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Subcellular localization and interactions among TGB proteins of cowpea mild mottle virus

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Abstract

Cowpea mild mottle virus (CPMMV) is a flexuous filamentous virus that belongs to the genus Carlavirus (family Betaflexiviridae). The CPMMV genome contains six open reading frames (ORFs), among which the triple gene block (TGB), encoded by ORFs 2 to 4, has been reported to encode movement proteins for different viruses. The subcellular localization of the TGB proteins of CPMMV isolate CPMMV:BR:MG:09:2 was analysed by transient expression of each protein fused to a fluorophore. Overall, the accumulation pattern and interactions among CPMMV TGB proteins (TGBp) were similar to those of their counterparts from the potex-like group. Considering these similarities, we evaluated the potential interactions between the TGB proteins of CPMMV and of potato virus X, which could complement cell-to-cell movement. The TGBp2 and TGBp3 of PVX had an effect on CPMMV TGBp1, directing it to the plasmodesmata, but the reverse was not true.

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References

  • Boevink P, Santa Cruz S, Hawes C, Harris N, Oparka KJ (1996) Virus-mediated delivery of the green fluorescent protein to the endoplasmic reticulum of plant cells. Plant J 10(5):935–941

    Article  CAS  Google Scholar 

  • Cowan GH, Lioliopoulou F, Ziegler A, Torrance L (2002) Subcellular localisation, protein interactions, and RNA binding of Potato mop-top virus triple gene block proteins. Virol v 298(1):106–115

    Article  CAS  Google Scholar 

  • Gaspar JO, Belintani P, Almeida AM (2008) ; Kitajima, E. W. A degenerate primer allows amplification of part of the 3’-terminus of three distinct carlavirus species. Journal of Virological Methods, v. 148, n. 1–2, p. 283-5

  • Hellens RP, Edwards EA, Leyland NR, Bean S, Mullineaux PM (2000) pGreen: a versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation. Plant Mol Biology v 42(6):819–832

    Article  CAS  Google Scholar 

  • Horsch RB, Fry JE, Hoffmann NL, Wallroth M, Eichholtz D, Rogers SG, Fraley RT(1985) A simple and general method for transferring genes into plants. Science, v. 227, n. 4691, p. 1229-31

  • Jiang C, Shan S, Huang Y, Mao C, Zhang H, Li Y, Chen J, Wei Z, Sun Z(2022) The C-terminal transmembrane domain of Cowpea mild mottle virus TGBp2 is critical for plasmodesmata localization and for its interaction with TGBp1 and TGBp3. Frontiers in Microbiology, v. 13, article 860695.

  • Ju HJ, Samuels TD, Wang Y-S, Blancaflor E, Payton M, Mitra M, Krishnamurthy K, Nelson RS, Verchot-Lubicz J(2005) The Potato virus X TGBp2 movement protein associates with endoplasmic reticulum-derived vesicles during virus infection. Plant Physiology, v. 138, p. 1877-95

  • Knox K, Kriechbaumer V, Tilsner J, Frigerio L, Sparkes I, Hawes C, Oparka K (2015) Putting the squeeze on plasmodesmata: a Role for reticulons in primary plasmodesmata formation. Plant Physiol 168(4):1563–1572

    Article  CAS  Google Scholar 

  • Krishnamurthy K, Heppler M, Mitra R, Blancaflor E, Payton M, Nelson RS, Verchot-Lubicz J (2003) The Potato virus X TGBp3 protein associates with the ER network for virus cell-to-cell movement. Virol v 309:135–151

    Article  CAS  Google Scholar 

  • Lazareva EA, Lezzhov AA, Chergintsev DA, Golyshev SA, Dolja VV, Morozov SY, Heinlein M, Solovyev AG (2021) Reticulon-like properties of a plant virus-encoded movement protein. New Phytologist v 229(2):1052–1066

    Article  CAS  Google Scholar 

  • Lee S-C, Wu C-H, Wang C-W (2010) Traffic of a viral movement protein complex to the highly curved tubules of the cortical endoplasmic reticulum. Traffic v 11:912–930

    Article  CAS  Google Scholar 

  • Leshchiner AD, Minina EA, Rakitina DV, Vishnichenko VK, Solovyev AG, Morozov SY, Kalinina NO (2008) Oligomerization of the potato virus X 25-kD movement protein. Biochem (Moscow) v 73(1):50–55

    Article  CAS  Google Scholar 

  • Linnik O, Liesche J, Tilsner J, Oparka KJ(2013) Unraveling the structure of viral replication complexes at super-resolution. Frontiers in Plant Science, v. 4, p. 6

  • Liu DYT, Kuhlmey BT, Smith PMC, Day DA, Faulkner CR, Overall RL (2008) Reflection across plant cell boundaries in confocal laser scanning microscopy. J Microscopy v 231:349–357

    Article  CAS  Google Scholar 

  • Mann K, Meng B(2013) The triple gene block movement proteins of a grape virus in the genus Foveavirus confer limited cell-to-cell spread of a mutant Potato virus X. Virus Genes, v. 47, n. 1, p.93–104

  • Matousek J, Schubert J, Dedic P (2009) Complementation analysis of triple gene block of Potato virus S (PVS) revealed its capability to support systemic infection and aphid transmissibility of recombinant Potato virus X. Virus Res v 146:1–2

    Google Scholar 

  • Menzel W, Winter S, Vetten HJ (2010) Complete nucleotide sequence of the type isolate of Cowpea mild mottle virus from Ghana. Archives of Virology v 155(12):2069–2073

    Article  CAS  Google Scholar 

  • Morozov SY, Solovyev AG(2003) Triple gene block: modular design of a multifunctional machine for plant virus movement.Journal of General Virology, v.84, n. Pt 6, p.1351–66

  • NAKAGAWA T, SUZUKI T, MURATA S, NAKAMURA S;HINO, T.

  • Nishiguchi M, Motoyoshi F, Oshima N (1978) Behaviour of a Temperature Sensitive Strain of Tobacco Mosaic Virus in Tomato Leaves and Protoplasts. J Gen Virol v 39:53–61

    Article  Google Scholar 

  • Perraki A, Binaghi M, Mecchia MA, Gronnier J, German-Retana S, Mongrand S, Bayer E, Zelada AM, Germain V(2014) StRemorin1.3 hampers Potato virus X TGBp1 ability to increase plasmodesmata permeability, but does not interfere with its silencing suppressor activity. FEBS Letters, v. 588, p. 1699–1705

  • Rebelo AR, Niewiadomski S, Prosser SW, Krell,P.; MENG B. Subcellular localization of the triple gene block proteins encoded by a Foveavirus infecting grapevines.Virus Research, v.138, n.1–2, p. 57–69

  • Rosario K, Capobianco H, Ng TF, Breitbart M;Polston, JE. RNA viral metagenome of whiteflies leads to the discovery and characterization of a whitefly-transmitted carlavirus in North America.PLoS One v. 9, n. 1, p. e86748

  • Sambrook J, Russel D (2001) Molecular Cloning - A Laboratory Manual, 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY

    Google Scholar 

  • Samuels TD, Ju HJ, Ye CM, Motes CM, Blancaflor EB, Verchot-Lubicz J (2007) Subcellular targeting and interactions among the Potato virus X TGB proteins. Virol v 367(2):375–389

    Article  CAS  Google Scholar 

  • Senshu H, Ozeki J, Komatsu K, Hashimoto M;Hatada, K.

  • Senshu H, Yamaji Y, Minato N, Shiraishi T, Maejima K, Hashimoto M, Miura C, Neriya Y, Namba S (2011) A dual strategy for the suppression of host antiviral silencing: two distinct suppressors for viral replication and viral movement encoded by potato virus M. J Virol v 85:10269–10278

    Article  CAS  Google Scholar 

  • Shaner NC, Davidson MW, Lin MZ, Mckeown MR, Steinbach PA, Hazelwood KL, Tsien RY (2008) Improving the photostability of bright monomeric orange and red fluorescent proteins. Nat Methods v 5(6):545–551

    Article  CAS  Google Scholar 

  • Tilsner J, Linnik O, Christensen NM, Bell K, Roberts IM, Lacomme C, Oparka KJ (2009) Live-cell imaging of viral RNA genomes using a Pumilio-based reporter. Plant J 57(4):758–770

    Article  CAS  Google Scholar 

  • Tilsner J, Linnik O, Louveaux M, Roberts IM;Chapman, Sat the entrances of plasmodesmata.Journal of Cell Biology, v.201, n. 7, p.981-95.

  • Tilsner, J.; Linnik, O.; Wright, K. M.; Bell, K.; Roberts, A. G.; Lacomme, C.; Santa Cruz, S.; Oparka, K. J. (2012). The TGB1 movement protein of Potato virus X reorganizes actin and endomembranes into the X-body,a viral replication factory. Plant Physiology, v. 158, n. 3, p. 1359-70

  • Tilslner, J.; Taliansky, M. E.; Torrance, L. Plant Virus Movement. Chichester: eLS. John Wiley & Sons, Ltd, 2014.

  • Tolley, N.; Sparkes, I. A.; Hunter, P. R.; Craddock, C. P.; Nuttall, J.; Roberts, L. M.; Hawes,C.; Pedrazzini, E.; Frigerio, L. (2008). Overexpression of a plant reticulon remodels the lumen of the cortical endoplasmic reticulum but does not perturb protein transport.Traffic, v. 9, n. 1, p. 94–102.

  • Verchot-Lubicz, J.; Torrance, L.; Solovyev, A. G.; Morozov, S. Y.; Jackson, A. O.; Gilmer, D. (2010). Varied movement strategies employed by triple gene block-encoding viruses. Molecular Plant-Microbe Interactions, v. 23,n. 10, p. 1231-47.

  • WU, C. H.; Lee, S. C.; Wang, C. W. (2011). Viral protein targeting to the cortical endoplasmic reticulum is required for cell-cell spreading in plants. Journal of Cell Biology, v. 193, n. 3, p. 521 – 35.

  • Zanardo, L. G.; Silva, F. N.; Bicalho, A. A. C.; Urquiza, G. P. C.; Lima, A. T. M.; Almeida, A. M. R.; Zerbini, F. M.; Carvalho, C. M. (2014a). Molecular and biological characterization of Cowpea mild mottle virus isolates infecting soybean in Brazil and evidence of recombination. Plant Pathology, v. 63, n. 2, p. 456–465.

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Funding

This work was funded by Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG) Processo: APQ-01604-14, Brazil. S.L.C. was supported by a scholarship from the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, Brasil. Parts of this work were funded by the U.K. Biotechnology and Biomedical Sciences Research Council (BBSRC) grant BB/M007200/1 to J.T. Work in the J.T. laboratory is supported by the Scottish Government’s Rural and Environment Science and Analytical Services Division (RESAS).

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Authors and Affiliations

  1. Departamento de Fitopatologia, Universidade Federal de Lavras, Campus Universitário, 37200- 900, Lavras, MG, Brazil

    A. R. Figueira & C. M. Carvalho

  2. Departamento de Fitopatologia, Universidade Federal de Viçosa, Av. P. H. Rolfs, s/ nº Campus Universitário, 36570-000, Viçosa, MG, Brasil

    S. L. Carvalho & C. M. Carvalho

  3. Cell and Molecular Sciences, The James Hutton Institute, DD2 5DA, Dundee, Scotland, UK

    J. Tilsner

  4. Biomedical Sciences Research Complex, University of St Andrews, KY16 9ST, St Andrews, Fife, Scotland, UK

    J. Tilsner

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  1. S. L. Carvalho
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Carvalho, S.L., Tilsner, J., Figueira, A.R. et al. Subcellular localization and interactions among TGB proteins of cowpea mild mottle virus. Arch Virol 167, 2555–2566 (2022). https://doi.org/10.1007/s00705-022-05576-7

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