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Archives of Virology

, Volume 163, Issue 5, pp 1317–1323 | Cite as

Targeting of rice grassy stunt virus pc6 protein to plasmodesmata requires the ER-to-Golgi secretory pathway and an actin-myosin VIII motility system

  • Xuelian Sui
  • Xiaojuan Liu
  • Wenwu Lin
  • Zujian Wu
  • Liang Yang
Brief Report
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Abstract

The nonstructural protein pc6 encoded by rice grassy stunt virus (RGSV) plays a significant role in viral cell-to-cell movement, presumably by transport through plasmodesmata (PD). We confirmed the association of pc6 with PD, and also elucidated the mechanisms of protein targeting to PD. Several inhibitor treatments showed conclusively that pc6 is targeted to PD via the ER-to-Golgi secretory system and actin filaments. In addition, VIII-1 myosin was also found to be involved in pc6 PD targeting. Deletion mutants demonstrated that C-terminal amino acid residues 209-229 (transmembrane domain 2; TM2) are essential for pc6 to move through PD.

Keywords

Rice grassy stunt virus pc6 plasmodesmata movement protein protein targeting 

Notes

Funding

This work was supported by the Natural Science Foundation of Fujian Province, China (Grant number 2014J06011) and the Science Fund for Distinguished Young Scholars of Fujian Agriculture and Forestry University (Grant number xjq201402).

Compliance with ethical standards

Conflict of interest

All authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies that used human participants.

References

  1. 1.
    Hibino H (1996) Biology and epidemiology of rice viruses. Annu Rev Phytopathol 34:249–274CrossRefPubMedGoogle Scholar
  2. 2.
    Xiong G, Liu X, Qiu P et al (2017) Rice grassy stunt virus p5 interacts with two protein components of the plant-specific CBL-CIPK Ca2+ signaling network of rice. Virus Genes 53(3):446–453CrossRefPubMedGoogle Scholar
  3. 3.
    Toriyama S, Tomaru K (1995) Genus tenuivirus. In: Murphy FA, Fauquet CM, Bishop DHL, Ghabrial SA, Jarvis AW, Martelli GP, Mayo MA, Summers MD (eds) Virus taxonomy. Sixth report of the international committee on taxonomy of viruses. Springer, Vienna, pp 316–318Google Scholar
  4. 4.
    Hibino H, Usugi T, Omura T, Tsuchizaki T, Shohara K, Iwasaki M (1985) Rice grassy stunt virus: a planthopper-borne circular filament. Phytopathology 75:894–899CrossRefGoogle Scholar
  5. 5.
    Toriyama S, Kimishima T, Takahashi M, Shimizu T, Minaka N, Akutsu K (1998) The complete nucleotide sequence of the rice grassy stunt virus genome and genomic comparisons with viruses of the genus Tenuivirus. J Gen Birol 79:2051–2058CrossRefGoogle Scholar
  6. 6.
    Kormelink R, Garcia ML, Goodin M, Sasaya T, Haenni AL (2011) Negative-strand RNA viruses: the plant-infecting counterparts. Virus Res 162:184–202CrossRefPubMedGoogle Scholar
  7. 7.
    Netsu O, Hiraguri A, Uehara-Ichiki T, Komatsu K, Sasaya T (2015) Functional comparison of RNA silencing suppressor between the p5protein of rice grassy stunt virus and the p3 protein of rice stripe virus. Virus Res 203:10–19CrossRefPubMedGoogle Scholar
  8. 8.
    Nguyen TD, Lacombe S, Bangratz M, Ta HA, Gantet P, Brugidou C (2015) P2 of Rice grassy stunt virus (RGSV) and p6 and p9 of Rice ragged stunt virus (RRSV) isolates from Vietnam exert suppressor activity on the RNA silencing pathway. Virus Genes 51(2):267–275CrossRefPubMedGoogle Scholar
  9. 9.
    Toriyama S, Kimishima T, Takahashi M (1997) The proteins encoded by rice grassy stunt virus RNA5 and RNA6 are only distantly related to the corresponding proteins of other members of the genus Tenuivirus. J Gen Virol 78:2355–2363CrossRefPubMedGoogle Scholar
  10. 10.
    Hiraguri A, Netsu O, Shimizu T, Uehara-Ichiki T, Omura T, Sasaki N, Nyunoya H, Sasaya T (2011) The nonstructural protein pC6 of rice grassy stunt virus trans-complements the cell-to-cell spread of a movement-defective tomato mosaic virus. Arch Virol 156:911–916CrossRefPubMedGoogle Scholar
  11. 11.
    Harries PA, Schoelz JE, Nelson RS (2010) Intracellular transport of viruses and their components: utilizing the cytoskeleton and membrane highways. Mol Plant Microbe Interact 23:1381–1393CrossRefPubMedGoogle Scholar
  12. 12.
    Andika IB, Zheng S, Tan Z, Sun L, Kondo H, Zhou X, Chen J (2013) Endoplasmic reticulum export and vesicle formation of the movement protein of Chinese wheat mosaic virus are regulated by two transmembrane domains and depend on the secretory pathway. Virology 435:493–503CrossRefPubMedGoogle Scholar
  13. 13.
    Niehl A, Heinlein M (2011) Cellular pathways for viral transport through plasmodesmata. Protoplasma 248:75–99CrossRefPubMedGoogle Scholar
  14. 14.
    Kawakami S, Watanabe Y, Beachy RN (2004) Tobacco mosaic virus infection spreads cell to cell as intact replication complexes. Proc Natl Acad Sci USA 101:6291–6296CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Wright KM, Wood NT, Roberts AG, Chapman S, Boevink P, MacKenzie KM, Oparka KJ (2007) Targeting of TMV movement protein to plasmodesmata requires the actin/ER network: evidence from FRAP. Traffic 8:21–31CrossRefPubMedGoogle Scholar
  16. 16.
    Pouwels J, van der Velden T, Willemse J, Borst JW, van Lent J, Bisseling T, Wellink J (2004) Study on the origin and structure of tubules made by the movement protein of Cowpea mosaic virus. J Gen Virol 85:3787–3796CrossRefPubMedGoogle Scholar
  17. 17.
    Wei T, Zhang C, Hong J, Xiong R, Kasschau KD, Zhou X, Carrington JC, Wang A (2010) Formation of complexes at plasmodesmata for Potyvirus intercellular movement is mediated by the viral protein P3N-PIPO. Plos Pathog 6:e1000962.  https://doi.org/10.1371/journal.ppat.1000962 CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Sun Z, Zhang S, Xie L, Zhu Q, Tan Z, Bian J, Sun L, Chen J (2013) The secretory pathway and the actomyosin motility system are required for plasmodesmatal localization of the P7-1 of rice black-streaked dwarf virus. Arch Virol 158:1055–1064CrossRefPubMedGoogle Scholar
  19. 19.
    Yuan Z, Chen H, Chen Q, Omura T, Xie L, Wu Z, Wei T (2011) The early secretory pathway and an actin-myosin VIII motility system are required for plasmodesmatal localization of the NSvc4 protein of Rice stripe virus. Virus Res 159:62–68CrossRefPubMedGoogle Scholar
  20. 20.
    Xu Y, Zhou X (2012) Role of rice stripe virus NSvc4 in cell-to-cell movement and symptom development in Nicotiana benthamiana. Front Plant Sci 3:269CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Avisar D, Prokhnevsky AI, Dolja VV (2008) Class VIII myosins are required for plasmodesmatal localization of a closterovirus Hsp70 homolog. J Virol 82:2836–2843CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Avisar D, Prokhnevsky AI, Makarova KS, Koonin EV, Dolja VV (2008) Myosin XI-K required for rapid trafficking of Golgi stacks, peroxisomes, and mitochondria in leaf cells of Nicotiana benthamiana. Am Soc Plant Biol 146:1098–1108Google Scholar
  23. 23.
    Thomas CL, Bayer EM, Ritzenthaler C, Fernandez-Calvino L, Maule AJ (2008) Specific targeting of a plasmodesmal protein affecting cell-to-cell communication. Plos Biol 6:e1–e7CrossRefGoogle Scholar
  24. 24.
    Harries PA, Park JW, Sasaki N, Ballard KD, Maule AJ, Nelson RS (2009) Differing requirements for actin and myosin by plant viruses for sustained intercellular movement. PNAS 106:17594–17599CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Ritzenthaler C, Nebenführ A, Movafeghi A, Stussi-Garaud C, Behnia L, Pimpl P, Staehelin LA, Robinson DG (2002) Reevaluation of the effects of Brefeldin A on plant cells using tobacco bright yellow 2 cells expressing Golgi-targeted green fluorescent protein and COPI antisera. Plant Cell 14:237–261CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Tse YC, Lo SW, Hillmer S, Dupree P, Jiang L (2006) Dynamic response of prevacuolar compartments to Brefeldin A in plant cells. Plant Physiol 142:1442–1459CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Gibbon BC, Kovar DR, Staiger CJ (1999) Latrunculin B has different effects on pollen germination and tube growth. Plant Cell 11:1363–2349CrossRefGoogle Scholar
  28. 28.
    Nakamura M, Naoi K, Shoji T, Hashimoto T (2004) Low concentrations of propyzamide and oryzalin alter microtubule dynamics in Arabidopsis epidermal cells. Plant Cell Physiol 45:1330–1334CrossRefPubMedGoogle Scholar
  29. 29.
    Buchnik L, Abu-Abied M, Sadot E (2014) Role of plant myosins in motile organelles: is a direct interaction required? J Integr Plant Biol 57:23–30CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2018

Authors and Affiliations

  1. 1.State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian Province Key Laboratory of Plant Virology, Institute of Plant VirologyFujian Agriculture and Forestry UniversityFuzhouChina

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