A plant RNA virus activates selective autophagy in a UPR-dependent manner to promote virus infection.
RNA-dependent RNA polymerase (RdRp)
autophagy
potyvirus
tonoplast
turnip mosaic virus (TuMV)
unfolded protein response (UPR)
vacuole
virus replication complex (VRC)
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
10 2020
10 2020
Historique:
received:
28
03
2020
accepted:
18
05
2020
pubmed:
2
6
2020
medline:
15
5
2021
entrez:
2
6
2020
Statut:
ppublish
Résumé
Autophagy is an evolutionarily conserved pathway in eukaryotes that delivers unwanted cytoplasmic materials to the lysosome/vacuole for degradation/recycling. Stimulated autophagy emerges as an integral part of plant immunity against intracellular pathogens. In this study, we used turnip mosaic virus (TuMV) as a model to investigate the involvement of autophagy in plant RNA virus infection. The small integral membrane protein 6K2 of TuMV, known as a marker of the virus replication site and an elicitor of the unfolded protein response (UPR), upregulates the selective autophagy receptor gene NBR1 in a UPR-dependent manner. NBR1 interacts with TuMV NIb, the RNA-dependent RNA polymerase of the virus replication complex (VRC), and the autophagy cargo receptor/adaptor protein ATG8f. The NIb/NBR1/ATG8f interaction complexes colocalise with the 6K2-stained VRC. Overexpression of NBR1 or ATG8f enhances TuMV replication, and deficiency of NBR1 or ATG8f inhibits virus infection. In addition, ATG8f interacts with the tonoplast-specific protein TIP1 and the NBR1/ATG8f-containing VRC is enclosed by the TIP1-labelled tonoplast. In TuMV-infected cells, numerous membrane-bound viral particles are evident in the vacuole. Altogether these results suggest that TuMV activates and manipulates UPR-dependent NBR1-ATG8f autophagy to target the VRC to the tonoplast to promote viral replication and virion accumulation.
Substances chimiques
Arabidopsis Proteins
0
Carrier Proteins
0
NBR1 protein, Arabidopsis
0
RNA, Plant
0
Viral Proteins
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
622-639Informations de copyright
© 2020 Her Majesty the Queen in Right of Canada New Phytologist © 2020 New Phytologist Trust.
Références
Beebo A, Thomas D, Der C, Sanchez L, Leborgne-Castel N, Marty F, Schoefs B, Bouhidel K. 2009. Life with and without AtTIP1;1, an Arabidopsis aquaporin preferentially localized in the apposing tonoplasts of adjacent vacuoles. Plant Molecular Biology 70: 193-209.
Bhardwaj M, Leli NM, Koumenis C, Amaravadi RK. 2019. Regulation of autophagy by canonical and non-canonical ER stress responses. Seminars in Cancer Biology, doi: 10.1016/j.semcancer.2019.11.007.
Brugidou C, Opalka N, Yeager M, Beachy RN, Fauquet C. 2002. Stability of rice yellow mottle virus and cellular compartmentalization during the infection process in Oryza sativa (L.). Virology 297: 98-108.
Cabanillas DG, Jiang J, Movahed N, Germain H, Yamaji Y, Zheng H, Laliberté JF. 2018. Turnip mosaic virus uses the SNARE protein VTI11 in an unconventional route for replication vesicle trafficking. The Plant Cell 30: 2594-2615.
Cheng X, Deng P, Cui H, Wang A. 2015. Visualizing double-stranded RNA distribution and dynamics in living cells by dsRNA binding-dependent fluorescence complementation. Virology 485: 439-451.
Cheng X, Wang A. 2017. The potyvirus silencing suppressor protein VPg mediates degradation of SGS3 via ubiquitination and autophagy pathways. Journal of Virology 91: e01478-01416.
Cheng X, Xiong R, Li Y, Li F, Zhou X, Wang A. 2017. Sumoylation of Turnip mosaic virus RNA polymerase promotes viral infection by counteracting the host NPR1-mediated immune response. The Plant Cell 29: 508-525.
Clavel M, Michaeli S, Genschik P. 2017. Autophagy: a double-edged sword to fight plant viruses. Trends Plant Science 22: 646-648.
Clough SJ, Bent AF. 1998. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant Journal 16: 735-743.
Cotton S, Grangeon R, Thivierge K, Mathieu I, Ide C, Wei T, Wang A, Laliberté JF. 2009. Turnip mosaic virus RNA replication complex vesicles are mobile, align with microfilaments, and are each derived from a single viral genome. Journal of Virology 83: 10460-10471.
Cui H, Wang A. 2016. The Plum pox virus 6K1 protein is required for viral replication and targets the viral replication complex at the early infection stage. Journal of Virology 90: 5119-5131.
Cui H, Wang A. 2019. The biological impact of the hypervariable N-terminal region of potyviral genomes. Annual Review of Virology 6: 255-274.
Daròs JA, Schaad MC, Carrington JC. 1999. Functional analysis of the interaction between VPg-proteinase (NIa) and RNA polymerase (NIb) of tobacco etch potyvirus, using conditional and suppressor mutants. Journal of Virology 73: 8732-8740.
Deng P, Wu Z, Wang A. 2015. The multifunctional protein CI of potyviruses plays interlinked and distinct roles in viral genome replication and intercellular movement. Virology Journal 12: 141.
Derrien B, Baumberger N, Schepetilnikov M, Viotti C, De Cillia J, Ziegler-Graff V, Isono E, Schumacher K, Genschik P. 2012. Degradation of the antiviral component ARGONAUTE1 by the autophagy pathway. Proceedings of the National Academy of Sciences, USA 109: 15942-15946.
Earley KW, Haag JR, Pontes O, Opper K, Juehne T, Song K, Pikaard CS. 2006. Gateway-compatible vectors for plant functional genomics and proteomics. The Plant Journal 45: 616-629.
Fu S, Xu Y, Li C, Li Y, Wu J, Zhou X. 2018. Rice stripe virus interferes with S-acylation of remorin and induces its autophagic degradation to facilitate virus infection. Molecular Plant 11: 269-287.
Gaguancela OA, Zúñiga LP, Arias AV, Halterman D, Flores FJ, Johansen IE, Wang A, Yamaji Y, Verchot J. 2016. The IRE1/bZIP60 pathway andbax inhibitor 1 suppress systemic sccumulation of potyviruses and potexviruses in Arabidopsis and Nicotiana benthamiana Plants. Molecular Plant-Microbe Interactions 29: 750-766.
Hafrén A, Macia JL, Love AJ, Milner JJ, Drucker M, Hofius D. 2017. Selective autophagy limits cauliflower mosaic virus infection by NBR1-mediated targeting of viral capsid protein and particles. Proceedings of the National Academy of Sciences, USA 114: E2026-E2035.
Hafrén A, Üstün S, Hochmuth A, Svenning S, Johansen T, Hofius D. 2018. Turnip mosaic virus counteracts selective autophagy of the viral silencing suppressor HCpro. Plant Physiology 176: 649-662.
Hanna RA, Quinsay MN, Orogo AM, Giang K, Rikka S, Gustafsson AB. 2012. Microtubule-associated protein 1 light chain 3 (LC3) interacts with Bnip3 protein to selectively remove endoplasmic reticulum and mitochondria via autophagy. Journal of Biological Chemistry 287: 19094-19104.
Hatta T, Francki RIB. 1981. Cytopathic structures associated with tonoplasts of plant cells infected with cucumber mosaic and tomato aspermy viruses. Journal of General Virology 53: 343-346.
Haxim Y, Ismayil A, Jia Q, Wang Y, Zheng X, Chen T, Qian L, Liu N, Wang Y, Han S et al. 2017. Autophagy functions as an antiviral mechanism against geminiviruses in plants. eLife 6: e23897.
Huang TS, Wei T, Laliberté JF, Wang A. 2010. A host RNA helicase-like protein, AtRH8, interacts with the potyviral genome-linked protein, VPg, associates with the virus accumulation complex, and is essential for infection. Plant Physiology 152: 255-266.
Ibrahim A, Hutchens HM, Berg RH, Loesch-Fries LS. 2012. Alfalfa mosaic virus replicase proteins, P1 and P2, localize to the tonoplast in the presence of virus RNA. Virology 433: 449-461.
Ismayil A, Yang M, Haxima Y, Wang Y, Li J, Han L, Wang Y, Zheng X, Wei X, Nagalakshmi U et al. 2020a. Cotton leaf curl Multan virus βC1 protein induces autophagy by disrupting the interaction of autophagy-related protein 3 with Glyceraldehyde-3-Phosphate Dehydrogenases. The Plant Cell 32: 1124-1135.
Ismayil A, Yang M, Liu Y. 2020b. Role of autophagy during plant-virus interactions. Seminars in Cell & Developmental Biology 101: 36-40.
Jiang J, Patarroyo C, Cabanillas DG, Zheng H, Laliberté JF. 2015. The vesicle-forming 6K2 protein of turnip mosaic virus interacts with the COPII coatomer Sec24a for viral systemic infection. Journal of Virology 89: 6695-6710.
Kirkin V, McEwan DG, Novak I, Dikic I. 2009. A role for ubiquitin in selective autophagy. Molecular Cell 34: 259-269.
Kushwaha NK, Hafrén A, Hofius D. 2019. Autophagy-virus interplay in plants: from antiviral recognition to proviral manipulation. Molecular Plant Pathology 20: 1211-1216.
Levine B, Kroemer G. 2019. Biological functions of autophagy genes: a disease perspective. Cell 176: 11-45.
Li F, Wang A. 2019. RNA-targeted antiviral immunity: More than just RNA silencing. Trends in Microbiology 27: 792-805.
Li F, Zhang C, Li Y, Wu G, Hou X, Zhou X, Wang A. 2018. Beclin1 restricts RNA virus infection in plants through suppression and degradation of the viral polymerase. Nature Communications 9: 1268.
Li F, Zhang M, Zhang C, Zhou X. 2020. Nuclear autophagy degrades a geminivirus nuclear protein to restrict viral infection in solanaceous plants. New Phytologist 225: 1746-1761.
Li XH, Valdez P, Olvera RE, Carrington JC. 1997. Functions of the tobacco etch virus RNA polymerase (NIb): subcellular transport and protein-protein interaction with VPg/proteinase (NIa). Journal of Virology 71: 1598-1607.
Li Y, Humbert S, Howell SH. 2012. ZmbZIP60 mRNA is spliced in maize in response to ER stress. BMC Research Notes 5: 144.
Liu Y, Schiff M, Dinesh-Kumar SP. 2002. Virus-induced gene silencing in tomato. The Plant Journal 31: 777-786.
Lu Q, Tang X, Tian G, Wang F, Liu K, Nguyen V, Kohalmi SE, Keller WA, Tsang ET, Harada JJ et al. 2010. Arabidopsis homolog of the yeast TREX-2 mRNA export complex: components and anchoring nucleoporin. The Plant Journal 61: 259-270.
Lu S, Yang Z, Sun L, Sun L, Song Z, Liu J. 2012. Conservation of IRE1-regulated bZIP74 mRNA unconventional splicing in rice (Oryza sativa L.) involved in ER stress responses. Molecular Plant 5: 504-514.
Mäkinen K, Hafrén A. 2014. Intracellular coordination of potyviral RNA functions in infection. Frontiers in Plant Science 5: 110.
Marshall RS, Vierstra RD. 2018. Proteasome storage granules protect proteasomes from autophagic degradation upon carbon starvation. eLife, 7: e34532.
Medina-Puche L, Lozano-Duran R. 2019. Tailoring the cell: a glimpse of how plant viruses manipulate their hosts. Current Opinion in Plant Biology 52: 164-173.
Nakahara KS, Masuta C, Yamada S, Shimura H, Kashihara Y, Wada TS, Meguro A, Goto K, Tadamura K, Sueda K et al. 2012. Tobacco calmodulin-like protein provides secondary defense by binding to and directing degradation of virus RNA silencing suppressors. Proceedings of the National Academy of Sciences, USA 109: 10113-10118.
Olspert A, Carr JP, Firth AE. 2016. Mutational analysis of the Potyviridae transcriptional slippage site utilized for expression of the P3N-PIPO and P1N-PISPO proteins. Nucleic Acids Research 44: 7618-7629.
Olspert A, Chung BY-W, Atkins JF, Carr JP, Firth AE. 2015. Transcriptional slippage in the positive-sense RNA virus family Potyviridae. EMBO Reports 16: 995-1004.
Revers F, García JA. 2015. Molecular biology of potyviruses. Advances in Virus Research 92: 101-199.
Schaad MC, Jensen PE, Carrington JC. 1997. Formation of plant RNA virus replication complexes on membranes: role of an endoplasmic reticulum-targeted viral protein. EMBO Journal. 16: 4049-4059.
Shen W, Shi Y, Dai Z, Wang A. 2020. The RNA-dependent RNA polymerase NIb of potyviruses plays multifunctional, contrasting roles during viral infection. Viruses 12: 77.
Sparrer KMJ, Gack MU. 2018. TRIM proteins: new players in virus-induced autophagy. PLoS Path 14: e1006787.
Svenning S, Lamark T, Krause K, Johansen T. 2011. Plant NBR1 is a selective autophagy substrate and a functional hybrid of the mammalian autophagic adapters NBR1 and p62/SQSTM1. Autophagy 7: 993-1010.
Wan J, Basu K, Mui J, Vali H, Zheng H, Laliberté J-F. 2015. Ultrastructural characterization of turnip mosaic virus-induced cellular rearrangements reveals membrane-bound viral particles accumulating in vacuoles. Journal of Virology 89: 12441-12456.
Wang A. 2015. Dissecting the molecular network of virus-plant interactions: the complex roles of host factors. Annual Review of Phytopathology 53: 45-66.
Wang A. 2018. Virus and host plant interactions. In: eLS. Chichester, UK: John Wiley & Sons Ltd.
Wei T, Huang TS, McNeil J, Laliberté JF, Hong J, Nelson RS, Wang A. 2010a. Sequential recruitment of the endoplasmic reticulum and chloroplasts for plant potyvirus replication. Journal of Virology 84: 799-809.
Wei T, Wang A. 2008. Biogenesis of cytoplasmic membranous vesicles for plant potyvirus replication occurs at endoplasmic reticulum exit sites in a COPI- and COPII-dependent manner. Journal of Virology 82: 12252-12264.
Wei T, Zhang C, Hong J, Xiong R, Kasschau KD, Zhou X, Carrington JC, Wang A. 2010b. Formation of complexes at plasmodesmata for potyvirus intercellular movement is mediated by the viral protein P3N-PIPO. PLoS Path 6: e1000962.
Wong HH, Sanyal S. 2020. Manipulation of autophagy by (+)RNA viruses. Seminar in Cell and Developmental Biology 101: 3-11.
Xiong R, Wu J, Zhou Y, Zhou X. 2009. Characterization and subcellular localization of an RNA silencing suppressor encoded by Rice stripe tenuivirus. Virology 387: 29-40.
Yang M, Zhang Y, Xie X, Yue N, Li J, Wang XB, Han C, Yu J, Liu Y, Li D. 2018. γb protein subverts autophagy to promote viral infection by disrupting the ATG7-ATG8 interaction. The Plant Cell 30: 1582-1595.
Yoshida H, Matsui T, Yamamoto A, Okada T, Mori K. 2001. XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107: 881-891.
Yu L, Chen Y, Tooze SA. 2018. Autophagy pathway: cellular and molecular mechanisms. Autophagy 14: 207-215.
Zeng HY, Zheng P, Wang L-Y, Bao H-N, Sahu SK, Yao N. 2019. Autophagy in plant immunity. Advances in Experimental Medicine and Biology 1209: 23-41.
Zhang L, Chen H, Brandizzi F, Verchot J, Wang A. 2015. The UPR branch IRE1-bZIP60 in plants plays an essential role in viral infection and is complementary to the only UPR pathway in yeast. PLoS Genetics 11: e1005164.
Zhou J, Wang J, Cheng Y, Chi Y-J, Fan B, Yu J-Q, Chen Z. 2013. NBR1-mediated selective autophagy targets insoluble ubiquitinated protein aggregates in plant stress responses. PLoS Genetics 9: e1003196.
Zhu H, Hu F, Wang R, Zhou X, Sze S-H, Liou LW, Barefoot A, Dickman M, Zhang X. 2011. Arabidopsis Argonaute10 specifically sequesters miR166/165 to regulate shoot apical meristem development. Cell 145: 242-256.
Zientara-Rytter K, Lukomska J, Moniuszko G, Gwozdecki R, Surowiecki P, Lewandowska M, Liszewska F, Wawrzyńska A, Sirko A. 2011. Identification and functional analysis of Joka2, a tobacco member of the family of selective autophagy cargo receptors. Autophagy 7: 1145-1158.