A rhabdovirus accessory protein inhibits jasmonic acid signaling in plants to attract insect vectors.


Journal

Plant physiology
ISSN: 1532-2548
Titre abrégé: Plant Physiol
Pays: United States
ID NLM: 0401224

Informations de publication

Date de publication:
28 09 2022
Historique:
received: 09 09 2021
accepted: 13 06 2022
pubmed: 1 7 2022
medline: 30 9 2022
entrez: 30 6 2022
Statut: ppublish

Résumé

Plant rhabdoviruses heavily rely on insect vectors for transmission between sessile plants. However, little is known about the underlying mechanisms of insect attraction and transmission of plant rhabdoviruses. In this study, we used an arthropod-borne cytorhabdovirus, Barley yellow striate mosaic virus (BYSMV), to demonstrate the molecular mechanisms of a rhabdovirus accessory protein in improving plant attractiveness to insect vectors. Here, we found that BYSMV-infected barley (Hordeum vulgare L.) plants attracted more insect vectors than mock-treated plants. Interestingly, overexpression of BYSMV P6, an accessory protein, in transgenic wheat (Triticum aestivum L.) plants substantially increased host attractiveness to insect vectors through inhibiting the jasmonic acid (JA) signaling pathway. The BYSMV P6 protein interacted with the constitutive photomorphogenesis 9 signalosome subunit 5 (CSN5) of barley plants in vivo and in vitro, and negatively affected CSN5-mediated deRUBylation of cullin1 (CUL1). Consequently, the defective CUL1-based Skp1/Cullin1/F-box ubiquitin E3 ligases could not mediate degradation of jasmonate ZIM-domain proteins, resulting in compromised JA signaling and increased insect attraction. Overexpression of BYSMV P6 also inhibited JA signaling in transgenic Arabidopsis (Arabidopsis thaliana) plants to attract insects. Our results provide insight into how a plant cytorhabdovirus subverts plant JA signaling to attract insect vectors.

Identifiants

pubmed: 35771641
pii: 6623419
doi: 10.1093/plphys/kiac319
pmc: PMC9516739
doi:

Substances chimiques

Cyclopentanes 0
Oxylipins 0
Proteins 0
Ubiquitins 0
jasmonic acid 6RI5N05OWW
COP9 Signalosome Complex EC 3.4.19.12

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

1349-1364

Informations de copyright

© American Society of Plant Biologists 2022. All rights reserved. For permissions, please email: journals.permissions@oup.com.

Références

Elife. 2020 Mar 24;9:
pubmed: 32207684
Annu Rev Phytopathol. 2005;43:623-60
pubmed: 16078897
Plant Cell. 2004 Nov;16(11):2984-3001
pubmed: 15486099
Plant Sci. 2014 Jul;224:54-61
pubmed: 24908506
J Exp Bot. 2019 Aug 7;70(15):4049-4062
pubmed: 31020313
Plant Cell Physiol. 2019 Dec 1;60(12):2638-2647
pubmed: 31418777
Plant Cell. 2003 May;15(5):1083-94
pubmed: 12724535
PLoS Pathog. 2019 Feb 21;15(2):e1007607
pubmed: 30789967
Viruses. 2020 Jan 27;12(2):
pubmed: 32012772
Mol Plant Microbe Interact. 2020 Mar;33(3):382-393
pubmed: 31914364
Development. 2009 Mar;136(6):1039-48
pubmed: 19234066
Plant J. 2002 Aug;31(3):375-83
pubmed: 12164816
Curr Opin Virol. 2021 Jun;48:1-9
pubmed: 33774424
Mol Plant Microbe Interact. 2010 Jul;23(7):835-45
pubmed: 20521947
Plant Cell. 2020 Sep;32(9):2878-2897
pubmed: 32641349
Science. 1998 May 15;280(5366):1091-4
pubmed: 9582125
Plant Physiol. 2003 Nov;133(3):1367-75
pubmed: 14551332
Plant J. 2004 Nov;40(3):428-38
pubmed: 15469500
Annu Rev Phytopathol. 2016 Aug 4;54:469-98
pubmed: 27359368
New Phytol. 2019 Sep;223(4):2120-2133
pubmed: 31059138
Plant Cell. 2003 Jan;15(1):165-78
pubmed: 12509529
Nature. 2007 Aug 9;448(7154):661-5
pubmed: 17637677
J Exp Bot. 2020 Oct 22;71(20):6684-6696
pubmed: 32865553
Curr Opin Virol. 2018 Dec;33:198-207
pubmed: 30500682
PLoS Pathog. 2015 Oct 20;11(10):e1005223
pubmed: 26484673
Plant Cell. 2014 Dec;26(12):4991-5008
pubmed: 25490915
PLoS Genet. 2012;8(5):e1002712
pubmed: 22589747
Plant Physiol. 2015 Sep;169(1):209-18
pubmed: 26091820
Plant Biotechnol J. 2021 Feb;19(2):375-393
pubmed: 32888338
Curr Opin Virol. 2018 Dec;33:144-150
pubmed: 30223172
Front Plant Sci. 2019 Sep 17;10:1095
pubmed: 31608079
Plant Physiol. 2007 Feb;143(2):684-96
pubmed: 17158585
J Exp Bot. 2019 Jul 5;70(13):3391-3400
pubmed: 30976791
PLoS Pathog. 2019 Jun 17;15(6):e1007897
pubmed: 31206553
Science. 2001 May 18;292(5520):1379-82
pubmed: 11337587
J Chem Ecol. 2018 Aug;44(7-8):681-689
pubmed: 29858747
Methods Mol Biol. 2022;2400:163-170
pubmed: 34905200
Plant Cell. 2004 Jul;16(7):1938-50
pubmed: 15208388
Mol Plant Pathol. 2022 May;23(5):749-756
pubmed: 35124878
Virus Res. 2011 Dec;162(1-2):110-25
pubmed: 21933691
Plant Cell. 2007 Feb;19(2):564-81
pubmed: 17307927
Mol Plant Microbe Interact. 2020 Oct;33(10):1209-1221
pubmed: 32815767
BMC Plant Biol. 2018 Jun 25;18(1):134
pubmed: 29940863
Nat Plants. 2021 Jan;7(1):6-16
pubmed: 33452490
Mol Ecol. 2012 Mar;21(5):1294-304
pubmed: 22269032
Mol Plant Microbe Interact. 2010 Nov;23(11):1420-32
pubmed: 20923350
Insect Biochem Mol Biol. 2022 Jan;140:103703
pubmed: 34933088
J Exp Bot. 2017 Mar 1;68(6):1303-1321
pubmed: 27940470
J Virol. 2005 Feb;79(4):2108-14
pubmed: 15681413
J Exp Bot. 2017 Mar 1;68(6):1371-1385
pubmed: 28069779
Arch Virol. 2014 Aug;159(8):1889-900
pubmed: 24610553
Virology. 2015 Apr;478:112-22
pubmed: 25666524
Sci Rep. 2015 Jun 04;5:10963
pubmed: 26043237
Mol Cancer Res. 2007 Oct;5(10):1063-72
pubmed: 17951406
Annu Rev Entomol. 2009;54:447-68
pubmed: 18793103
Cell Res. 2017 Mar;27(3):402-415
pubmed: 28059067
Plant Cell. 2011 Mar;23(3):1014-32
pubmed: 21441437
Curr Opin Plant Biol. 2014 Oct;21:112-119
pubmed: 25064075
J Biol Chem. 2006 Oct 6;281(40):30166-74
pubmed: 16882664
Comp Med. 2017 Jun 1;67(3):232-241
pubmed: 28662752
Nature. 2007 Aug 9;448(7154):666-71
pubmed: 17637675
BMC Plant Biol. 2018 Oct 29;18(1):260
pubmed: 30373512
Insect Sci. 2017 Dec;24(6):929-946
pubmed: 28426155
Elife. 2022 Feb 22;11:
pubmed: 35191833
Oncogene. 2006 Jan 26;25(4):633-42
pubmed: 16247477
Plant Cell. 2022 Jul 30;34(8):3110-3127
pubmed: 35567529
New Phytol. 2011 Jun;190(4):1069-1080
pubmed: 21561458
Front Microbiol. 2018 Jun 29;9:1419
pubmed: 30008708
Annu Rev Plant Biol. 2018 Apr 29;69:387-415
pubmed: 29539269
Virus Res. 2009 May;141(2):158-68
pubmed: 19152819
EMBO J. 2021 Aug 2;40(15):e108050
pubmed: 34155657
Proc Natl Acad Sci U S A. 2020 Jan 14;117(2):1181-1190
pubmed: 31879355
J Virol. 2019 Jul 17;93(15):
pubmed: 31118256
New Phytol. 2020 Jan;225(2):896-912
pubmed: 31318448

Auteurs

Dong-Min Gao (DM)

State Key Laboratory of Agro-Biotechnology, College of Biological Sciences, China Agricultural University, Beijing 100193, China.

Zhen-Jia Zhang (ZJ)

State Key Laboratory of Agro-Biotechnology, College of Biological Sciences, China Agricultural University, Beijing 100193, China.

Ji-Hui Qiao (JH)

State Key Laboratory of Agro-Biotechnology, College of Biological Sciences, China Agricultural University, Beijing 100193, China.

Qiang Gao (Q)

State Key Laboratory of Agro-Biotechnology, College of Biological Sciences, China Agricultural University, Beijing 100193, China.
College of Plant Protection, China Agricultural University, Beijing 100193, China.

Ying Zang (Y)

State Key Laboratory of Agro-Biotechnology, College of Biological Sciences, China Agricultural University, Beijing 100193, China.

Wen-Ya Xu (WY)

State Key Laboratory of Agro-Biotechnology, College of Biological Sciences, China Agricultural University, Beijing 100193, China.

Liang Xie (L)

State Key Laboratory of Agro-Biotechnology, College of Biological Sciences, China Agricultural University, Beijing 100193, China.

Xiao-Dong Fang (XD)

State Key Laboratory of Agro-Biotechnology, College of Biological Sciences, China Agricultural University, Beijing 100193, China.

Zhi-Hang Ding (ZH)

State Key Laboratory of Agro-Biotechnology, College of Biological Sciences, China Agricultural University, Beijing 100193, China.

Yi-Zhou Yang (YZ)

State Key Laboratory of Agro-Biotechnology, College of Biological Sciences, China Agricultural University, Beijing 100193, China.

Ying Wang (Y)

College of Plant Protection, China Agricultural University, Beijing 100193, China.

Xian-Bing Wang (XB)

State Key Laboratory of Agro-Biotechnology, College of Biological Sciences, China Agricultural University, Beijing 100193, China.

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