2013Stierhof Y.D. Viotti C. Scheuring D. Sturm S. Robinson D.G. Sorting nexins 1 and 2a locate mainly to the TGN.Protoplasma. 2013; 250: 235-240Crossref PubMed Scopus (30) Google Scholar). From this I infer that if recycling from the late endocytic pathway of plants does occur, it must take place very early in the development of an LE and before completion of the MVB as we recognize it. Therefore, I strongly believe that we should define the LE as being an endocytic compartment irreversibly committed to cargo delivery to the lytic vacuole and from which upstream recycling can no longer occur. No conflict of interest declared." @default.
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• W1900516175 title "Endocytosis: Is There Really a Recycling from Late Endosomes?" @default.
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