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Abstract

Communication between plant cells and interacting microorganisms requires the secretion and uptake of functional molecules to and from the extracellular environment and is essential for the survival of both plants and their pathogens. Extracellular vesicles (EVs) are lipid bilayer–enclosed spheres that deliver RNA, protein, and metabolite cargos from donor to recipient cells and participate in many cellular processes. Emerging evidencehas shown that both plant and microbial EVs play important roles in cross-kingdom molecular exchange between hosts and interacting microbes to modulate host immunity and pathogen virulence. Recent studies revealed that plant EVs function as a defense system by encasing and delivering small RNAs (sRNAs) into pathogens, thereby mediating cross-species and cross-kingdom RNA interference to silence virulence-related genes. This review focuses on the latest advances in our understanding of plant and microbial EVs and their roles in transporting regulatory molecules, especially sRNAs, between hosts and pathogens. EV biogenesis and secretion are also discussed, as EV function relies on these important processes.

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2021-06-17
2024-05-05
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Literature Cited

  1. 1. 
    Akers JC, Gonda D, Kim R, Carter BS, Chen CC. 2013. Biogenesis of extracellular vesicles (EV): exosomes, microvesicles, retrovirus-like vesicles, and apoptotic bodies. J. Neurooncol. 113:1–11
    [Google Scholar]
  2. 2. 
    Akinc A, Maier MA, Manoharan M, Fitzgerald K, Jayaraman M et al. 2019. The Onpattro story and the clinical translation of nanomedicines containing nucleic acid-based drugs. Nat. Nanotechnol. 14:1084–87
    [Google Scholar]
  3. 3. 
    Akuma P, Okagu OD, Udenigwe CC. 2019. Naturally occurring exosome vesicles as potential delivery vehicle for bioactive compounds. Front. Sustain. Food Syst. 3:23
    [Google Scholar]
  4. 4. 
    Alavi M, Karimi N, Safaei M. 2017. Application of various types of liposomes in drug delivery systems. Adv. Pharm. Bull. 7:3–9
    [Google Scholar]
  5. 5. 
    An Q, Ehlers K, Kogel KH, van Bel AJ, Huckelhoven R. 2006. Multivesicular compartments proliferate in susceptible and resistant MLA12-barley leaves in response to infection by the biotrophic powdery mildew fungus. New Phytol 172:563–76
    [Google Scholar]
  6. 6. 
    An Q, Huckelhoven R, Kogel KH, van Bel AJ. 2006. Multivesicular bodies participate in a cell wall-associated defence response in barley leaves attacked by the pathogenic powdery mildew fungus. Cell. Microbiol. 8:1009–19
    [Google Scholar]
  7. 7. 
    An Q, van Bel AJ, Huckelhoven R. 2007. Do plant cells secrete exosomes derived from multivesicular bodies?. Plant Signal. Behav. 2:4–7
    [Google Scholar]
  8. 8. 
    Anderson J, Mihalik R, Soll DR. 1990. Ultrastructure and antigenicity of the unique cell wall pimple of the Candida opaque phenotype. J. Bacteriol. 172:224–35
    [Google Scholar]
  9. 9. 
    Andreu Z, Yáñez-Mó M. 2014. Tetraspanins in extracellular vesicle formation and function. Front. Immunol. 5:442
    [Google Scholar]
  10. 10. 
    Aqil F, Kausar H, Agrawal AK, Jeyabalan J, Kyakulaga AH et al. 2016. Exosomal formulation enhances therapeutic response of celastrol against lung cancer. Exp. Mol. Pathol. 101:12–21
    [Google Scholar]
  11. 11. 
    Armstrong JPK, Stevens MM. 2018. Strategic design of extracellular vesicle drug delivery systems. Adv. Drug Deliver. Rev. 130:12–16
    [Google Scholar]
  12. 12. 
    Atkin-Smith GK, Tixeira R, Paone S, Mathivanan S, Collins C et al. 2015. A novel mechanism of generating extracellular vesicles during apoptosis via a beads-on-a-string membrane structure. Nat. Commun. 6:7439
    [Google Scholar]
  13. 13. 
    Avellan A, Yun J, Zhang YL, Spielman-Sun E, Unrine JM et al. 2019. Nanoparticle size and coating chemistry control foliar uptake pathways, translocation, and leaf-to-rhizosphere transport in wheat. ACS Nano 13:5291–305
    [Google Scholar]
  14. 14. 
    Bachman PM, Huizinga KM, Jensen PD, Mueller G, Tan JG et al. 2016. Ecological risk assessment for DvSnf7 RNA: A plant-incorporated protectant with targeted activity against western corn rootworm. Regul. Toxicol. Pharm. 81:77–88
    [Google Scholar]
  15. 15. 
    Bahar O, Mordukhovich G, Luu DD, Schwessinger B, Daudi A et al. 2016. Bacterial outer membrane vesicles induce plant immune responses. Mol. Plant Microbe Interact. 29:374–84
    [Google Scholar]
  16. 16. 
    Bajan S, Hutvagner G. 2020. RNA-based therapeutics: from antisense oligonucleotides to miRNAs. Cells 9:137
    [Google Scholar]
  17. 17. 
    Baldrich P, Rutter BD, Zand Karimi H, 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 31:315–24
    [Google Scholar]
  18. 18. 
    Baulcombe D. 2004. RNA silencing in plants. Nature 431:356–63
    [Google Scholar]
  19. 19. 
    Bielska E, Sisquella MA, Aldeieg M, Birch C, O'Donoghue EJ, May RC 2018. Pathogen-derived extracellular vesicles mediate virulence in the fatal human pathogen Cryptococcus gattii. Nat. Commun. 9:1556
    [Google Scholar]
  20. 20. 
    Bishop DG, Work E. 1965. An extracellular glycolipid produced by Escherichia coli grown under lysine-limiting conditions. Biochem. J. 96:567–76
    [Google Scholar]
  21. 21. 
    Bleackley MR, Dawson CS, Anderson MA. 2019. Fungal extracellular vesicles with a focus on proteomic analysis. Proteomics 19:e1800232
    [Google Scholar]
  22. 22. 
    Bleackley MR, Samuel M, Garcia-Ceron D, McKenna JA, Lowe RGT et al. 2019. Extracellular vesicles from the cotton pathogen Fusarium oxysporum f. sp. vasinfectum induce a phytotoxic response in plants. Front. Plant Sci. 10:1610This study showed that plant fungal-pathogen-derived EVs play a crucial role in the infection process.
    [Google Scholar]
  23. 23. 
    Boavida LC, Qin P, Broz M, Becker JD, McCormick S. 2013. Arabidopsis tetraspanins are confined to discrete expression domains and cell types in reproductive tissues and form homo- and heterodimers when expressed in yeast. Plant Physiol 163:696–712
    [Google Scholar]
  24. 24. 
    Bozkurt TO, Belhaj K, Dagdas YF, Chaparro-Garcia A, Wu C-H et al. 2015. Rerouting of plant late endocytic trafficking toward a pathogen interface. Traffic 16:204–26
    [Google Scholar]
  25. 25. 
    Brown L, Wolf JM, Prados-Rosales R, Casadevall A. 2015. Through the wall: extracellular vesicles in Gram-positive bacteria, mycobacteria and fungi. Nat. Rev. Microbiol. 13:620–30This review discusses how EVs escape the thick cell walls of microorganisms.
    [Google Scholar]
  26. 26. 
    Buck AH, Coakley G, Simbari F, McSorley HJ, Quintana JF et al. 2014. Exosomes secreted by nematode parasites transfer small RNAs to mammalian cells and modulate innate immunity. Nat. Commun. 5:5488This work provides a mechanistic framework for RNA transport between animal species.
    [Google Scholar]
  27. 27. 
    Cagliari D, Dias NP, Galdeano DM, dos Santos EA, Smagghe G, Zotti MJ. 2019. Management of pest insects and plant diseases by non-transformative RNAi. Front. Plant Sci. 10:1319
    [Google Scholar]
  28. 28. 
    Cai Q, He B, Jin H 2019. A safe ride in extracellular vesicles—small RNA trafficking between plant hosts and pathogens. Curr. Opin. Plant Biol. 52:140–48
    [Google Scholar]
  29. 29. 
    Cai Q, He B, Kogel KH, Jin H 2018. Cross-kingdom RNA trafficking and environmental RNAi—nature's blueprint for modern crop protection strategies. Curr. Opin. Microbiol. 46:58–64
    [Google Scholar]
  30. 30. 
    Cai Q, He B, Weiberg A, Buck AH, Jin H 2019. Small RNAs and extracellular vesicles: new mechanisms of cross-species communication and innovative tools for disease control. PLOS Pathog 15:e1008090
    [Google Scholar]
  31. 31. 
    Cai Q, Qiao L, Wang M, He B, Lin FM et al. 2018. Plants send small RNAs in extracellular vesicles to fungal pathogen to silence virulence genes. Science 360:1126–29The authors discovered that plant hosts have adapted exosome-mediated cross-kingdom RNAi as part of their immune responses.
    [Google Scholar]
  32. 32. 
    Castellanos NL, Smagghe G, Sharma R, Oliveira EE, Christiaens O. 2019. Liposome encapsulation and EDTA formulation of dsRNA targeting essential genes increase oral RNAi-caused mortality in the Neotropical stink bug Euschistus heros. Pest Manag. Sci. 75:537–48
    [Google Scholar]
  33. 33. 
    Cha DJ, Franklin JL, Dou YC, Liu Q, Higginbotham JN et al. 2015. KRAS-dependent sorting of miRNA to exosomes. eLife 4:e07197
    [Google Scholar]
  34. 34. 
    Chowdhury C, Jagannadham MV. 2013. Virulence factors are released in association with outer membrane vesicles of Pseudomonas syringae pv. tomato T1 during normal growth. Biochim. Biophys. Acta 1834:231–39
    [Google Scholar]
  35. 35. 
    Coakley G, Maizels RM, Buck AH. 2015. Exosomes and other extracellular vesicles: the new communicators in parasite infections. Trends Parasitol 31:477–89
    [Google Scholar]
  36. 36. 
    Colombo M, Raposo G, Thery C. 2014. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu. Rev. Cell Dev. Biol. 30:255–89
    [Google Scholar]
  37. 37. 
    Crescitelli R, Lässer C, Szabó TG, Kittel A, Eldh M et al. 2013. Distinct RNA profiles in subpopulations of extracellular vesicles: apoptotic bodies, microvesicles and exosomes. J. Extracell. Vesicles 2:1 https://doi.org/10.3402/jev.v2i0.20677
    [Crossref] [Google Scholar]
  38. 38. 
    Cui C, Wang Y, Liu J, Zhao J, Sun P, Wang S 2019. A fungal pathogen deploys a small silencing RNA that attenuates mosquito immunity and facilitates infection. Nat. Commun. 10:4298
    [Google Scholar]
  39. 39. 
    da Silva RP, Heiss C, Black I, Azadi P, Gerlach JQ et al. 2015. Extracellular vesicles from Paracoccidioides pathogenic species transport polysaccharide and expose ligands for DC-SIGN receptors. Sci. Rep. 5:14213
    [Google Scholar]
  40. 40. 
    Das S, Ansel KM, Bitzer M, Breakefield XO, Charest A et al. 2019. The Extracellular RNA Communication Consortium: establishing foundational knowledge and technologies for extracellular RNA research. Cell 177:231–42
    [Google Scholar]
  41. 41. 
    Dawson CS, Garcia-Ceron D, Rajapaksha H, Faou P, Bleackley MR, Anderson MA. 2020. Protein markers for Candida albicans EVs include claudin-like Sur7 family proteins. J. Extracell. Vesicles 9:1 https://doi.org/10.1080/20013078.2020.1750810
    [Crossref] [Google Scholar]
  42. 42. 
    de Paula RG, Antonieto ACC, Nogueira KMV, Ribeiro LFC, Rocha MC et al. 2019. Extracellular vesicles carry cellulases in the industrial fungus Trichoderma reesei. Biotechnol. Biofuels 12:146
    [Google Scholar]
  43. 43. 
    de Toledo Martins S, Szwarc P, Goldenberg S, Alves LR. 2018. Extracellular vesicles in fungi: composition and functions. Curr. Top. Microbiol. Immunol. 422:45–59
    [Google Scholar]
  44. 44. 
    Demirer GS, Zhang H, Goh NS, Gonzalez-Grandio E, Landry MP. 2019. Carbon nanotube-mediated DNA delivery without transgene integration in intact plants. Nat. Protoc. 14:2954–71
    [Google Scholar]
  45. 45. 
    Demirer GS, Zhang H, Goh NS, Pinals RL, Chang R, Landry MP 2020. Carbon nanocarriers deliver siRNA to intact plant cells for efficient gene knockdown. Sci. Adv. 6:eaaz0495
    [Google Scholar]
  46. 46. 
    Ding Y, Wang J, Chun Lai JH, Ling Chan VH, Wang X et al. 2014. Exo70E2 is essential for exocyst subunit recruitment and EXPO formation in both plants and animals. Mol. Biol. Cell 25:412–26
    [Google Scholar]
  47. 47. 
    Dorward DW, Garon CF. 1990. DNA is packaged within membrane-derived vesicles of gram-negative but not gram-positive bacteria. Appl. Environ. Microb. 56:1960–62
    [Google Scholar]
  48. 48. 
    Dragomir M, Chen BQ, Calin GA. 2018. Exosomal lncRNAs as new players in cell-to-cell communication. Transl. Cancer Res. 7:S243–52
    [Google Scholar]
  49. 49. 
    Dunker F, Trutzenberg A, Rothenpieler JS, Kuhn S, Prols R et al. 2020. Oomycete small RNAs bind to the plant RNA-induced silencing complex for virulence. eLife 9:e56096
    [Google Scholar]
  50. 50. 
    El-Andaloussi S, Lee Y, Lakhal-Littleton S, Li JH, Seow Y et al. 2012. Exosome-mediated delivery of siRNA in vitro and in vivo. Nat. Protoc. 7:2112–26
    [Google Scholar]
  51. 51. 
    Ellen AF, Albers SV, Huibers W, Pitcher A, Hobel CFV et al. 2009. Proteomic analysis of secreted membrane vesicles of archaeal Sulfolobus species reveals the presence of endosome sorting complex components. Extremophiles 13:67–79
    [Google Scholar]
  52. 52. 
    Elsharkasy OM, Nordin JZ, Hagey DW, de Jong OG, Schiffelers RM et al. 2020. Extracellular vesicles as drug delivery systems: Why and how?. Adv. Drug Deliver. Rev. 159:332–42
    [Google Scholar]
  53. 53. 
    Fan L, Li R, Pan J, Ding Z, Lin J. 2015. Endocytosis and its regulation in plants. Trends Plant Sci 20:388–97
    [Google Scholar]
  54. 54. 
    Feitosa-Junior OR, Stefanello E, Zaini PA, Nascimento R, Pierry PM et al. 2019. Proteomic and metabolomic analyses of Xylella fastidiosa OMV-enriched fractions reveal association with virulence factors and signaling molecules of the DSF family. Phytopathology 109:1344–53
    [Google Scholar]
  55. 55. 
    Ferrari S, Galletti R, Denoux C, De Lorenzo G, Ausubel FM, Dewdney J. 2007. Resistance to Botrytis cinerea induced in Arabidopsis by elicitors is independent of salicylic acid, ethylene, or jasmonate signaling but requires PHYTOALEXIN DEFICIENT3. Plant Physiol 144:367–79
    [Google Scholar]
  56. 56. 
    Fletcher SJ, Reeves PT, Hoang BT, Mitter N. 2020. A perspective on RNAi-based biopesticides. Front. Plant Sci. 11:51
    [Google Scholar]
  57. 57. 
    Freitas MS, Bonato VLD, Pessoni AM, Rodrigues ML, Casadevall A, Almeida F. 2019. Fungal extracellular vesicles as potential targets for immune interventions. Msphere 4:e00747–19
    [Google Scholar]
  58. 58. 
    Halperin W, Jensen WA. 1967. Ultrastructural changes during growth and embryogenesis in carrot cell cultures. J. Ultrastruct. R. 18:428–43
    [Google Scholar]
  59. 59. 
    He B, Cai Q, Qiao L, Huang C, Wang S et al. 2021. RNA-binding proteins contribute to small RNA loading in plant extracellular vesicles. Nat. Plants 7:34252This work showed that RBPs play an important role in selective loading and stabilization of sRNAs in plant EVs.
    [Google Scholar]
  60. 60. 
    Hegedus N, Marx F. 2013. Antifungal proteins: more than antimicrobials?. Fungal Biol. Rev. 26:132–45
    [Google Scholar]
  61. 61. 
    Hiruma K, Onozawa-Komori M, Takahashi F, Asakura M, Bednarek P et al. 2010. Entry mode–dependent function of an indole glucosinolate pathway in Arabidopsis for nonhost resistance against anthracnose pathogens. Plant Cell 22:2429–43
    [Google Scholar]
  62. 62. 
    Hou Y, Zhai Y, Feng L, Karimi HZ, Rutter BD et al. 2019. A Phytophthora effector suppresses trans-kingdom RNAi to promote disease susceptibility. Cell Host Microbe 25:153–65.e5
    [Google Scholar]
  63. 63. 
    Huang CY, Wang H, Hu P, Hamby R, Jin H 2019. Small RNAs—big players in plant-microbe interactions. Cell Host Microbe 26:173–82
    [Google Scholar]
  64. 64. 
    Ionescu M, Zaini PA, Baccari C, Tran S, da Silva AM, Lindow SE 2014. Xylella fastidiosa outer membrane vesicles modulate plant colonization by blocking attachment to surfaces. PNAS 111:E3910–18
    [Google Scholar]
  65. 65. 
    Jan AT. 2017. Outer membrane vesicles (OMVs) of gram-negative bacteria: a perspective update. Front. Microbiol. 8:1053
    [Google Scholar]
  66. 66. 
    Jeppesen DK, Fenix AM, Franklin JL, Higginbotham JN, Zhang Q et al. 2019. Reassessment of exosome composition. Cell 177:428–45.e18
    [Google Scholar]
  67. 67. 
    Jia RZ, Zhao H, Huang J, Kong H, Zhang YL et al. 2017. Use of RNAi technology to develop a PRSV-resistant transgenic papaya. Sci. Rep. 7:12636
    [Google Scholar]
  68. 68. 
    Jiao J, Peng D. 2018. Wheat microRNA1023 suppresses invasion of Fusarium graminearum via targeting and silencing FGSG_03101. J. Plant Interact. 13:514–21
    [Google Scholar]
  69. 69. 
    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. 262:9412–20
    [Google Scholar]
  70. 70. 
    Jose AM. 2015. Movement of regulatory RNA between animal cells. Genesis 53:395–416
    [Google Scholar]
  71. 71. 
    Katsir L, Bahar O. 2017. Bacterial outer membrane vesicles at the plant-pathogen interface. PLOS Pathog 13:e1006306
    [Google Scholar]
  72. 72. 
    Kimura M, Anzai H, Yamaguchi I. 2001. Microbial toxins in plant-pathogen interactions: biosynthesis, resistance mechanisms, and significance. J. Gen. Appl. Microbiol. 47:149–60
    [Google Scholar]
  73. 73. 
    Knip M, Constantin ME, Thordal-Christensen H. 2014. Trans-kingdom cross-talk: small RNAs on the move. PLOS Genet 10:e1004602
    [Google Scholar]
  74. 74. 
    Koch A, Biedenkopf D, Furch A, Weber L, Rossbach O et al. 2016. An RNAi-based control of Fusarium graminearum infections through spraying of long dsRNAs involves a plant passage and is controlled by the fungal silencing machinery. PLOS Pathog 12:e1005901
    [Google Scholar]
  75. 75. 
    Koch A, Kumar N, Weber L, Keller H, Imani J, Kogel KH 2013. Host-induced gene silencing of cytochrome P450 lanosterol C14α-demethylase–encoding genes confers strong resistance to Fusarium species. PNAS 110:19324–29
    [Google Scholar]
  76. 76. 
    Koch A, Schlemmer T, Höfle L, Werner BT, Preußer C et al. 2020. Host-induced gene silencing involves transfer of dsRNA-derived siRNA via extracellular vesicles. bioRxiv 2020.02.12.945154. https://doi.org/10.1101/2020.02.12.945154
    [Crossref]
  77. 77. 
    Konoshenko MY, Lekchnov EA, Vlassov AV, Laktionov PP. 2018. Isolation of extracellular vesicles: general methodologies and latest trends. BioMed. Res. Int. 2018:8545347
    [Google Scholar]
  78. 78. 
    Kowal J, Arras G, Colombo M, Jouve M, Morath JP et al. 2016. Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes. PNAS 113:E968–77
    [Google Scholar]
  79. 79. 
    Kwon C, Neu C, Pajonk S, Yun HS, Lipka U et al. 2008. Co-option of a default secretory pathway for plant immune responses. Nature 451:835–40
    [Google Scholar]
  80. 80. 
    Laurent J, Paulin JP, Zucca J. 1987. Ultrastructural study of Erwinia amylovora strains: effect of culture conditions and fixation procedures. Protoplasma 139:1–8
    [Google Scholar]
  81. 81. 
    Lee EY, Choi DY, Kim DK, Kim JW, Park JO et al. 2009. Gram-positive bacteria produce membrane vesicles: proteomics-based characterization of Staphylococcus aureus-derived membrane vesicles. Proteomics 9:5425–36
    [Google Scholar]
  82. 82. 
    Liu F, Wen LX, Li ZZ, Yu W, Sun HY, Chen JF. 2006. Porous hollow silica nanoparticles as controlled delivery system for water-soluble pesticide. Mater. Res. Bull. 41:2268–75
    [Google Scholar]
  83. 83. 
    Liu NJ, Wang N, Bao JJ, Zhu HX, Wang LJ, Chen XY. 2020. Lipidomic analysis reveals the importance of GIPCs in Arabidopsis leaf extracellular vesicles. Mol. Plant 13:1523–32
    [Google Scholar]
  84. 84. 
    Liu Y, Mittal R, Solis NV, Prasadarao NV, Filler SG. 2011. Mechanisms of Candida albicans trafficking to the brain. PLOS Pathog 7:e1002305
    [Google Scholar]
  85. 85. 
    Lu M, Xing HN, Xun Z, Yang TZ, Ding PT et al. 2018. Exosome-based small RNA delivery: progress and prospects. Asian J. Pharm. Sci. 13:1–11
    [Google Scholar]
  86. 86. 
    Lu R, Drubin DG, Sun YD. 2016. Clathrin-mediated endocytosis in budding yeast at a glance. J. Cell Sci. 129:1531–36
    [Google Scholar]
  87. 87. 
    Ma CX, White JC, Zhao J, Zhao Q, Xing BS. 2018. Uptake of engineered nanoparticles by food crops: characterization, mechanisms, and implications. Annu. Rev. Food Sci. Technol. 9:129–53
    [Google Scholar]
  88. 88. 
    Mahlapuu M, Hakansson J, Ringstad L, Bjorn C. 2016. Antimicrobial peptides: an emerging category of therapeutic agents. Front. Cell. Infect. Microbiol. 6:194
    [Google Scholar]
  89. 89. 
    Manning AJ, Kuehn MJ. 2011. Contribution of bacterial outer membrane vesicles to innate bacterial defense. BMC Microbiol 11:258
    [Google Scholar]
  90. 90. 
    Marsollier L, Brodin P, Jackson M, Kordulakova J, Tafelmeyer P et al. 2007. Impact of Mycobacterium ulcerans biofilm on transmissibility to ecological niches and Buruli ulcer pathogenesis. PLOS Pathog 3:e62
    [Google Scholar]
  91. 91. 
    Matsumoto A, Huston SL, Killiny N, Igo MM. 2012. XatA, an AT-1 autotransporter important for the virulence of Xylellafastidiosa Temecula1. MicrobiologyOpen 1:33–45
    [Google Scholar]
  92. 92. 
    McKenzie AJ, Hoshino D, Hong NH, Cha DJ, Franklin JL et al. 2016. KRAS-MEK Signaling Controls Ago2 Sorting into Exosomes. Cell Rep 15:978–87
    [Google Scholar]
  93. 93. 
    McLoughlin AG, Wytinck N, Walker PL, Girard IJ, Rashid KY et al. 2018. Identification and application of exogenous dsRNA confers plant protection against Sclerotinia sclerotiorum and Botrytis cinerea. Sci. Rep. 8:7320
    [Google Scholar]
  94. 94. 
    Mendes JS, Santiago AS, Toledo MA, Horta MA, de Souza AA et al. 2016. In vitro determination of extracellular proteins from Xylella fastidiosa. Front. Microbiol 7:2090
    [Google Scholar]
  95. 95. 
    Meng WR, He CS, Hao YY, Wang LL, Li L, Zhu GQ. 2020. Prospects and challenges of extracellular vesicle-based drug delivery system: considering cell source. Drug Deliv 27:585–98
    [Google Scholar]
  96. 96. 
    Meng Z, Lu M. 2017. RNA interference-induced innate immunity, off-target effect, or immune adjuvant?. Front. Immunol. 8:331
    [Google Scholar]
  97. 97. 
    Micali CO, Neumann U, Grunewald D, Panstruga R, O'Connell R. 2011. Biogenesis of a specialized plant-fungal interface during host cell internalization of Golovinomyces orontii haustoria. Cell. Microbiol. 13:210–26
    [Google Scholar]
  98. 98. 
    Mitter N, Worrall EA, Robinson KE, Li P, Jain RG et al. 2017. Clay nanosheets for topical delivery of RNAi for sustained protection against plant viruses. Nat. Plants 3:16207
    [Google Scholar]
  99. 99. 
    Miyado K, Yoshida K, Yamagata K, Sakakibara K, Okabe M et al. 2008. The fusing ability of sperm is bestowed by CD9-containing vesicles released from eggs in mice. PNAS 105:12921–26
    [Google Scholar]
  100. 100. 
    Morra MR, Petty ITD. 2000. Tissue specificity of geminivirus infection is genetically determined. Plant Cell 12:2259–70
    [Google Scholar]
  101. 101. 
    Movahed N, Cabanillas DG, Wan J, Vali H, Laliberté JF, Zheng HQ. 2019. Turnip mosaic virus components are released into the extracellular space by vesicles in infected leaves. Plant Physiol 180:1375–88
    [Google Scholar]
  102. 102. 
    Mulcahy LA, Pink RC, Carter DR. 2014. Routes and mechanisms of extracellular vesicle uptake. J. Extracell. Vesicles 3:1 https://doi.org/10.3402/jev.v3.24641
    [Crossref] [Google Scholar]
  103. 103. 
    Namork E, Brandtzaeg P. 2002. Fatal meningococcal septicaemia with “blebbing” meningococcus. Lancet 360:P1741
    [Google Scholar]
  104. 104. 
    Nascimento R, Gouran H, Chakraborty S, Gillespie HW, Almeida-Souza HO et al. 2016. The type II secreted lipase/esterase LesA is a key virulence factor required for Xylella fastidiosa pathogenesis in grapevines. Sci. Rep. 6:18598
    [Google Scholar]
  105. 105. 
    Nielsen ME, Feechan A, Bohlenius H, Ueda T, Thordal-Christensen H 2012. Arabidopsis ARF-GTP exchange factor, GNOM, mediates transport required for innate immunity and focal accumulation of syntaxin PEN1. PNAS 109:11443–48
    [Google Scholar]
  106. 106. 
    Nielsen ME, Jürgens G, Thordal-Christensen H. 2017. VPS9a activates the Rab5 GTPase ARA7 to confer distinct pre- and postinvasive plant innate immunity. Plant Cell 29:1927–37
    [Google Scholar]
  107. 107. 
    Nowara D, Gay A, Lacomme C, Shaw J, Ridout C et al. 2010. HIGS: host-induced gene silencing in the obligate biotrophic fungal pathogen Blumeria graminis. Plant Cell 22:3130–41
    [Google Scholar]
  108. 108. 
    Ofir-Birin Y, Regev-Rudzki N. 2019. Extracellular vesicles in parasite survival. Science 363:817–18
    [Google Scholar]
  109. 109. 
    Oliveira DL, Nakayasu ES, Joffe LS, Guimaraes AJ, Sobreira TJ et al. 2010. Characterization of yeast extracellular vesicles: evidence for the participation of different pathways of cellular traffic in vesicle biogenesis. PLOS ONE 5:e11113
    [Google Scholar]
  110. 110. 
    Ozpolat B, Sood AK, Lopez-Berestein G. 2014. Liposomal siRNA nanocarriers for cancer therapy. Adv. Drug Deliver. Rev. 66:110–16
    [Google Scholar]
  111. 111. 
    Pan BT, Johnstone RM. 1983. Fate of the transferrin receptor during maturation of sheep reticulocytes in vitro: selective externalization of the receptor. Cell 33:967–77
    [Google Scholar]
  112. 112. 
    Panepinto J, Komperda K, Frases S, Park YD, Djordjevic JT et al. 2009. Sec6-dependent sorting of fungal extracellular exosomes and laccase of Cryptococcus neoformans. Mol. Microbiol. 71:1165–76
    [Google Scholar]
  113. 113. 
    Peng Z, Liu XJ, Zhang W, Zeng ZT, Liu ZF et al. 2020. Advances in the application, toxicity and degradation of carbon nanomaterials in environment: a review. Environ. Int. 134:105298
    [Google Scholar]
  114. 114. 
    Peres da Silva R, Puccia R, Rodrigues ML, Oliveira DL, Joffe LS et al. 2015. Extracellular vesicle-mediated export of fungal RNA. Sci. Rep. 5:7763
    [Google Scholar]
  115. 115. 
    Polack FP, Thomas SJ, Kitchin N, Absalon J, Gurtman A et al. 2020. Safety and efficacy of the BNT162b2 mRNA Covid-19 vaccine. N. Engl. J. Med. 383:2603–15
    [Google Scholar]
  116. 116. 
    Poulsen CP, Dilokpimol A, Mouille G, Burow M, Geshi N. 2014. Arabinogalactan glycosyltransferases target to a unique subcellular compartment that may function in unconventional secretion in plants. Traffic 15:1219–34
    [Google Scholar]
  117. 117. 
    Prado N, Alché JD, Casado-Vela J, Mas S, Villalba M et al. 2014. Nanovesicles are secreted during pollen germination and pollen tube growth: a possible role in fertilization. Mol. Plant 7:573–77
    [Google Scholar]
  118. 118. 
    Prado N, De Linares C, Sanz ML, Gamboa P, Villalba M et al. 2015. Pollensomes as natural vehicles for pollen allergens. J. Immunol. 195:445–49
    [Google Scholar]
  119. 119. 
    Prosser DC, Drivas TG, Maldonado-Baez L, Wendland B. 2011. Existence of a novel clathrin-independent endocytic pathway in yeast that depends on Rho1 and formin. J. Cell Biol. 195:657–71
    [Google Scholar]
  120. 120. 
    Qiao L, Lan C, Capriotti L, Ah-Fong A, Niño-Sánchez J et al. 2021. Spray-induced gene silencing for disease control is dependent on the efficiency of pathogen RNA uptake. Plant Biotechnol. J In press https://doi.org/10.1111/pbi.13589 This work shows that dsRNA uptake efficiencies varied among different types of eukaryotic microbes, and the majority of aggressive fungal pathogens can take up environmental RNAs efficiently.
    [Crossref] [Google Scholar]
  121. 121. 
    Quintana JF, Babayan SA, Buck AH. 2017. Small RNAs and extracellular vesicles in filarial nematodes: from nematode development to diagnostics. Parasite Immunol 39:e12395
    [Google Scholar]
  122. 122. 
    Regente M, Corti Monzon G, de la Canal L 2008. Phospholipids are present in extracellular fluids of imbibing sunflower seeds and are modulated by hormonal treatments. J. Exp. Bot. 59:553–62
    [Google Scholar]
  123. 123. 
    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. 68:5485–95
    [Google Scholar]
  124. 124. 
    Reichmuth AM, Oberli MA, Jaklenec A, Langer R, Blankschtein D. 2016. mRNA vaccine delivery using lipid nanoparticles. Ther. Deliv. 7:319–34
    [Google Scholar]
  125. 125. 
    Reiner AT, Somoza V. 2019. Extracellular vesicles as vehicles for the delivery of food bioactives. J. Agr. Food Chem. 67:2113–19
    [Google Scholar]
  126. 126. 
    Ren B, Wang X, Duan J, Ma J. 2019. Rhizobial tRNA-derived small RNAs are signal molecules regulating plant nodulation. Science 365:919–22
    [Google Scholar]
  127. 127. 
    Rivera J, Cordero RJ, Nakouzi AS, Frases S, Nicola A, Casadevall A 2010. Bacillus anthracis produces membrane-derived vesicles containing biologically active toxins. PNAS 107:19002–7
    [Google Scholar]
  128. 128. 
    Robinson D, Ding Y, Jiang LW. 2016. Unconventional protein secretion in plants: a critical assessment. Protoplasma 253:31–43
    [Google Scholar]
  129. 129. 
    Rodrigues ML, Nakayasu ES, Oliveira DL, Nimrichter L, Nosanchuk JD et al. 2008. Extracellular vesicles produced by Cryptococcus neoformans contain protein components associated with virulence. Eukaryot. Cell 7:58–67
    [Google Scholar]
  130. 130. 
    Rodrigues ML, Nimrichter L, Oliveira DL, Frases S, Miranda K et al. 2007. Vesicular polysaccharide export in Cryptococcus neoformans is a eukaryotic solution to the problem of fungal trans-cell wall transport. Eukaryot. Cell 6:48–59
    [Google Scholar]
  131. 131. 
    Rodrigues TB, Petrick JS. 2020. Safety considerations for humans and other vertebrates regarding agricultural uses of externally applied RNA molecules. Front. Plant Sci. 11:407
    [Google Scholar]
  132. 132. 
    Rome S. 2019. Biological properties of plant-derived extracellular vesicles. Food Funct 10:529–38
    [Google Scholar]
  133. 133. 
    Roovers J, De Jonghe P, Weckhuysen S. 2018. The therapeutic potential of RNA regulation in neurological disorders. Expert Opin. Ther. Targets 22:1017–28
    [Google Scholar]
  134. 134. 
    Roth R, Hillmer S, Funaya C, Chiapello M, Schumacher K et al. 2019. Arbuscular cell invasion coincides with extracellular vesicles and membrane tubules. Nat. Plants 5:204–11
    [Google Scholar]
  135. 135. 
    Rutter BD, Innes RW. 2017. Extracellular vesicles isolated from the leaf apoplast carry stress-response proteins. Plant Physiol 173:728–41
    [Google Scholar]
  136. 136. 
    Rybak K, Robatzek S. 2019. Functions of extracellular vesicles in immunity and virulence. Plant Physiol 179:1236–47
    [Google Scholar]
  137. 137. 
    Saleh MC, van Rij RP, Hekele A, Gillis A, Foley E et al. 2006. The endocytic pathway mediates cell entry of dsRNA to induce RNAi silencing. Nat. Cell Biol. 8:793–802
    [Google Scholar]
  138. 138. 
    Sanchez-Vallet A, Ramos B, Bednarek P, Lopez G, Pislewska-Bednarek M et al. 2010. Tryptophan-derived secondary metabolites in Arabidopsis thaliana confer non-host resistance to necrotrophic Plectosphaerella cucumerina fungi. Plant J 63:115–27
    [Google Scholar]
  139. 139. 
    Santangelo L, Giurato G, Cicchini C, Montaldo C, Mancone C et al. 2016. The RNA-binding protein SYNCRIP is a component of the hepatocyte exosomal machinery controlling microRNA sorting. Cell Rep 17:799–808
    [Google Scholar]
  140. 140. 
    Santiago AD, Mendes JS, dos Santos CA, de Toledo MA, Beloti LL et al. 2016. The antitoxin protein of a toxin-antitoxin system from Xylella fastidiosa is secreted via outer membrane vesicles. Front. Microbiol. 7:2030
    [Google Scholar]
  141. 141. 
    Schorey JS, Cheng Y, Singh PP, Smith VL. 2015. Exosomes and other extracellular vesicles in host–pathogen interactions. EMBO Rep 16:24–43
    [Google Scholar]
  142. 142. 
    Sercombe L, Veerati T, Moheimani F, Wu SY, Sood AK, Hua S. 2015. Advances and challenges of liposome assisted drug delivery. Front. Pharmacol. 6:286
    [Google Scholar]
  143. 143. 
    Shahid S, Kim G, Johnson NR, Wafula E, Wang F et al. 2018. MicroRNAs from the parasitic plant Cuscuta campestris target host messenger RNAs. Nature 553:82–85
    [Google Scholar]
  144. 144. 
    Sharpe HR, Gilbride C, Allen E, Belij-Rammerstorfer S, Bissett C et al. 2020. The early landscape of coronavirus disease 2019 vaccine development in the UK and rest of the world. Immunology 160:223–32
    [Google Scholar]
  145. 145. 
    Shurtleff MJ, Temoche-Diaz MM, Karfilis KV, Ri S, Schekman R. 2016. Y-box protein 1 is required to sort microRNAs into exosomes in cells and in a cell-free reaction. eLife 5:19276The authors show that an RNA-binding protein controls the secretion of exosomal miRNAs in vitro and in vivo.
    [Google Scholar]
  146. 146. 
    Shurtleff MJ, Temoche-Diaz MM, Schekman R 2018. Extracellular vesicles and cancer: caveat lector. Annu. Rev. Canc. Biol. 2:395–411
    [Google Scholar]
  147. 147. 
    Sidhu VK, Vorholter FJ, Niehaus K, Watt SA. 2008. Analysis of outer membrane vesicle associated proteins isolated from the plant pathogenic bacterium Xanthomonas campestris pv. campestris. BMC Microbiol 8:87
    [Google Scholar]
  148. 148. 
    Silva BM, Prados-Rosales R, Espadas-Moreno J, Wolf JM, Luque-Garcia JL et al. 2014. Characterization of Alternaria infectoria extracellular vesicles. Med. Mycol. 52:202–10
    [Google Scholar]
  149. 149. 
    Solé M, Scheibner F, Hoffmeister A-K, Hartmann N, Hause G et al. 2015. Xanthomonas campestris pv. vesicatoria secretes proteases and xylanases via the Xps type II secretion system and outer membrane vesicles. J. Bacteriol. 197:2879–93
    [Google Scholar]
  150. 150. 
    Tayler A, Heschuk D, Giesbrecht D, Park JY, Whyard S. 2019. Efficiency of RNA interference is improved by knockdown of dsRNA nucleases in tephritid fruit flies. Open. Biol. 9:190198
    [Google Scholar]
  151. 151. 
    Temoche-Diaz MM, Shurtleff MJ, Nottingham RM, Yao J, Fadadu RP et al. 2019. Distinct mechanisms of microRNA sorting into cancer cell-derived extracellular vesicle subtypes. eLife 8:e47544
    [Google Scholar]
  152. 152. 
    Tenllado F, Díaz-Ruíz JR. 2001. Double-stranded RNA-mediated interference with plant virus infection. J. Virol. 75:12288–97
    [Google Scholar]
  153. 153. 
    Thanh Le T, Andreadakis Z, Kumar A, Gómez Román R, Tollefsen S et al. 2020. The COVID-19 vaccine development landscape. Nat. Rev. Drug Discov. 19:305–6
    [Google Scholar]
  154. 154. 
    Théry C, Amigorena S, Raposo G, Clayton A 2006. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr. Protoc. Cell Biol. 30:3.22.1–29
    [Google Scholar]
  155. 155. 
    Théry C, Witwer KW, Aikawa E, Alcaraz MJ, Anderson JD et al. 2018. Minimal information for studies of extracellular vesicles 2018 (MISEV2018): a position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines. J. Extracell. Vesicles 7:1535750
    [Google Scholar]
  156. 156. 
    Toruño TY, Stergiopoulos I, Coaker G. 2016. Plant–pathogen effectors: cellular probes interfering with plant defenses in spatial and temporal manners. Annu. Rev. Phytopathol. 54:419–41
    [Google Scholar]
  157. 157. 
    Unal CM, Schaar V, Riesbeck K. 2011. Bacterial outer membrane vesicles in disease and preventive medicine. Semin. Immunopathol. 33:395–408
    [Google Scholar]
  158. 158. 
    Vader P, Mol EA, Pasterkamp G, Schiffelers RM. 2016. Extracellular vesicles for drug delivery. Adv. Drug Deliver. Rev. 106:148–56
    [Google Scholar]
  159. 159. 
    Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO. 2007. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol. 9:654–59
    [Google Scholar]
  160. 160. 
    Vallejo MC, Matsuo AL, Ganiko L, Medeiros LCS, Miranda K et al. 2011. The pathogenic fungus Paracoccidioides brasiliensis exports extracellular vesicles containing highly immunogenic α-Galactosyl epitopes. Eukaryot. Cell 10:343–51
    [Google Scholar]
  161. 161. 
    van der Meel R, Fens MHAM, Vader P, van Solinge WW, Eniola-Adefeso O, Schiffelers RM. 2014. Extracellular vesicles as drug delivery systems: lessons from the liposome field. J. Control Release 195:72–85
    [Google Scholar]
  162. 162. 
    van Niel G, D'Angelo G, Raposo G 2018. Shedding light on the cell biology of extracellular vesicles. Nat. Rev. Mol. Cell Bio. 19:213–28
    [Google Scholar]
  163. 163. 
    Vargas G, Rocha JD, Oliveira DL, Albuquerque PC, Frases S et al. 2015. Compositional and immunobiological analyses of extracellular vesicles released by Candida albicans. Cell. Microbiol. 17:389–407
    [Google Scholar]
  164. 164. 
    Villarroya-Beltri C, Baixauli F, Gutierrez-Vazquez C, Sanchez-Madrid F, Mittelbrunn M. 2014. Sorting it out: Regulation of exosome loading. Semin. Cancer Biol. 28:3–13
    [Google Scholar]
  165. 165. 
    Villarroya-Beltri C, Gutiérrez-Vázquez C, Sánchez-Cabo F, Pérez-Hernández D, Vázquez J et al. 2013. Sumoylated hnRNPA2B1 controls the sorting of miRNAs into exosomes through binding to specific motifs. Nat. Commun. 4:2980
    [Google Scholar]
  166. 166. 
    Walker L, Sood P, Lenardon MD, Milne G, Olson J et al. 2018. The viscoelastic properties of the fungal cell wall allow traffic of AmBisome as intact liposome vesicles. mBio 9:e02383–17
    [Google Scholar]
  167. 167. 
    Wang B, Sun YF, Song N, Zhao MX, Liu R et al. 2017. Puccinia striiformis f. sp tritici microRNA-like RNA 1 (Pst-milR1), an important pathogenicity factor of Pst, impairs wheat resistance to Pst by suppressing the wheat pathogenesis-related 2 gene. New Phytol 215:338–50
    [Google Scholar]
  168. 168. 
    Wang F, Muto A, Van de Velde J, Neyt P, Himanen K et al. 2015. Functional analysis of the Arabidopsis TETRASPANIN gene family in plant growth and development. Plant Physiol 169:2200–14
    [Google Scholar]
  169. 169. 
    Wang F, Shang Y, Fan B, Yu JQ, Chen Z 2014. Arabidopsis LIP5, a positive regulator of multivesicular body biogenesis, is a critical target of pathogen-responsive MAPK cascade in plant basal defense. PLOS Pathog 10:e1004243
    [Google Scholar]
  170. 170. 
    Wang J, Ding Y, Wang J, Hillmer S, Miao Y et al. 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 22:4009–30
    [Google Scholar]
  171. 171. 
    Wang J, Lu Z, Wientjes MG, Au JLS. 2010. Delivery of siRNA therapeutics: barriers and carriers. AAPS J 12:492–503
    [Google Scholar]
  172. 172. 
    Wang K, Peng Y, Chen J, Peng Y, Wang X et al. 2020. Comparison of efficacy of RNAi mediated by various nanoparticles in the rice striped stem borer (Chilo suppressalis). Pesticide Biochem. Physiol. 165:104467
    [Google Scholar]
  173. 173. 
    Wang M, Jin HL. 2017. Spray-induced gene silencing: a powerful innovative strategy for crop protection. Trends Microbiol 25:4–6
    [Google Scholar]
  174. 174. 
    Wang M, Thomas N, Jin H. 2017. Cross-kingdom RNA trafficking and environmental RNAi for powerful innovative pre- and post-harvest plant protection. Curr. Opin. Plant Biol. 38:133–41
    [Google Scholar]
  175. 175. 
    Wang M, Weiberg A, Lin F-M, Thomma BP, Huang H-D, Jin H 2016. Bidirectional cross-kingdom RNAi and fungal uptake of external RNAs confer plant protection. Nat. Plants 2:16151This is the first study that demonstrated fungal RNA uptake from environment.
    [Google Scholar]
  176. 176. 
    Wang QL, Zhuang XY, Mu JY, Deng Z-B, Jiang H et al. 2013. Delivery of therapeutic agents by nanoparticles made of grapefruit-derived lipids. Nat. Commun. 4:1867
    [Google Scholar]
  177. 177. 
    Weiberg A, Bellinger M, Jin H 2015. Conversations between kingdoms: small RNAs. Curr. Opin. Biotechnol. 32:207–15
    [Google Scholar]
  178. 178. 
    Weiberg A, Jin H 2015. Small RNAs—the secret agents in the plant–pathogen interactions. Curr. Opin. Plant Biol. 26:87–94
    [Google Scholar]
  179. 179. 
    Weiberg A, Wang M, Bellinger M, Jin H 2014. Small RNAs: a new paradigm in plant-microbe interactions. Annu. Rev. Phytopathol. 52:495–516
    [Google Scholar]
  180. 180. 
    Weiberg A, Wang M, Lin FM, Zhao H, Zhang Z et al. 2013. Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. Science 342:118–23The first report of naturally occurring cross-kingdom RNAi being employed as an aggressive virulence mechanism by pathogens.
    [Google Scholar]
  181. 181. 
    Woith E, Fuhrmann G, Melzig MF. 2019. Extracellular vesicles—connecting kingdoms. Int. J. Mol. Sci. 20:5695
    [Google Scholar]
  182. 182. 
    Worrall EA, Bravo-Cazar A, Nilon AT, Fletcher SJ, Robinson KE et al. 2019. Exogenous application of RNAi-inducing double-stranded RNA inhibits aphid-mediated transmission of a plant virus. Front. Plant Sci. 10:265
    [Google Scholar]
  183. 183. 
    Wytinck N, Sullivan DS, Biggar KT, Crisostomo L, Pelka P et al. 2020. Clathrin mediated endocytosis is involved in the uptake of exogenous double-stranded RNA in the white mold phytopathogen Sclerotinia sclerotiorum. Sci. Rep. 10:12773
    [Google Scholar]
  184. 184. 
    Xiao D, Gao X, Xu J, Liang X, Li Q et al. 2015. Clathrin-dependent endocytosis plays a predominant role in cellular uptake of double-stranded RNA in the red flour beetle. Insect Biochem. Mol. Biol. 60:68–77
    [Google Scholar]
  185. 185. 
    Xin XF, Nomura K, Underwood W, He SY. 2013. Induction and suppression of PEN3 focal accumulation during Pseudomonas syringae pv. tomato DC3000 infection of Arabidopsis. Mol. Plant Microbe Interact 26:861–67
    [Google Scholar]
  186. 186. 
    Yokoi A, Yoshioka Y, Yamamoto Y, Ishikawa M, Ikeda SI et al. 2017. Malignant extracellular vesicles carrying MMP1 mRNA facilitate peritoneal dissemination in ovarian cancer. Nat. Commun. 8:14470
    [Google Scholar]
  187. 187. 
    Zamith-Miranda D, Nimrichter L, Rodrigues ML, Nosanchuk JD. 2018. Fungal extracellular vesicles: modulating host–pathogen interactions by both the fungus and the host. Microbes Infect 20:501–4
    [Google Scholar]
  188. 188. 
    Zhang J, Khan SA, Hasse C, Ruf S, Heckel DG, Bock R. 2015. Full crop protection from an insect pest by expression of long double-stranded RNAs in plastids. Science 347:991–94
    [Google Scholar]
  189. 189. 
    Zhang J, Li S, Li L, Li M, Guo C et al. 2015. Exosome and exosomal microRNA: trafficking, sorting, and function. Genom. Proteom. Bioinformat. 13:17–24
    [Google Scholar]
  190. 190. 
    Zhang T, Zhao YL, Zhao JH, Wang S, Jin Y et al. 2016. Cotton plants export microRNAs to inhibit virulence gene expression in a fungal pathogen. Nat. Plants 2:16153
    [Google Scholar]
  191. 191. 
    Zhao KN, Bleackley M, Chisanga D, Gangoda L, Fonseka P et al. 2019. Extracellular vesicles secreted by Saccharomyces cerevisiae are involved in cell wall remodelling. Commun. Biol. 2:305
    [Google Scholar]
  192. 192. 
    Zhuang XY, Teng Y, Samykutty A, Mu JY, Deng ZB et al. 2016. Grapefruit-derived nanovectors delivering therapeutic miR17 through an intranasal route inhibit brain tumor progression. Mol. Ther. 24:96–105
    [Google Scholar]
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