Exosomes mediate horizontal transmission of viral pathogens from insect vectors to plant phloem.


Journal

eLife
ISSN: 2050-084X
Titre abrégé: Elife
Pays: England
ID NLM: 101579614

Informations de publication

Date de publication:
02 07 2021
Historique:
received: 04 11 2020
accepted: 21 06 2021
entrez: 2 7 2021
pubmed: 3 7 2021
medline: 23 9 2021
Statut: epublish

Résumé

Numerous piercing-sucking insects can horizontally transmit viral pathogens together with saliva to plant phloem, but the mechanism remains elusive. Here, we report that an important rice reovirus has hijacked small vesicles, referred to as exosomes, to traverse the apical plasmalemma into saliva-stored cavities in the salivary glands of leafhopper vectors. Thus, virions were horizontally transmitted with exosomes into rice phloem to establish the initial plant infection during vector feeding. The purified exosomes secreted from cultured leafhopper cells were enriched with virions. Silencing the exosomal secretion-related small GTPase Rab27a or treatment with the exosomal biogenesis inhibitor GW4869 strongly prevented viral exosomal release in vivo and in vitro. Furthermore, the specific interaction of the 15-nm-long domain of the viral outer capsid protein with Rab5 induced the packaging of virions in exosomes, ultimately activating the Rab27a-dependent exosomal release pathway. We thus anticipate that exosome-mediated viral horizontal transmission is the conserved strategy hijacked by vector-borne viruses.

Identifiants

pubmed: 34214032
doi: 10.7554/eLife.64603
pii: 64603
pmc: PMC8253596
doi:
pii:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : National Natural Science Foundation of China
ID : 31772124
Organisme : National Natural Science Foundation of China
ID : 31920103014
Organisme : National Natural Science Foundation of China
ID : 31972239

Informations de copyright

© 2021, Chen et al.

Déclaration de conflit d'intérêts

QC, YL, JR, PZ, MC, DJ, HC, TW No competing interests declared

Références

Nat Rev Mol Cell Biol. 2013 Nov;14(11):699-712
pubmed: 24105322
Eur J Cell Biol. 1993 Apr;60(2):261-7
pubmed: 8330623
Plant Physiol. 2008 Aug;147(4):1516-26
pubmed: 18678743
Traffic. 2008 Sep;9(10):1728-42
pubmed: 18637904
Adv Virus Res. 2014;89:141-99
pubmed: 24751196
J Virol. 2007 Jul;81(14):7811-5
pubmed: 17475659
Proc Natl Acad Sci U S A. 2004 Sep 7;101(36):13368-73
pubmed: 15326289
Elife. 2021 Jul 02;10:
pubmed: 34214032
J Virol. 2014 Nov;88(22):13460-8
pubmed: 25210181
Commun Integr Biol. 2009 Jul;2(4):324-6
pubmed: 19721879
Nat Cell Biol. 2010 Jan;12(1):19-30; sup pp 1-13
pubmed: 19966785
Mol Phylogenet Evol. 2017 Apr;109:343-350
pubmed: 28189616
J Virol. 2017 Oct 27;91(22):
pubmed: 28878075
Cell. 1991 Mar 8;64(5):915-25
pubmed: 1900457
Annu Rev Biochem. 2010;79:803-33
pubmed: 20196649
PLoS One. 2009;4(4):e5219
pubmed: 19381331
J Immunol. 2010 Jan 1;184(1):236-43
pubmed: 19949097
Viruses. 2015 Jun 19;7(6):3204-25
pubmed: 26102580
J Gen Virol. 2008 Nov;89(Pt 11):2915-2920
pubmed: 18931091
FEBS Lett. 2015 Jun 4;589(13):1391-8
pubmed: 25937124
J Biochem. 2016 Feb;159(2):181-90
pubmed: 26374901
J Virol. 2017 May 26;91(12):
pubmed: 28381575
J Virol. 2006 Sep;80(17):8593-602
pubmed: 16912308
Nature. 2017 May 25;545(7655):482-486
pubmed: 28514450
PLoS Pathog. 2019 Jan 17;15(1):e1007510
pubmed: 30653614
Science. 2020 Feb 7;367(6478):
pubmed: 32029601
Proc Natl Acad Sci U S A. 2018 Jul 10;115(28):E6604-E6613
pubmed: 29946031
Can J Microbiol. 1970 Jul;16(7):581-6
pubmed: 4097196
Micron. 2010 Oct;41(7):754-9
pubmed: 20591681
Wiley Interdiscip Rev RNA. 2017 Jul;8(4):
pubmed: 28130830
Science. 2018 Jun 8;360(6393):1126-1129
pubmed: 29773668
J Neurooncol. 2013 May;113(1):1-11
pubmed: 23456661
J Biol Chem. 2003 Dec 26;278(52):52347-54
pubmed: 14561735
Annu Rev Phytopathol. 2016 Aug 4;54:99-120
pubmed: 27296147
Acta Trop. 2017 Feb;166:155-163
pubmed: 27876643
J Gen Virol. 2006 Feb;87(Pt 2):429-438
pubmed: 16432031
Cells. 2020 Jan 04;9(1):
pubmed: 31947958
Proc Natl Acad Sci U S A. 2007 Dec 4;104(49):19547-52
pubmed: 18042708
Virology. 1965 Dec;27(4):461-75
pubmed: 5855567
Annu Rev Phytopathol. 2008;46:327-59
pubmed: 18680428
Curr Opin Plant Biol. 2018 Aug;44:16-22
pubmed: 29452903
Cell Rep. 2015 May 12;11(6):884-892
pubmed: 25937276
Nature. 1998 Jul 30;394(6692):494-8
pubmed: 9697774
Proc Natl Acad Sci U S A. 2012 Jul 10;109(28):11443-8
pubmed: 22733775
Nat Microbiol. 2017 Mar 06;2:17025
pubmed: 28263320
Nat Commun. 2019 Apr 9;10(1):1639
pubmed: 30967557
Plant Physiol. 2019 Jul;180(3):1375-1388
pubmed: 31019004
Intervirology. 1985;24(1):33-41
pubmed: 4044200
Annu Rev Phytopathol. 2003;41:539-66
pubmed: 12730400
Virus Res. 2019 Jun;266:1-14
pubmed: 30930201
Viruses. 2015 Sep 17;7(9):5066-83
pubmed: 26393640
Annu Rev Entomol. 2018 Jan 7;63:169-191
pubmed: 28968147
Proc Natl Acad Sci U S A. 2013 Aug 6;110(32):13109-13
pubmed: 23878230
Arthropod Struct Dev. 2003 Oct;32(2-3):189-99
pubmed: 18089004
Nat Cell Biol. 1999 Oct;1(6):376-82
pubmed: 10559966
J Cell Biol. 2003 May 12;161(3):609-24
pubmed: 12743108

Auteurs

Qian Chen (Q)

Vector-borne Virus Research Center, Fujian Province Key Laboratory of Plant Virology, Institute of Plant Virology, Fujian Agriculture and Forestry University, Fuzhou, China.

Yuyan Liu (Y)

Vector-borne Virus Research Center, Fujian Province Key Laboratory of Plant Virology, Institute of Plant Virology, Fujian Agriculture and Forestry University, Fuzhou, China.

Jiping Ren (J)

Vector-borne Virus Research Center, Fujian Province Key Laboratory of Plant Virology, Institute of Plant Virology, Fujian Agriculture and Forestry University, Fuzhou, China.

Panpan Zhong (P)

Vector-borne Virus Research Center, Fujian Province Key Laboratory of Plant Virology, Institute of Plant Virology, Fujian Agriculture and Forestry University, Fuzhou, China.

Manni Chen (M)

Vector-borne Virus Research Center, Fujian Province Key Laboratory of Plant Virology, Institute of Plant Virology, Fujian Agriculture and Forestry University, Fuzhou, China.

Dongsheng Jia (D)

Vector-borne Virus Research Center, Fujian Province Key Laboratory of Plant Virology, Institute of Plant Virology, Fujian Agriculture and Forestry University, Fuzhou, China.

Hongyan Chen (H)

Vector-borne Virus Research Center, Fujian Province Key Laboratory of Plant Virology, Institute of Plant Virology, Fujian Agriculture and Forestry University, Fuzhou, China.

Taiyun Wei (T)

Vector-borne Virus Research Center, Fujian Province Key Laboratory of Plant Virology, Institute of Plant Virology, Fujian Agriculture and Forestry University, Fuzhou, China.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH