Salicylic acid and the viral virulence factor 2b regulate the divergent roles of autophagy during cucumber mosaic virus infection

References

• Mizushima N. A brief history of autophagy from cell biology to physiology and disease. Nat Cell Biol. 2018;20(5):521–7.
   PubMed Web of Science ®Google Scholar
• Batoko H, Dagdas Y, Baluska F, et al. Understanding and exploiting autophagy signaling in plants. Essays Biochem. 2017;61(6):675–85.
   PubMed Web of Science ®Google Scholar
• Rogov V, Dotsch V, Johansen T, et al. Interactions between autophagy receptors and ubiquitin-like proteins form the molecular basis for selective autophagy. Mol Cell. 2014;53(2):167–78.
   PubMed Web of Science ®Google Scholar
• Michaeli S, Galili G, Genschik P, et al. Autophagy in Plants–What’s New on the Menu? Trends Plant Sci. 2016;21(2):134–44.
   PubMed Web of Science ®Google Scholar
• Gatica D, Lahiri V, Klionsky DJ. Cargo recognition and degradation by selective autophagy. Nat Cell Biol. 2018;20(3):233–42.
   PubMed Web of Science ®Google Scholar
• Stephani M, Dagdas Y. Plant Selective Autophagy-Still an Uncharted Territory With a Lot of Hidden Gems. J Mol Biol. 2020;432(1):63–79.
   PubMed Web of Science ®Google Scholar
• Soto-Burgos J, Zhuang X, Jiang L, et al. Dynamics of Autophagosome Formation. Plant Physiol. 2018;176(1):219–29.
   PubMed Web of Science ®Google Scholar
• Hofius D, Li L, Hafren A, et al. Autophagy as an emerging arena for plant-pathogen interactions. Curr Opin Plant Biol. 2017;38:117–23.
   PubMed Web of Science ®Google Scholar
• Ustun S, Hafren A, Liu Q, et al. Bacteria Exploit Autophagy for Proteasome Degradation and Enhanced Virulence in Plants. Plant Cell. 2018;30(3):668–85.
   PubMed Web of Science ®Google Scholar
• Hafren A, Ustun S, Hochmuth A, et al. Turnip Mosaic Virus Counteracts Selective Autophagy of the Viral Silencing Suppressor HCpro. Plant Physiol. 2018;176(1):649–62.
   PubMed Web of Science ®Google Scholar
• Hafren A, Macia JL, Love AJ, et al. Selective autophagy limits cauliflower mosaic virus infection by NBR1-mediated targeting of viral capsid protein and particles. Proc Natl Acad Sci U S A. 2017;114(10):E2026–E35.
   PubMed Web of Science ®Google Scholar
• Haxim Y, Ismayil A, Jia Q, et al. Autophagy functions as an antiviral mechanism against geminiviruses in plants. Elife. 2017;6.
   Web of Science ®Google Scholar
• Dagdas YF, Belhaj K, Maqbool A, et al. An effector of the Irish potato famine pathogen antagonizes a host autophagy cargo receptor. Elife. 2016;5.
   Web of Science ®Google Scholar
• Paudel DB, Sanfacon H. Exploring the Diversity of Mechanisms Associated With Plant Tolerance to Virus Infection. Front Plant Sci. 2018;9:1575.
   PubMed Web of Science ®Google Scholar
• Pagan I, Garcia-Arenal F. Tolerance to Plant Pathogens: Theory and Experimental Evidence. Int J Mol Sci. 2018;19(3).
   Web of Science ®Google Scholar
• Dong XN, Levine B. Autophagy and Viruses: Adversaries or Allies? Journal of Innate Immunity. 2013;5(5):480–93.
   PubMed Web of Science ®Google Scholar
• Fu S, Xu Y, Li C, et al. Rice Stripe Virus Interferes with S-acylation of Remorin and Induces Its Autophagic Degradation to Facilitate Virus Infection. Mol Plant. 2018;11(2):269–87.
   PubMed Web of Science ®Google Scholar
• Yang M, Zhang Y, Xie X, et al. Barley stripe mosaic virus gammab Protein Subverts Autophagy to Promote Viral Infection by Disrupting the ATG7-ATG8 Interaction. Plant Cell. 2018;30(7):1582–95.
   PubMed Web of Science ®Google Scholar
• Nakahara KS, Masuta C, Yamada S, et al. 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 of the United States of America. 2012;109(25):10113–8.
   PubMed Web of Science ®Google Scholar
• Cheng X, Wang A. The Potyvirus Silencing Suppressor Protein VPg Mediates Degradation of SGS3 via Ubiquitination and Autophagy Pathways. J Virol. 2017;91(1).
   Web of Science ®Google Scholar
• Derrien B, Baumberger N, Schepetilnikov M, et al. Degradation of the antiviral component ARGONAUTE1 by the autophagy pathway. Proc Natl Acad Sci U S A. 2012;109(39):15942–6.
   PubMed Web of Science ®Google Scholar
• Tong X, Liu SY, Zou JZ, et al. A small peptide inhibits siRNA amplification in plants by mediating autophagic degradation of SGS3/RDR6 bodies. EMBO J. 2021:e108050.
   PubMed Web of Science ®Google Scholar
• Yoshimoto K, Jikumaru Y, Kamiya Y, et al. Autophagy negatively regulates cell death by controlling NPR1-dependent salicylic acid signaling during senescence and the innate immune response in Arabidopsis. Plant Cell. 2009;21(9):2914–27.
   PubMed Web of Science ®Google Scholar
• Murphy AM, Zhou T, Carr JP. An update on salicylic acid biosynthesis, its induction and potential exploitation by plant viruses. Curr Opin Virol. 2020;42:8–17.
   PubMed Web of Science ®Google Scholar
• Carr JP, Murphy AM, Tungadi T, et al. Plant defense signals: Players and pawns in plant-virus-vector interactions. Plant Sci. 2019;279:87–95.
   PubMed Web of Science ®Google Scholar
• Mayers CN, Lee KC, Moore CA, et al. Salicylic acid-induced resistance to Cucumber mosaic virus in squash and Arabidopsis thaliana: contrasting mechanisms of induction and antiviral action. Mol Plant Microbe Interact. 2005;18(5):428–34.
   PubMed Web of Science ®Google Scholar
• Lee WS, Fu SF, Verchot-Lubicz J, et al. Genetic modification of alternative respiration in Nicotiana benthamiana affects basal and salicylic acid-induced resistance to potato virus X. BMC Plant Biol. 2011;11:41.
   PubMed Web of Science ®Google Scholar
• Ji LH, Ding SW. The suppressor of transgene RNA silencing encoded by Cucumber mosaic virus interferes with salicylic acid-mediated virus resistance. Mol Plant Microbe Interact. 2001;14(6):715–24.
   PubMed Web of Science ®Google Scholar
• Zhou T, Murphy AM, Lewsey MG, et al. Domains of the cucumber mosaic virus 2b silencing suppressor protein affecting inhibition of salicylic acid-induced resistance and priming of salicylic acid accumulation during infection. J Gen Virol. 2014;95(Pt 6):1408–13.
   PubMedGoogle Scholar
• Chung T, Phillips AR, Vierstra RD. ATG8 lipidation and ATG8-mediated autophagy in Arabidopsis require ATG12 expressed from the differentially controlled ATG12A AND ATG12B loci. Plant J. 2010;62(3):483–93.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Li X. Salicylic acid: biosynthesis, perception, and contributions to plant immunity. Curr Opin Plant Biol. 2019;50:29–36.
   PubMed Web of Science ®Google Scholar
• Gibbs AJ, Gower, J.C. The use of multiple transfer method in plant virus transmission studies- some statistical points arising from the analysis of results. Annals of Applied Biology. 1960;48(1):75–83.
   Web of Science ®Google Scholar
• Pagan I, Fraile A, Fernandez-Fueyo E, et al. Arabidopsis thaliana as a model for the study of plant-virus co-evolution. Philos Trans R Soc Lond B Biol Sci. 2010;365(1548):1983–95.
   PubMed Web of Science ®Google Scholar
• Lewsey M, Robertson FC, Canto T, et al. Selective targeting of miRNA-regulated plant development by a viral counter-silencing protein. Plant J. 2007;50(2):240–52.
   PubMed Web of Science ®Google Scholar
• Gonzalez I, Martinez L, Rakitina DV, et al. Cucumber mosaic virus 2b protein subcellular targets and interactions: their significance to RNA silencing suppressor activity. Mol Plant Microbe Interact. 2010;23(3):294–303.
   PubMed Web of Science ®Google Scholar
• Diaz-Pendon JA, Li F, Li WX, et al. Suppression of antiviral silencing by cucumber mosaic virus 2b protein in Arabidopsis is associated with drastically reduced accumulation of three classes of viral small interfering RNAs. Plant Cell. 2007;19(6):2053–63.
   PubMed Web of Science ®Google Scholar
• Zhang X, Yuan YR, Pei Y, et al. Cucumber mosaic virus-encoded 2b suppressor inhibits Arabidopsis Argonaute1 cleavage activity to counter plant defense. Genes Dev. 2006;20(23):3255–68.
   PubMed Web of Science ®Google Scholar
• Han S, Wang Y, Zheng X, et al. Cytoplastic Glyceraldehyde-3-Phosphate Dehydrogenases Interact with ATG3 to Negatively Regulate Autophagy and Immunity in Nicotiana benthamiana. Plant Cell. 2015;27(4):1316–31.
   PubMed Web of Science ®Google Scholar
• Ziebell H, Carr JP. Effects of dicer-like endoribonucleases 2 and 4 on infection of Arabidopsis thaliana by cucumber mosaic virus and a mutant virus lacking the 2b counter-defence protein gene. J Gen Virol. 2009;90(Pt 9):2288–92.
   PubMedGoogle Scholar
• Mason GA, Lemus T, Queitsch C. The Mechanistic Underpinnings of an ago1-Mediated, Environmentally Dependent, and Stochastic Phenotype. Plant Physiol. 2016;170(4):2420–31.
   PubMed Web of Science ®Google Scholar
• Kushwaha NK, Hafren A, Hofius D. Autophagy-virus interplay in plants: from antiviral recognition to proviral manipulation. Mol Plant Pathol. 2019;20(9):1211–6.
   PubMed Web of Science ®Google Scholar
• Roy BA, Kirchner JW. Evolutionary dynamics of pathogen resistance and tolerance. Evolution. 2000;54(1):51–63.
   PubMed Web of Science ®Google Scholar
• Li F, Zhang C, Li Y, et al. Beclin1 restricts RNA virus infection in plants through suppression and degradation of the viral polymerase. Nat Commun. 2018;9(1):1268.
   PubMedGoogle Scholar
• Zvereva AS, Golyaev V, Turco S, et al. Viral protein suppresses oxidative burst and salicylic acid-dependent autophagy and facilitates bacterial growth on virus-infected plants. New Phytol. 2016.
   PubMed Web of Science ®Google Scholar
• Love AJ, Geri C, Laird J, et al. Cauliflower mosaic virus protein P6 inhibits signaling responses to salicylic acid and regulates innate immunity. PLoS One. 2012;7(10):e47535.
   PubMed Web of Science ®Google Scholar
• Alamillo JM, Saenz P, Garcia JA. Salicylic acid-mediated and RNA-silencing defense mechanisms cooperate in the restriction of systemic spread of plum pox virus in tobacco. Plant J. 2006;48(2):217–27.
   PubMed Web of Science ®Google Scholar
• Poque S, Wu HW, Huang CH, et al. Potyviral Gene-Silencing Suppressor HCPro Interacts with Salicylic Acid (SA)-Binding Protein 3 to Weaken SA-Mediated Defense Responses. Mol Plant Microbe Interact. 2018;31(1):86–100.
   PubMed Web of Science ®Google Scholar
• Zhao JH, Liu XL, Fang YY, et al. CMV2b-Dependent Regulation of Host Defense Pathways in the Context of Viral Infection. Viruses. 2018;10(11).
   Web of Science ®Google Scholar
• Goto K, Kobori T, Kosaka Y, et al. Characterization of silencing suppressor 2b of cucumber mosaic virus based on examination of its small RNA-binding abilities. Plant Cell Physiol. 2007;48(7):1050–60.
   PubMed Web of Science ®Google Scholar
• Hafren A, Lohmus A, Makinen K. Formation of Potato Virus A-Induced RNA Granules and Viral Translation Are Interrelated Processes Required for Optimal Virus Accumulation. PLoS Pathog. 2015;11(12):e1005314.
   PubMed Web of Science ®Google Scholar
• Elena SF, Agudelo-Romero P, Carrasco P, et al. Experimental evolution of plant RNA viruses. Heredity (Edinb). 2008;100(5):478–83.
   PubMed Web of Science ®Google Scholar
• Lenski RE, May RM. The evolution of virulence in parasites and pathogens: reconciliation between two competing hypotheses. J Theor Biol. 1994;169(3):253–65.
   PubMed Web of Science ®Google Scholar
• Alizon S, Hurford A, Mideo N, et al. Virulence evolution and the trade-off hypothesis: history, current state of affairs and the future. J Evol Biol. 2009;22(2):245–59.
   PubMed Web of Science ®Google Scholar
• Lipsitch M, Siller S, Nowak MA. The Evolution of Virulence in Pathogens with Vertical and Horizontal Transmission. Evolution. 1996;50(5):1729–41.
   PubMed Web of Science ®Google Scholar
• Stewart AD, Logsdon JM, Jr., Kelley SE. An empirical study of the evolution of virulence under both horizontal and vertical transmission. Evolution. 2005;59(4):730–9.
   PubMed Web of Science ®Google Scholar
• Du Z, Chen A, Chen W, et al. Nuclear-cytoplasmic partitioning of cucumber mosaic virus protein 2b determines the balance between its roles as a virulence determinant and an RNA-silencing suppressor. J Virol. 2014;88(10):5228–41.
   PubMed Web of Science ®Google Scholar
• Kraft LJ, Manral P, Dowler J, et al. Nuclear LC3 Associates with Slowly Diffusing Complexes that Survey the Nucleolus. Traffic. 2016;17(4):369–99.
   PubMed Web of Science ®Google Scholar
• Li F, Zhang M, Zhang C, et al. Nuclear autophagy degrades a geminivirus nuclear protein to restrict viral infection in solanaceous plants. New Phytol. 2020;225(4):1746–61.
   PubMed Web of Science ®Google Scholar
• Gonda T, Symons R. Cucumber mosaic virus replication in Cowpea protoplasts: Time course of virus, coat protein and RNA synthesis. Journal of General Virology. 1979;45:723–36.
   Web of Science ®Google Scholar
• Zhang XP, Liu DS, Yan T, et al. Cucumber mosaic virus coat protein modulates the accumulation of 2b protein and antiviral silencing that causes symptom recovery in planta. PLoS Pathog. 2017;13(7):e1006522.
   PubMed Web of Science ®Google Scholar
• Hofius D, Schultz-Larsen T, Joensen J, et al. Autophagic components contribute to hypersensitive cell death in Arabidopsis. Cell. 2009;137(4):773–83.
   PubMed Web of Science ®Google Scholar
• Zhou J, Wang J, Cheng Y, et al. NBR1-mediated selective autophagy targets insoluble ubiquitinated protein aggregates in plant stress responses. PLoS Genet. 2013;9(1):e1003196.
   PubMed Web of Science ®Google Scholar
• Munch D, Teh OK, Malinovsky FG, et al. Retromer contributes to immunity-associated cell death in Arabidopsis. Plant Cell. 2015;27(2):463–79.
   PubMed Web of Science ®Google Scholar
• Shinozaki D, Merkulova EA, Naya L, et al. Autophagy Increases Zinc Bioavailability to Avoid Light-Mediated Reactive Oxygen Species Production under Zinc Deficiency. Plant Physiol. 2020;182(3):1284–96.
   PubMed Web of Science ®Google Scholar
• Nakagawa T, Kurose T, Hino T, et al. Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. J Biosci Bioeng. 2007;104(1):34–41.
   PubMed Web of Science ®Google Scholar
• Koncz C, Schell J. The promoter of TL-DNA gene 5 controls the tissue-specific expression of chimaeric genes carried by a novel type of Agrobacterium binary vector. Mol Gen Genet. 1986;204: 383–396.
   Google Scholar
• Groen SC, Jiang S, Murphy AM, et al. Virus Infection of Plants Alters Pollinator Preference: A Payback for Susceptible Hosts? PLoS Pathog. 2016;12(8):e1005790.
   PubMed Web of Science ®Google Scholar
• Svenning S, Lamark T, Krause K, et al. Plant NBR1 is a selective autophagy substrate and a functional hybrid of the mammalian autophagic adapters NBR1 and p62/SQSTM1. Autophagy. 2011;7(9):993–1010.
   PubMed Web of Science ®Google Scholar