Unconventional protein secretion (UPS) pathways in plants

Current Opinion in Cell Biology

Volumn 29, Issue 1, 2014, Pages 107-115

  Ding, Yu ^a   Robinson, David G ^b   Jiang, Liwen ^a  

^a CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^b UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; BREFELDIN A; CONCANAMYCIN A; EXOCYST; HYGROMYCIN; MEMBRANE PROTEIN; METHIONINE ADENOSYLTRANSFERASE; PROTEIN; SALICYLIC ACID;

ARABIDOPSIS; AUTOPHAGOSOME; AUTOPHAGY; BARLEY; CELL VACUOLE; ENZYME ACTIVE SITE; EXOSOME; HELIANTHUS ANNUUS; HUMAN; MEMBRANE FUSION; MULTIVESICULAR BODY; NONHUMAN; PLANT; PLANT CELL; POLLEN TUBE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN SECRETION; REVIEW; SECRETORY PATHWAY; UNCONVENTIONAL PROTEIN SECRETION;

ANIMALS; EXOCYTOSIS; GOLGI APPARATUS; HUMANS; PLANT PROTEINS; PLANTS; PROTEIN TRANSPORT; SECRETORY PATHWAY;

EID: 84902489866     PISSN: 09550674     EISSN: 18790410     Source Type: Journal    
DOI: 10.1016/j.ceb.2014.05.008     Document Type: Review

References (74)

1. Burgess T.L., Kelly R.B. Constitutive and regulated secretion of proteins. Annu Rev Cell Biol 1987, 3:243-293.
2. Drakakaki G., Dandekar A. Protein secretion: how many secretory routes does a plant cell have?. Plant Sci 2013, 203-204:74-78.
3. Nickel W., Rabouille C. Mechanisms of regulated unconventional protein secretion. Nat Rev Mol Cell Biol 2009, 10:234.
4. Zhang M., Schekman R. Cell biology. Unconventional secretion, unconventional solutions. Science 2013, 340:559-561.
5. Malhotra V. Unconventional protein secretion: an evolving mechanism. EMBO J 2013, 32:1660-1664.
6. Rabouille C., Malhotra V., Nickel W. Diversity in unconventional protein secretion. J Cell Sci 2012, 125:5251-5255.
7. Ding Y., Wang J., Wang J., Stierhof Y.D., Robinson D.G., Jiang L. Unconventional protein secretion. Trends Plant Sci 2012, 17:606-615.
8. Manjithaya R., Subramani S. Autophagy: a broad role in unconventional protein secretion?. Trends Cell Biol 2011, 21:67-73.
9. Grieve A., Rabouille C. Golgi bypass: skirting around the heart of classical secretion. Cold Spring Harb Perspect Biol 2011, 3:a005298.
10. Krause C., Richter S., Knöll C., Jürgens G. Plant secretome - from cellular process to biological activity. Biochim Biophys Acta 2013, 1834:2429-2441.
11. Alexandersson E., Ali A., Resjö S., Andreasson E. Plant secretome proteomics. Front Plant Sci 2013, 4:9.
12. Kim S.J., Brandizzi F. The plant secretory pathway: an essential factory for building plant cell walls. Plant Cell Physiol 2014, 55:687-693.
13. Irene K., Stefan H., Gotthard K., Klaus M. Brefeldin A differentially affects protein secretion from suspension-cultured tobacco cells (Nicotiana tabacum L.). J Plant Physiol 1995, 146:71-80.
14. Kunze I., Kunze G., Ramm S., Horstmann C., Manteuffel R., Müntz K. Two polypeptides that are secreted from suspension-cultured tobacco cells in the presence of Brefeldin A have chitin-binding domains. J Plant Physiol 1995, 147:63-70.
15. Agrawal G., Jwa N.S., Lebrun M.H., Job D., Rakwal R. Plant secretome: unlocking secrets of the secreted proteins. Proteomics 2010, 10:799-827.
16. Zhang H., Zhang L., Gao B., Fan H., Jin J., Botella M., Jiang L., Lin J. Golgi apparatus-localized synaptotagmin 2 is required for unconventional secretion in Arabidopsis. PLoS ONE 2011, 6:e26477.
17. Cheng F., Zamski E., Guo W., Pharr D., Williamson J. Salicylic acid stimulates secretion of the normally symplastic enzyme mannitol dehydrogenase: a possible defense against mannitol-secreting fungal pathogens. Planta 2009, 230:1093-1103.
18. Hara-Nishimura I., Hatsugai N. The role of vacuole in plant cell death. Cell Death Differ 2011, 18:1298-1304.
19. Hatsugai N., Iwasaki S., Tamura K., Kondo M., Fuji K., Ogasawara K., Nishimura M., Hara-Nishimura I. A novel membrane fusion-mediated plant immunity against bacterial pathogens. Genes Dev 2009, 23:2496-2506.
20. Nielsen M.E., Thordal-Christensen H. Transcytosis shuts the door for an unwanted guest. Trends Plant Sci 2013, 18:611-616.
21. Nielsen M.E., Feechan A., Bohlenius H., Ueda T., Thordal-Christensen H. Arabidopsis ARF-GTP exchange factor, GNOM, mediates transport required for innate immunity and focal accumulation of syntaxin PEN1. Proc Natl Acad Sci U S A 2012, 109:11443-11448.
22. Lu Y., Schornack S., Spallek T., Geldner N., Chory J., Schellmann S., Schumacher K., Kamoun S., Robatzek S. Patterns of plant subcellular responses to successful oomycete infections reveal differences in host cell reprogramming and endocytic trafficking. Cell Microbiol 2012, 14:682-697.
23. Huckelhoven R., Panstruga R. Cell biology of the plant-powdery mildew interaction. Curr Opin Plant Biol 2011, 14:738-746.
24. Bednarek P., Kwon C., Schulze-Lefert P. Not a peripheral issue: secretion in plant-microbe interactions. Curr Opin Plant Biol 2010, 13:378-387.
25. Meyer D., Pajonk S., Micali C., O'Connell R., Schulze-Lefert P. Extracellular transport and integration of plant secretory proteins into pathogen-induced cell wall compartments. Plant J 2009, 57:986-999.
26. An Q., Ehlers K., Kogel K.-H., Van Bel A.J.E., Hückelhoven R. Multivesicular compartments proliferate in susceptible and resistant MLA12-barley leaves in response to infection by the biotrophic powdery mildew fungus. New Phytol 2006, 172:563-576.
27. An Q., Huckelhoven R., Kogel K.H., Van Bel A.J.E. Multivesicular bodies participate in a cell wall-associated defence response in barley leaves attacked by the pathogenic powdery mildew fungus. Cell Microbiol 2006, 8:1009-1019.
28. Pinedo M., Regente M., Elizalde M., Quiroga I.Y., Pagnussat L.A., Jorrin-Novo J., Maldonado A., de la Canal L. Extracellular sunflower proteins: evidence on non-classical secretion of a jacalin-related lectin. Protein Pept Lett 2012, 19:270-276.
29. Regente M., Corti-Monzon G., Maldonado A.M., Pinedo M., Jorrin J., de la Canal L. Vesicular fractions of sunflower apoplastic fluids are associated with potential exosome marker proteins. FEBS Lett 2009, 583:3363-3366.
30. Teh O.K., Hofius D. Membrane trafficking and autophagy in pathogen-triggered cell death and immunity. J Exp Bot 2014, 65:1297-1312.
31. Prado N., Alché J.d.D., Casado-Vela J., Mas S., Villalba M., Rodríguez R., Batanero E. Nanovesicles are secreted during pollen germination and pollen tube growth: a possible role in fertilization. Mol Plant 2014, 7:573-577.
32. Safavian D., Goring D.R. Secretory activity is rapidly induced in stigmatic papillae by compatible pollen, but inhibited for self-incompatible pollen in the Brassicaceae. PLOS ONE 2013, 8:e84286.
33. Ding Y., Wang J., Chun Lai J.H., Ling Chan V.H., Wang X., Cai Y., Tan X., Bao Y., Xia J., Robinson D.G., et al. Exo70E2 is essential for exocyst subunit recruitment and for EXPO formation in both plants and animals. Mol Biol Cell 2014, 25:412-426.
34. Wang J., Ding Y., Wang J., Hillmer S., Miao Y., Lo S.W., Wang X., Robinson D.G., Jiang L. EXPO, an exocyst-positive organelle distinct from multivesicular endosomes and autophagosomes, mediates cytosol to cell wall exocytosis in Arabidopsis and tobacco cells. Plant Cell 2010, 22:4009-4030.
35. Tse Y.C., Mo B., Hillmer S., Zhao M., Lo S.W., Robinson D.G., Jiang L. Identification of multivesicular bodies as prevacuolar compartments in Nicotiana tabacum BY-2 cells. Plant Cell 2004, 16:672-693.
36. Lam S.K., Siu C.L., Hillmer S., Jang S., An G.H., Robinson D.G., Jiang L. Rice SCAMP1 defines clathrin-coated, trans-Golgi-located tubular-vesicular structures as an early endosome in tobacco BY-2 cells. Plant Cell 2007, 19:296-319.
37. Lazniewska J., Macioszek V.K., Kononowicz A.K. Plant-fungus interface: the role of surface structures in plant resistance and susceptibility to pathogenic fungi. Physiol Mol Plant Pathol 2012, 78:24-30.
38. Hoefle C., Huckelhoven R. Enemy at the gates: traffic at the plant cell pathogen interface. Cell Microbiol 2008, 10:2400-2407.
39. Wang W., Wen Y., Berkey R., Xiao S. Specific targeting of the Arabidopsis resistance protein RPW8.2 to the interfacial membrane encasing the fungal haustorium renders broad-spectrum resistance to powdery mildew. Plant Cell 2009, 21:2898-2913.
40. Kwaaitaal M., Keinath N.F., Pajonk S., Biskup C., Panstruga R. Combined bimolecular fluorescence complementation and Forster resonance energy transfer reveals ternary SNARE complex formation in living plant cells. Plant Physiol 2010, 152:1135-1147.
41. Bohlenius H., Morch S.M., Godfrey D., Nielsen M.E., Thordal-Christensen H. The multivesicular body-localized GTPase ARFA1b/1c is important for callose deposition and ROR2 syntaxin-dependent preinvasive basal defense in barley. Plant Cell 2010, 22:3831-3844.
42. Bhat R.A., Miklis M., Schmelzer E., Schulze-Lefert P., Panstruga R. Recruitment and interaction dynamics of plant penetration resistance components in a plasma membrane microdomain. Proc Natl Acad Sci U S A 2005, 102:3135-3140.
43. Fujimoto M., Ueda T. Conserved and plant-unique mechanisms regulating plant post-Golgi traffic. Front Plant Sci 2012, 3:197.
44. Ebine K., Fujimoto M., Okatani Y., Nishiyama T., Goh T., Ito E., Dainobu T., Nishitani A., Uemura T., Sato M.H., et al. A membrane trafficking pathway regulated by the plant-specific RAB GTPase ARA6. Nat Cell Biol 2011, 13. 853-U279.
45. Raposo G., Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol 2013, 200:373-383.
46. Wang H., Zhuang X., Hillmer S., Robinson D.G., Jiang L. Vacuolar sorting receptor (VSR) proteins reach the plasma membrane in germinating pollen tubes. Mol Plant 2011, 4:845-853.
47. TerBush D.R., Maurice T., Roth D., Novick P. The Exocyst is a multiprotein complex required for exocytosis in Saccharomyces cerevisiae. EMBO J 1996, 15:6483-6494.
48. Hsu S.C., Ting A.E., Hazuka C.D., Davanger S., Kenny J.W., Kee Y., Scheller R.H. The mammalian brain rsec6/8 complex. Neuron 1996, 17:1209-1219.
49. Elias M., Drdova E., Ziak D., Bavlnka B., Hala M., Cvrckova F., Soukupova H., Zarsky V. The exocyst complex in plants. Cell Biol Int 2003, 27:199-201.
50. Heider M., Munson M. Exorcising the exocyst complex. Traffic 2012, 13:898-907.
51. Synek L., Schlager N., Elias M., Quentin M., Hauser M.T., Zarsky V. AtEXO70A1, a member of a family of putative exocyst subunits specifically expanded in land plants, is important for polar growth and plant development. Plant J 2006, 48:54-72.
52. Cvrčková F., Grunt M., Bezvoda R., Hála M., Kulich I., Rawat A., Zárský V. Evolution of the land plant exocyst complexes. Front Plant Sci 2012, 3:159.
53. Zarsky V., Kulich I., Fendrych M., Pecenkova T. Exocyst complexes multiple functions in plant cells secretory pathways. Curr Opin Plant Biol 2013, 16:726-733.
54. Fendrych M., Synek L., Pecenkova T., Drdova E.J., Sekeres J., de Rycke R., Nowack M.K., Zarsky V. Visualization of the exocyst complex dynamics at the plasma membrane of Arabidopsis thaliana. Mol Biol Cell 2013, 24:510-520.
55. Hala M., Cole R., Synek L., Drdova E., Pecenkova T., Nordheim A., Lamkemeyer T., Madlung J., Hochholdinger F., Fowler J.E., et al. An exocyst complex functions in plant cell growth in Arabidopsis and tobacco. Plant Cell 2008, 20:1330-1345.
56. Zhang Y., Immink R., Liu C.M., Emons A.M., Ketelaar T. The Arabidopsis exocyst subunit SEC3A is essential for embryo development and accumulates in transient puncta at the plasma membrane. New Phytol 2013, 199:74-88.
57. Wu J., Tan X., Wu C., Cao K., Li Y., Bao Y. Regulation of cytokinesis by exocyst subunit SEC6 and KEULE in Arabidopsis thaliana. Mol Plant 2013, 6:1863-1876.
58. Drdova E.J., Synek L., Pecenkova T., Hala M., Kulich I., Fowler J.E., Murphy A.S., Zarsky V. The exocyst complex contributes to PIN auxin efflux carrier recycling and polar auxin transport in Arabidopsis. Plant J 2013, 73:709-719.
59. Kulich I., Cole R., Drdova E., Cvrckova F., Soukup A., Fowler J., Zarsky V. Arabidopsis exocyst subunits SEC8 and EXO70A1 and exocyst interactor ROH1 are involved in the localized deposition of seed coat pectin. New Phytol 2010, 188:615-625.
60. Samuel M.A., Chong Y.T., Haasen K.E., Aldea-Brydges M.G., Stone S.L., Goring D.R. Cellular pathways regulating responses to compatible and self-incompatible pollen in Brassica and Arabidopsis stigmas intersect at Exo70A1, a putative component of the exocyst complex. Plant Cell 2009, 21:2655-2671.
61. Pecenkova T., Hala M., Kulich I., Kocourkova D., Drdova E., Fendrych M., Toupalova H., Zarsky V. The role for the exocyst complex subunits Exo70B2 and Exo70H1 in the plant-pathogen interaction. J Exp Bot 2011, 62:2107-2116.
62. Stegmann M., Anderson R.G., Ichimura K., Pecenkova T., Reuter P., Zarsky V., McDowell J.M., Shirasu K., Trujillo M. The ubiquitin ligase PUB22 targets a subunit of the exocyst complex required for PAMP-triggered responses in Arabidopsis. Plant Cell 2012, 24:4703-4716.
63. Ostertag M., Stammler J., Douchkov D., Eichmann R., Huckelhoven R. The conserved oligomeric Golgi complex is involved in penetration resistance of barley to the barley powdery mildew fungus. Mol Plant Pathol 2013, 14:230-240.
64. Genre A., Ivanov S., Fendrych M., Faccio A., Zarsky V., Bisseling T., Bonfante P. Multiple exocytotic markers accumulate at the sites of perifungal membrane biogenesis in arbuscular mycorrhizas. Plant Cell Physiol 2012, 53:244-255.
65. Li S., Chen M., Yu D., Ren S., Sun S., Liu L., Ketelaar T., Emons A.M.C., Liu C. EXO70A1-mediated vesicle trafficking is critical for tracheary element development in Arabidopsis. Plant Cell 2013, 25:1774-1786.
66. Kulich I., Pecenkova T., Sekeres J., Smetana O., Fendrych M., Foissner I., Hoftberger M., Zarsky V. Arabidopsis exocyst subcomplex containing subunit EXO70B1 is involved in the autophagy-related transport to the vacuole. Traffic 2013, 14:1115-1165.
67. Zhao Y., Liu J., Yang C., Capraro B.R., Baumgart T., Bradley R.P., Ramakrishnan N., Xu X., Radhakrishnan R., Svitkina T., et al. Exo70 generates membrane curvature for morphogenesis and cell migration. Dev Cell 2013, 26:266-278.
68. Zhuang X., Wang H., Lam S.K., Gao C., Wang X., Cai Y., Jiang L. A BAR-domain protein SH3P2, which binds to phosphatidylinositol 3-phosphate and ATG8, regulates autophagosome formation in Arabidopsis. Plant Cell 2013, 25:4596-4615.
69. Jiang S., Dupont N., Castillo E., Deretic V. Secretory versus degradative autophagy: unconventional secretion of inflammatory mediators. J Innate Immun 2013, 5:471-479.
70. Manjithaya R., Anjard C., Loomis W., Subramani S. Unconventional secretion of Pichia pastoris Acb1 is dependent on GRASP protein, peroxisomal functions, and autophagosome formation. J Cell Biol 2010, 188:537-546.
71. Duran J., Anjard C., Stefan C., Loomis W., Malhotra V. Unconventional secretion of Acb1 is mediated by autophagosomes. J Cell Biol 2010, 188:527-536.
72. Bruns C., McCaffery J., Curwin A., Duran J., Malhotra V. Biogenesis of a novel compartment for autophagosome-mediated unconventional protein secretion. J Cell Biol 2011, 195:979-992.
73. Moore B.A., Robinson H.H., Xu Z.H. The crystal structure of mouse Exo70 reveals unique features of the mammalian exocyst. J Mol Biol 2007, 371:410-421.
74. Dong G., Hutagalung A.H., Fu C.M., Novick P., Reinisch K.M. The structures of exocyst subunit Exo70p and the Exo84p C-terminal domains reveal a common motif. Nat Struct Mol Biol 2005, 12:1094-1100.