Skip to main content

Plant extracellular vesicles

Abstract

Exocytosis is a key mechanism for delivering materials into the extracellular space for cell function and communication. In plant cells, conventional protein secretion (CPS) is achieved via an ER (endoplasmic reticulum)-Golgi-TGN (trans-Golgi network)-PM (plasma membrane) pathway. Unconventional protein secretion (UPS) bypassing these secretory organelles is also in operation and can potentially lead to the formation of extracellular vesicles (EVs) in plant cells. Although multiple types of EVs have been identified and shown to play important roles in mediating intercellular communications in mammalian cells, there has been a long debate about the possible existence of EVs in plants because of the presence of the cell wall. However, increasing evidence suggests that plants also release EVs having various functions including unconventional protein secretion, RNA transport, and defense against pathogens. In this review, we present an update on the current knowledge about the nature, secretory mechanism, and function of various types of EVs in plants. The key regulators involved in EV secretion are also summarized and discussed. We pay special attention to the function of EVs in plant defense and symbiosis.

This is a preview of subscription content, access via your institution.

Fig. 1

References

  1. Alenquer M, Amorim MJ (2015) Exosome biogenesis, regulation, and function in viral infection. Viruses 7:5066–5083

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  2. An QL, Huckelhoven R, Kogel KH, Van Bel AJE (2006a) Multivesicular bodies participate in a cell wall-associated defence response in barley leaves attacked by the pathogenic powdery mildew fungus. Cell Microbiol 8:1009–1019

    CAS  PubMed  Article  Google Scholar 

  3. An QL, Ehlers K, Kogel KH, van Bel AJE, Huckelhoven R (2006b) Multivesicular compartments proliferate in susceptible and resistant MLA12-barley leaves in response to infection by the biotrophic powdery mildew fungus. New Phytol 172:563–576

    CAS  PubMed  Article  Google Scholar 

  4. Baldrich P, Rutter BD, Karimi HZ, Podicheti R, Meyers BC, Innes RW (2019) Plant extracellular vesicles contain diverse small RNA species and are enriched in 10- to 17-nucleotide "tiny" RNAs. Plant Cell 31:315–324

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  5. Boevink PC (2017) Exchanging missives and missiles: the roles of extracellular vesicles in plant-pathogen interactions. J Exp Bot 68:5411–5414

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  6. Bozkurt TO, Belhaj K, Dagdas YF, Chaparro-Garcia A, Wu CH, Cano LM, Kamoun S (2015) Rerouting of plant late endocytic trafficking toward a pathogen Interface. Traffic 16:204–226

    CAS  PubMed  Article  Google Scholar 

  7. Bruns C, McCaffery JM, Curwin AJ, Duran JM, Malhotra V (2011) Biogenesis of a novel compartment for autophagosome-mediated unconventional protein secretion. J Cell Biol 195:979–992

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  8. Cai Q, Qiao LL, Wang M, He BY, Lin FM, Palmquist J, Huang SND, Jin HL (2018) Plants send small RNAs in extracellular vesicles to fungal pathogen to silence virulence genes. Science 360:1126–1129

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  9. Colombo M, Raposo G, Thery C (2014) Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu Rev Cell Dev Bi 30:255–289

    CAS  Article  Google Scholar 

  10. Cox G, Sanders F (1974) Ultrastructure of host-fungus Interface in a vesicular-arbuscular mycorrhiza. New Phytol 73:901 -&

    Article  Google Scholar 

  11. Cui Y, Zhang X, Yu M, Zhu Y, Xing J, Lin J (2019a) Techniques for detecting protein-protein interactions in living cells: principles, limitations, and recent progress. Sci China Life Sci 62:619–632

    PubMed  Article  Google Scholar 

  12. Cui Y, Zhao Q, Gao C, Ding Y, Zeng Y, Ueda T, Nakano A, Jiang L (2014) Activation of the Rab7 GTPase by the MON1-CCZ1 complex is essential for PVC-to-vacuole trafficking and plant growth in Arabidopsis. Plant Cell 26:2080–2097

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  13. Cui Y, Cao W, He Y, Zhao Q, Wakazaki M, Zhuang X, Gao J, Zeng Y, Gao C, Ding Y, Wong HY, Wong WS, Lam HK, Wang P, Ueda T, Rojas-Pierce M, Toyooka K, Kang BH, Jiang L (2019b) A whole-cell electron tomography model of vacuole biogenesis in Arabidopsis root cells. Nat Plants 5:95–105

    CAS  PubMed  Article  Google Scholar 

  14. de la Canal L, Pinedo M (2018) Extracellular vesicles: a missing component in plant cell wall remodeling. J Exp Bot 69:4655–4658

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  15. Deatherage BL, Cookson BT (2012) Membrane vesicle release in bacteria, eukaryotes, and archaea: a conserved yet underappreciated aspect of microbial life. Infect Immun 80:1948–1957

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  16. Dexheimer J, Marx C, Gianinazzipearson V, Gianinazzi S (1985) Ultracytological studies of Plasmalemma formations produced by host and fungus in Vesiculararbuscular mycorrhizae. Cytologia (Tokyo) 50:461–471

    Article  Google Scholar 

  17. Ding Y, Robinson DG, Jiang L (2014a) Unconventional protein secretion (UPS) pathways in plants. Curr Opin Cell Biol 29:107–115

    CAS  PubMed  Article  Google Scholar 

  18. Ding Y, Wang J, Wang JQ, Stierhof YD, Robinson DG, Jiang L (2012) Unconventional protein secretion. Trends Plant Sci 17:606–615

    CAS  PubMed  Article  Google Scholar 

  19. Ding Y, Wang J, Lai JHC, Chan VHL, Wang XF, Cai Y, Tan XY, Bao YQ, Xia J, Robinson DG, Jiang L (2014b) Exo70E2 is essential for exocyst subunit recruitment and EXPO formation in both plants and animals. Mol Biol Cell 25:412–426

    PubMed  PubMed Central  Article  Google Scholar 

  20. Ebine K, Inoue T, Ito J, Ito E, Uemura T, Goh T, Abe H, Sato K, Nakano A, Ueda T (2014) Plant vacuolar trafficking occurs through distinctly regulated pathways. Curr Biol 24:1375–1382

    CAS  PubMed  Article  Google Scholar 

  21. Gao C, Zhuang X, Shen J, Jiang L (2017) Plant ESCRT complexes: moving beyond endosomal sorting. Trends Plant Sci 22:986–998

    CAS  PubMed  Article  Google Scholar 

  22. Gonorazky G, Laxalt AM, Dekker HL, Rep M, Munnik T, Testerink C, de la Canal L (2012) Phosphatidylinositol 4-phosphate is associated to extracellular lipoproteic fractions and is detected in tomato apoplastic fluids. Plant Biol 14:41–49

    CAS  PubMed  Google Scholar 

  23. Gu YN, Zavaliev R, Dong XN (2017) Membrane trafficking in plant immunity. Mol Plant 10:1026–1034

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  24. Gutjahr C, Parniske M (2013) Cell and developmental biology of arbuscular mycorrhiza symbiosis. Annu Rev Cell Dev Biol 29:593–617

    CAS  Article  Google Scholar 

  25. Halperin W, Jensen WA (1967) Ultrastructural changes during growth and embryogenesis in carrot cell cultures. J Ultrastruct Res 18:428–443

    CAS  PubMed  Article  Google Scholar 

  26. Hansen LL, Nielsen ME (2018) Plant exosomes: using an unconventional exit to prevent pathogen entry? J Exp Bot 69:59–68

    Article  CAS  Google Scholar 

  27. Harding C, Heuser J, Stahl P (1983) Receptor-mediated endocytosis of transferrin and recycling of the transferrin receptor in rat reticulocytes. J Cell Biol 97:329–339

    CAS  PubMed  Article  Google Scholar 

  28. Hatsugai N, Kuroyanagi M, Nishimura M, Hara-Nishimura I (2006) A cellular suicide strategy of plants: vacuole-mediated cell death. Apoptosis 11:905–911

    CAS  PubMed  Article  Google Scholar 

  29. Hatsugai N, Kuroyanagi M, Yamada K, Meshi T, Tsuda S, Kondo M, Nishimura M, Hara-Nishimura I (2004) A plant vacuolar protease, VPE, mediates virus-induced hypersensitive cell death. Science 305:855–858

    CAS  PubMed  Article  Google Scholar 

  30. Hatsugai N, Iwasaki S, Tamura K, Kondo M, Fuji K, Ogasawara K, Nishimura M, Hara-Nishimura I (2009) A novel membrane fusion-mediated plant immunity against bacterial pathogens. Genes Dev 23:2496–2506

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  31. Hessvik NP, Llorente A (2018) Current knowledge on exosome biogenesis and release. Cell Mol Life Sci 75:193–208

    CAS  PubMed  Article  Google Scholar 

  32. Ivanov S, Austin J, Berg RH, Harrison MJ (2019) Extensive membrane systems at the host-arbuscular mycorrhizal fungus interface. Nat plants 5:194 −+

    PubMed  Article  Google Scholar 

  33. Jin D, Meng X, Wang Y, Wang J, Zhao Y, Chen M (2018) Computational investigation of small RNAs in the establishment of root nodules and arbuscular mycorrhiza in leguminous plants. Sci China Life Sci 61:706–717

    CAS  PubMed  Article  Google Scholar 

  34. Johnstone RM, Adam M, Hammond JR, Orr L, Turbide C (1987) Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J Biol Chem 262:9412–9420

    CAS  PubMed  Google Scholar 

  35. Ju S, Mu J, Dokland T, Zhuang X, Wang Q, Jiang H, Xiang X, Deng ZB, Wang B, Zhang L, Roth M, Welti R, Mobley J, Jun Y, Miller D, Zhang HG (2013) Grape exosome-like nanoparticles induce intestinal stem cells and protect mice from DSS-induced colitis. Mol Ther 21:1345–1357

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  36. Limpens E (2019) Extracellular membranes in symbiosis. Nat Plants 5:131–132

    PubMed  Article  Google Scholar 

  37. Lin Y, Ding Y, Wang J, Shen J, Kung CH, Zhuang X, Cui Y, Yin Z, Xia Y, Lin H, Robinson DG, Jiang L (2015) Exocyst-positive organelles and autophagosomes are distinct organelles in plants. Plant Physiol 169:1917–1932

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Ma C, Wang Y, Gu D, Nan J, Chen S, Li H (2017) Overexpression of S-adenosyl-Lmethionine synthetase 2 from sugar beet M14 increased Arabidopsis tolerance to salt and oxidative stress. Int J Mol Sci 18:847. 

    PubMed Central  Article  CAS  PubMed  Google Scholar 

  39. Manjithaya R, Subramani S (2010) Role of autophagy in unconventional protein secretion. Autophagy 6:650–651

    PubMed  PubMed Central  Article  Google Scholar 

  40. Manocha MS, Shaw M (1964) Occurrence of Lomasomes in mesophyll cells of Khapli wheat. Nature 203:1402 -&

    Article  Google Scholar 

  41. Mathieu M, Martin-Jaular L, Lavieu G, Thery C (2019) Specificities of secretion and uptake of exosomes and other extracellular vesicles for cell-to-cell communication. Nat Cell Biol 21:9–17

    CAS  PubMed  Article  Google Scholar 

  42. Meyer D, Pajonk S, Micali C, O'Connell R, Schulze-Lefert P (2009) Extracellular transport and integration of plant secretory proteins into pathogen-induced cell wall compartments. Plant J 57:986–999

    CAS  PubMed  Article  Google Scholar 

  43. Movahed N, Cabanillas DG, Wan J, Vali H, Laliberte JF, Zheng HQ (2019) Turnip mosaic virus components are released into the extracellular space by vesicles in infected leaves. Plant Physiol 180:1375-1388

    CAS  PubMed  Article  Google Scholar 

  44. Prado N, Alche JD, Casado-Vela J, Mas S, Villalba M, Rodriguez R, Batanero E (2014) Nanovesicles are secreted during pollen germination and pollen tube growth: A possible role in fertilization. Mol Plant 7:573–577

    CAS  PubMed  Article  Google Scholar 

  45. Regente M, Pinedo M, San Clemente H, Balliau T, Jamet E, de la Canal L (2017) Plant extracellular vesicles are incorporated by a fungal pathogen and inhibit its growth. J Exp Bot 68:5485–5495

    CAS  PubMed  Article  Google Scholar 

  46. Robinson D, Ding Y, Jiang L (2016) Unconventional protein secretion in plants: a critical assessment. Protoplasma 253:31–43

    CAS  PubMed  Article  Google Scholar 

  47. Roth R, Hillmer S, Funaya C, Chiapello M, Schumacher K, Lo Presti L, Kahmann R, Paszkowski U (2019) Arbuscular cell invasion coincides with extracellular vesicles and membrane tubules. Nat plants 5:204−+

    PubMed  Article  CAS  Google Scholar 

  48. Rutter BD, Innes RW (2017) Extracellular vesicles isolated from the leaf Apoplast carry stress-response proteins. Plant Physiol 173:728–741

    CAS  PubMed  Article  Google Scholar 

  49. Rutter BD, Innes RW (2018) Extracellular vesicles as key mediators of plant-microbe interactions. Curr Opin Plant Biol 44:16–22

    CAS  PubMed  Article  Google Scholar 

  50. Rybak K, Robatzek S (2019) Functions of extracellular vesicles in immunity and virulence. Plant Physiol 179:1236–1247

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  51. Schooling SR, Beveridge TJ (2006) Membrane vesicles: an overlooked component of the matrices of biofilms. J Bacteriol 188:5945–5957

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  52. Singh MK, Kruger F, Beckmann H, Brumm S, Vermeer JEM, 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

    CAS  PubMed  Article  Google Scholar 

  53. Tse YC, Mo BX, Hillmer S, Zhao M, Lo SW, Robinson DG, Jiang LW (2004) Identification of multivesicular bodies as prevacuolar compartments in Nicotiana tabacum BY-2 cells. Plant Cell 16:672–693

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  54. van Niel G, D'Angelo G, Raposo G (2018) Shedding light on the cell biology of extracellular vesicles. Nat Rev Mol Cell Biol 19:213–228

    PubMed  Article  CAS  Google Scholar 

  55. Wang J, Silva M, Haas LA, Morsci NS, Nguyen KCQ, Hall DH, Barr MM (2014) C-elegans ciliated sensory neurons release extracellular vesicles that function in animal communication. Curr Biol 24:519–525

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  56. Wang JA, Ding Y, Wang JQ, Hillmer S, Miao YS, Lo SW, Wang XF, Robinson DG, Jiang L (2010) EXPO, an exocyst-positive organelle distinct from multivesicular endosomes and autophagosomes, mediates cytosol to Cell Wall exocytosis in Arabidopsis and tobacco cells. Plant Cell 22:4009–4030

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  57. Wang XF, Chung KP, Lin WL, Jiang L (2018) Protein secretion in plants: conventional and unconventional pathways and new techniques. J Exp Bot 69:21–37

    Article  CAS  Google Scholar 

  58. Xu X, Xue Y, Tian B, Feng F, Gu L, Li W, Ji W, Xu T (2018) Ultra-stable super-resolution fluorescence cryo-microscopy for correlative light and electron cryo-microscopy. Sci China Life Sci 61:1312–1319

    CAS  PubMed  Article  Google Scholar 

  59. Yanez-Mo M, Siljander PRM, Andreu Z, Zavec AB, Borras FE, Buzas EI, Buzas K, Casal E, Cappello F, Carvalho J, Colas E, Cordeiro-da Silva A, Fais S, Falcon-Perez JM, Ghobrial IM, Giebel B, Gimona M, Graner M, Gursel I, Gursel M, Heegaard NHH, Hendrix A, Kierulf P, Kokubun K, Kosanovic M, Kralj-Iglic V, Kramer-Albers EM, Laitinen S, Lasser C, Lener T, Ligeti E, Line A, Lipps G, Llorente A, Lotvall J, Mancek-Keber M, Marcilla A, Mittelbrunn M, Nazarenko I, Nolte-t’ Hoen ENM, Nyman TA, O'Driscoll L, Olivan M, Oliveira C, Pallinger E, del Portillo HA, Reventos J, Rigau M, Rohde E, Sammar M, Sanchez-Madrid F, Santarem N, Schallmoser K, Ostenfeld MS, Stoorvogel W, Stukelj R, Van der Grein SG, Vasconcelos MH, Wauben MHM, De Wever O (2015) Biological properties of extracellular vesicles and their physiological functions. J Extracell Vesicles 4:27066

    PubMed  Article  Google Scholar 

  60. Zhao ZH, Yu SR, Li M, Gui X, Li P (2018) Isolation of exosome-like nanoparticles and analysis of MicroRNAs derived from coconut water based on small RNA high-throughput sequencing. J Agric Food Chem 66:2749–2757

    CAS  PubMed  Article  Google Scholar 

  61. Zhuang X, Chung KP, Luo M, Jiang L (2018) Autophagosome biogenesis and the endoplasmic reticulum: A plant perspective. Trends Plant Sci 23:677–692

    CAS  PubMed  Article  Google Scholar 

  62. Zhuang X, Chung KP, Cui Y, Lin W, Gao C, Kang BH, Jiang L (2017) ATG9 regulates autophagosome progression from the endoplasmic reticulum in Arabidopsis. Proc Natl Acad Sci U S A 114:E426–E435

    CAS  PubMed  PubMed Central  Article  Google Scholar 

Download references

Acknowledgments

We apologize to researchers whose work could not be included in this manuscript owing to space limitations.

Funding

This work was supported by grants from the Research Grants Council of Hong Kong (AoE/M-05/12, CUHK14130716, 14102417, 14100818, 14104716, C4012-16E, C4002-17G, and RIF R4005-18), the National Natural Science Foundation of China (31670179 and 91854201), and CUHK Research Committee.

Author information

Affiliations

Authors

Corresponding authors

Correspondence to Yong Cui or Liwen Jiang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Specialty issue: This article is submitted as an invited contribution to a special issue on “intercellular communication mediated by membrane vesicles and their components, respectively” edited by Dr. Joern Bullerdiek, associate editor Protoplasma. Our contribution is to address possible mechanisms of exosomal release by plant cells.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Cui, Y., Gao, J., He, Y. et al. Plant extracellular vesicles. Protoplasma 257, 3–12 (2020). https://doi.org/10.1007/s00709-019-01435-6

Download citation

Keywords

  • Extracellular vesicle
  • Exosome
  • EXPO
  • Protein secretion
  • Plant defense