1887

Abstract

The badnavirus replication cycle is poorly understood and most knowledge is based on extrapolations from model viruses such as (CaMV). However, in contrast to CaMV, badnaviruses are thought not to produce viroplasms and therefore it has been a mystery as to where virion assembly occurs. In this study, ultrathin sections of a banana leaf infected with a badnavirus, banana streak MY virus (BSMYV), were examined by transmission electron microscopy. Electron-dense inclusion bodies (EDIBs) were sporadically distributed in parenchymatous tissues of the leaf, most commonly in the palisade and spongy mesophyll cells. These EDIBs had a characteristic structure, comprising an electron-dense core, a single, encircling lacuna and an outer ring of electron-dense material. However, much less frequently, EDIBs with two or three lacunae were observed. In the outer ring, densely packed virions were visible with a shape and size consistent with that expected for badnaviruses. Immunogold labelling was done with primary antibodies that detected the N-terminus of the capsid protein and strong labelling of the outer ring but not the central core or lacuna was observed. It is concluded that the EDIBs that were observed are equivalent in function to the viroplasms of CaMV, although obviously different in composition as there is not a paralogue of the transactivation/viroplasm protein in the badnavirus genome. It is postulated that production of a viroplasm could be a conserved characteristic of all members of the .

Funding
This study was supported by the:
  • , Hort Innovation, http://dx.doi.org/10.13039/501100000981
Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.001498
2020-10-01
2020-12-01
Loading full text...

Full text loading...

References

  1. Teycheney P-Y, Geering ADW, Dasgupta I, Hull R, Kreuze JF et al. ICTV Virus Taxonomy Profile: Caulimoviridae. J Gen Virol 2020
    [Google Scholar]
  2. Jones AT, Roberts IM. Ultrastructural changes and small bacilliform particles associated with infection by Rubus yellow net virus. Ann Appl Biol 1976; 84:305–310 [CrossRef]
    [Google Scholar]
  3. Cheng CP, Tzafrir I, Lockhart BE, Olszewski NE. Tubules containing virions are present in plant tissues infected with Commelina yellow mottle badnavirus. J Gen Virol 1998; 79:925–929 [CrossRef][PubMed]
    [Google Scholar]
  4. Jacquot E, Hagen LS, Michler P, Rohfritsch O, Stussi-Garaud C et al. In situ localization of cacao swollen shoot virus in agroinfected Theobroma cacao. Arch Virol 1999; 144:259–271 [CrossRef][PubMed]
    [Google Scholar]
  5. Saito Y, Roechan M, Tantera DM, Iwaki M. Small bacilliform particles associated with Penyakit Habang (Tungro-like) disease of rice in Indonesia. Phytopathology 1975; 65:793–796 [CrossRef]
    [Google Scholar]
  6. Shepherd RJ, Richins R, Shalla TA. Isolation and properties of the inclusion bodies of cauliflower mosaic virus. Virology 1980; 102:389–400 [CrossRef][PubMed]
    [Google Scholar]
  7. Schoelz JE, Leisner S. Setting up shop: the formation and function of the viral factories of cauliflower mosaic virus. Front Plant Sci 2017; 8:8 [CrossRef][PubMed]
    [Google Scholar]
  8. Espinoza AM, Medina V, Hull R, Markham PG. Cauliflower mosaic virus gene II product forms distinct inclusion bodies in infected plant cells. Virology 1991; 185:337–344 [CrossRef][PubMed]
    [Google Scholar]
  9. Martinière A, Gargani D, Uzest M, Lautredou N, Blanc S et al. A role for plant microtubules in the formation of transmission-specific inclusion bodies of Cauliflower mosaic virus. Plant J 2009; 58:135–146 [CrossRef][PubMed]
    [Google Scholar]
  10. Martinière A, Bak A, Macia JL, Lautredou N, Gargani D et al. A virus responds instantly to the presence of the vector on the host and forms transmission morphs. Elife 2013; 2:e00183 [CrossRef][PubMed]
    [Google Scholar]
  11. Bak A, Gargani D, Macia JL, Malouvet E, Vernerey MS et al. Virus factories of cauliflower mosaic virus are virion reservoirs that engage actively in vector transmission. J Virol 2013; 87:12207–12215 [CrossRef][PubMed]
    [Google Scholar]
  12. Bhat AI, Hohn T, Selvarajan R. Badnaviruses: the current global scenario. Viruses 2016; 8:177 [CrossRef][PubMed]
    [Google Scholar]
  13. Wardlaw CW. Banana Diseases, Including Plantains and Abaca London: Longmans; 1961 p 648
    [Google Scholar]
  14. Geering A, Pooggin M, Olszewski N, Lockhart B, Thomas JE. Characterisation of Banana streak Mysore virus and evidence that its DNA is integrated in the B genome of cultivated Musa. Arch Virol 2005; 150:787–796 [CrossRef][PubMed]
    [Google Scholar]
  15. Vo JN, Campbell PR, Mahfuz NN, Ramli R, Pagendam D et al. Characterization of the banana streak virus capsid protein and mapping of the immunodominant continuous B-cell epitopes to the surface-exposed N terminus. J Gen Virol 2016; 97:3446–3457 [CrossRef][PubMed]
    [Google Scholar]
  16. Netherton CL, Wileman T. Virus factories, double membrane vesicles and viroplasm generated in animal cells. Curr Opin Virol 2011; 1:381–387 [CrossRef][PubMed]
    [Google Scholar]
  17. Lesemann D, Casper R. An isometric plant virus associated with specific inclusions. Phytopathology 1973; 63:1118–1124
    [Google Scholar]
  18. Dzahini-Obiatey H, Fox R. Early signs of infection in Cacao swollen shoot virus (CSSV) inoculated cocoa seeds and the discovery of the cotyledons of the resultant plants as rich sources of CSSV. African Journal of Biotechnology 2010; 9:593–603
    [Google Scholar]
  19. Harper G, Hart D, Moult S, Hull R. Detection of Banana streak virus in field samples of bananas from Uganda. Annals of Applied Biology 2002; 141:247–257 [CrossRef]
    [Google Scholar]
  20. Hull R, Shepherd RJ, Harvey JD. Cauliflower mosaic virus: an improved purification procedure and some properties of the virus particles. J Gen Virol 1976; 31:93–100 [CrossRef]
    [Google Scholar]
  21. Carluccio AV, Zicca S, Stavolone L. Hitching a ride on vesicles: cauliflower mosaic virus movement protein trafficking in the endomembrane system. Plant Physiol 2014; 164:1261–1270
    [Google Scholar]
  22. Geering ADW, Olszewski NE, Harper G, Lockhart BEL, Hull R et al. Banana contains a diverse array of endogenous badnaviruses. J Gen Virol 2005; 86:511–520 [CrossRef][PubMed]
    [Google Scholar]
  23. Duroy P-O, Laboureau N, Seguin J, Rajendran R, Pooggin M et al. Natural resistance of the diploid Musa balbisiana Piang Klutuk Wulung (PKW) banana plant to infectious endogenous Banana streak virus sequences is driven by transcriptional gene silencing 2017: Abstract, COST iPLANTA CA15223, WG1 Meeting Comparing siRNA and miRNA technology and role for improving perennial plants. France: Bordeaux; 2018 pp 17–18
  24. Hafrén A, Macia J-L, Love AJ, Milner JJ, Drucker M 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:E2026–E2035 [CrossRef]
    [Google Scholar]
  25. Schoelz JE, Angel CA, Nelson RS, Leisner SM. A model for intracellular movement of cauliflower mosaic virus: the concept of the mobile virion factory. J Exp Bot 2016; 67:2039–2048 [CrossRef][PubMed]
    [Google Scholar]
  26. Cheng CP, Lockhart BE, Olszewski NE. The ORF I and II proteins of Commelina yellow mottle virus are virion-associated. Virology 1996; 223:263–271 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.001498
Loading
/content/journal/jgv/10.1099/jgv.0.001498
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error