Submitted Successfully!
To reward your contribution, here is a gift for you: A free trial for our video production service.
Thank you for your contribution! You can also upload a video entry or images related to this topic.
Version Summary Created by Modification Content Size Created at Operation
1 -- 1661 2022-08-07 03:50:39 |
2 format correct + 5 word(s) 1666 2022-08-08 02:30:57 |

Video Upload Options

Do you have a full video?

Confirm

Are you sure to Delete?
Cite
If you have any further questions, please contact Encyclopedia Editorial Office.
Sun, Y.;  Spellman-Kruse, A.;  Folimonova, S.Y. Examples of Xylem-Invading Viruses. Encyclopedia. Available online: https://encyclopedia.pub/entry/25924 (accessed on 24 June 2024).
Sun Y,  Spellman-Kruse A,  Folimonova SY. Examples of Xylem-Invading Viruses. Encyclopedia. Available at: https://encyclopedia.pub/entry/25924. Accessed June 24, 2024.
Sun, Yong-Duo, Arianna Spellman-Kruse, Svetlana Y. Folimonova. "Examples of Xylem-Invading Viruses" Encyclopedia, https://encyclopedia.pub/entry/25924 (accessed June 24, 2024).
Sun, Y.,  Spellman-Kruse, A., & Folimonova, S.Y. (2022, August 07). Examples of Xylem-Invading Viruses. In Encyclopedia. https://encyclopedia.pub/entry/25924
Sun, Yong-Duo, et al. "Examples of Xylem-Invading Viruses." Encyclopedia. Web. 07 August, 2022.
Examples of Xylem-Invading Viruses
Edit

Viruses are trailblazers in hijacking host systems for their own needs. Plant viruses have been shown to exploit alternative avenues of translocation within a host, including a challenging route through the xylem, to expand their niche and establish systemic spread, despite apparent host-imposed obstacles.

plant virus vascular loading xylem movement virus-xylem interaction

1. Introduction

In plants, the xylem tissue functions to transport water and minerals unidirectionally, from roots towards the aboveground parts [1][2]. At the same time, the phloem serves as a highway for the bidirectional distribution of sugars, nutrients, and hormones, in a source-to-sink manner. Apparently, the microaerophilic environment of the phloem is thought to provide a suitable niche for plant-infecting viruses. In the past decades, considerable knowledge of the phloem structure and its role in virus colonization has been gained. It is widely accepted that plant viruses utilize the phloem as the main route for the long-distance spread within a host, along with photoassimilate translocation, and, thus, the virus–phloem interplay has been a hot area in plant virus research [3][4][5]. However, virus–xylem interactions have been largely overlooked. On the one hand, functional xylem cells are mainly dead cells, which lack the cellular machinery that the virus needs for the synthesis of its proteins, replication, and assembly of new particles. On the other hand, the movement of a virus from an adjacent cell containing a protoplast to the apoplastic compartment of the xylem requires passing across an intact plasma membrane and a thickened secondary cell wall. With that, the xylem seems to be a challenging territory for the plant viruses and an unlikely area to serve for virus occupation. Interestingly, a growing number of studies, especially those in more recent years, point to the importance of the relationship between the vascular xylem in the plant host–virus interactions and disease production [6][7][8]. Viruses do find ways out to blaze trails in the xylem, as they constantly evolve and adapt to environmental challenges. Some studies even suggest that, for specific viruses, active virus accumulation takes place in immature xylem-associated cells, rather than in phloem-associated cells. For instance, virions of Lettuce necrotic yellows virus (LNYV) were not observed in the thin sections of the phloem cells of tobacco (Nicotiana glutinosa L.). Instead, the virus particles were successfully visualized in juvenile xylem cells [9]. With evidence generated from these studies, it seems that at least some plant viruses can manipulate xylem cells to replicate and spread to distal plant parts.
Research on the virus-xylem interplay can be traced back to the 1930s when Johnson revealed the presence of Tobacco mosaic virus (TMV) in the xylem guttation from tomato (Solanum lycopersicum L.) [10]. Since guttation fluid is the exudation of xylem sap, finding virus particles in this exudate demonstrated that infectious TMV could spread via the xylem conduit. Later, the presence of several plant viruses was observed in the xylem of many herbaceous plant hosts. Virions of Beet necrotic yellow vein virus (BNYVV) were frequently found in the undifferentiated and mature xylem vessel elements and xylem parenchyma of sugar beet (Beta vulgaris L.) [11]. The infectious virions of Tomato mosaic virus (ToMV) and Pepper mild mottle virus (PMMV) were recovered and visualized from the guttation fluid of tomato (Lycopersicon esculentum Mill.) and green pepper (Capsicum annuum L.), respectively [12]. With such evidence on hand, French and colleagues tested the potential capability of a diverse group of viruses to move in the xylem sap. Strikingly, the respective results showed that plant viruses from at least ten genera could employ the xylem tissue as a conduit for their transportation [13]. Compared to those in the herbaceous hosts, studies on virus–xylem interactions in perennial woody plants are limited. The reason could be due largely to the fact that fewer viruses have been reported to infect the xylem of a tree. Some time ago, Blueberry shoestring virus (BSV) was shown to achieve the long-distance movement through the xylem, in addition to the phloem of a low woody shrub, highbush blueberry (Vaccinium corymbosum L.) [14]. Furthermore, a recent study on Citrus tristeza virus (CTV) reignited an interest in exploring virus–xylem interactions in perennial woody plants by demonstrating that CTV can invade and further develop a ‘clustered oasis’ of infected cells in the xylem tissue of Citrus macrophylla Wester [7]. It is possible that hijacking the xylem cells could be a strategy adapted by plant viruses to promote infection in a broad range of plant host.
The healthy and functional xylem of a plant is important to its vigorous growth. The invasion of certain vascular pathogens was shown to damage the xylem function and trigger disease syndromes. For instance, a xylem-residing Verticillium dahliae Klebahn, a filamentous fungus, could secret a toxic protein named xylanase 4 to degrade the xylem’s cell walls and induce necrosis. The destruction of the xylem vessels results in wilt syndrome in the infected cotton plants [15]. In contrast, the connection between the virus invasion of the xylem and disease development has not been clearly demonstrated, largely because the vascular xylem is not the main or the sole tissue that the virus colonizes. Other tissues, such as the epidermis, mesophyll, cortex, and phloem, provide more suitable niches for plant viruses, and the phenotypes induced by the virus in those tissues are usually more easily noticeable. For instance, while Brome mosaic virus (BMV) is able to invade xylem cells in oat (Arena sativa L.) and barley (Hordeum vulgare L.), leaf mosaic symptoms are attributed to the virus accumulation in the juvenile phloem and mesophyll cells [16]. In contrast, there is an exception where CTV triggers an obvious phenotype in the vascular tissues of several different citrus varieties, including the xylem. Remarkably, the invasion of CTV into the immature xylem treachery elements and ray parenchyma cells in the citrus plants was shown to account for the development of one of the major disease syndromes induced by this virus. Such invasion interrupts the differentiation of the xylem and phloem cells in the vasculature and eventually triggers the stem pitting disease, which is accompanied by the loss of tree vigor and production of unmarketable fruit. The manifestation of this syndrome in the citrus trees may emerge months or years after CTV inoculation [7][17]. Such phenotype in the CTV-colonized citrus stems and branches could be contingent upon the continuous growth of the xylem rings and the virus xylem invasion. Consequently, the severity of disease is enhanced with tree growth. It is possible that some xylem-invading viruses share similar mechanisms to trigger diseases in other hosts.

2. Examples of Xylem-Invading Viruses

To date, at least 39 plant viruses have been reportedly found in the xylem-associated cells of many different hosts, including herbaceous and perennial woody plants (Table 1). Interestingly, the majority of xylem-invading viruses (35/39) studied to date belong to the group of positive-sense single-stranded RNA (+ssRNA) viruses in the following families: AlphaflexiviridaeBenyviridaeBromoviridaeClosteroviridaePotyviridaeSecoviridaeSobemoviridaeTombusviridae, and Virgaviridae (Table 1) [6][7][8][10][11][12][13][14][16][18][19][20][21][22][23][24][25][26][27][28][29][30][31][32][33][34][35][36]. Other viruses are three single-stranded DNA (ssDNA) viruses in the family of Geminiviridae [37] and a negative-sense RNA virus in the family Rhabdoviridae (Table 1) [9]. With such a broad range of virus families, the morphology of xylem-invading viruses is quite diverse. Virions produced by those viruses could be long flexuous or short rigid rod-like particles or have icosahedral, twinned-icosahedral, or bullet-like shape and range from approximately 10 nm to over 2000 nm (Table 2). The diversity of these viruses suggests that the xylem exploitation appears to be a widely adapted strategy for plant viruses, which might be an evolutionary consequence of the virus niche expansion.
Table 1. Current list of viruses found in the xylem of herbaceous and perennial plant hosts.
Table 2. Characteristic features of xylem-invading viruses.

References

  1. Schuetz, M.; Smith, R.; Ellis, B. Xylem tissue specification, patterning, and differentiation mechanisms. J. Exp. Bot. 2012, 64, 11–31.
  2. Růžička, K.; Ursache, R.; Hejátko, J.; Helariutta, Y. Xylem development—From the cradle to the grave. New Phytol. 2015, 207, 519–535.
  3. Folimonova, S.Y.; Tilsner, J. Hitchhikers, highway tolls and roadworks: The interactions of plant viruses with the phloem. Curr. Opin. Plant Biol. 2018, 43, 82–88.
  4. Kappagantu, M.; Collum, T.D.; Dardick, C.; Culver, J.N. Viral hacks of the plant vasculature: The role of phloem alterations in systemic virus infection. Annu. Rev. Virol. 2020, 7, 351–370.
  5. Lewis, J.D.; Knoblauch, M.; Turgeon, R. The phloem as an arena for plant pathogens. Annu. Rev. Phytopathol. 2022, 60, 4.1–4.20.
  6. Mochizuki, T.; Nobuhara, S.; Nishimura, M.; Ryang, B.S.; Naoe, M.; Matsumoto, T.; Kosaka, Y.; Ohki, S.T. The entry of cucumber mosaic virus into cucumber xylem is facilitated by co-infection with zucchini yellow mosaic virus. Arch. Virol. 2016, 161, 2683–2692.
  7. Sun, Y.D.; Folimonova, S.Y. Location matters: From changing a presumption about the Citrus tristeza virus tissue tropism to understanding the stem pitting disease. New Phytol. 2022, 233, 631–638.
  8. Wan, J.; Cabanillas, D.G.; Zheng, H.; Laliberte, J.F. Turnip mosaic virus moves systemically through both phloem and xylem as membrane-associated complexes. Plant Physiol. 2015, 167, 1374–1388.
  9. Chambers, T.C.; Francki, R.I. Localization and recovery of lettuce necrotic yellows virus from xylem tissues of Nicotiana glutinosa. Virology 1966, 29, 673–676.
  10. Johnson, J. Factors relating to the control of ordinary tobacco mosaic. J. Agric. Res. 1937, 54, 239–273.
  11. Dubois, F.; Sangwan, R.S.; Sangwan-Norreel, B.S. Spread of beet necrotic yellow vein virus in infected seedlings and plants of sugar beet (Beta vulgaris). Protoplasma 1994, 179, 72–82.
  12. French, C.J.; Elder, M.; Skelton, F. Recovering and Identifying Infectious Plant Viruses in Guttation Fluid. HortScience 1993, 28, 746–747.
  13. French, C.J.; Elder, M. Virus particles in guttate and xylem of infected cucumber (Cucumis sativus L.). Ann. Appl. Biol. 1999, 134, 81–87.
  14. Urban, L.A.; Ramsdell, D.C.; Klomparens, K.L.; Lynch, T.L.; Hancock, J.F. Detection of Blueberry Shoestring Virus in Xylem and Phloem Tissues of Highbush Blueberry. Phytopathology 1989, 79, 488–493.
  15. Wang, D.; Chen, J.Y.; Song, J.; Li, J.J.; Klosterman, S.J.; Li, R.; Kong, Z.Q.; Subbarao, K.V.; Dai, X.F.; Zhang, D.D. Cytotoxic function of xylanase VdXyn4 in the plant vascular wilt pathogen Verticillium dahliae. Plant Physiol. 2021, 187, 409–429.
  16. Paliwal, Y.C. Electron microscopy of Bromegrass mosaic virus in infected leaves. J. Ultrastruct. Res. 1970, 30, 491–502.
  17. Sun, Y.D.; Folimonova, S.Y. The p33 protein of Citrus tristeza virus affects viral pathogenicity by modulating a host immune response. New Phytol. 2019, 221, 2039–2053.
  18. Betti, C.; Lico, C.; Maffi, D.; D’Angeli, S.; Altamura, M.M.; Benvenuto, E.; Faoro, F.; Baschieri, S. Potato virus X movement in Nicotiana benthamiana: New details revealed by chimeric coat protein variants. Mol. Plant Pathol. 2012, 13, 198–203.
  19. Giunchedi, L.; Poggi-Pollini, C. Immunogold-silver localization of Beet necrotic yellow vein virus antigen in susceptible and moderately resistant Sugar-beets. Phytopathol. Mediterr. 1988, 27, 1–6.
  20. Ding, X.S.; Boydston, C.M.; Nelson, R.S. Presence of Brome mosaic virus in barley guttation fluid and its association with localized cell death response. Phytopathology 2001, 91, 440–448.
  21. Kozieł, E.; Otulak, K.; Lockhart, B.E.L.; Garbaczewska, G. Subcelullar localization of proteins associated with Prune dwarf virus replication. Eur. J. Plant. Pathol. 2017, 149, 653–668.
  22. Bar-Joseph, M.; Josephs, R.; Cohen, J. Carnation yellow fleck virus particles “in vivo”. A structural analysis. Virology 1977, 81, 144–151.
  23. Khan, J.A.; Lohuis, D.; Bakardjieva, N.; Peters, D.; Goldbach, R.; Dijkstra, J. Interference between two strains of Bean common mosaic virus is accompanied by suppression of symptoms without affecting replication of the challenging virus. J. Phytopathol. 1994, 140, 260–268.
  24. Khan, J.A.; Lohuis, H.; Goldbach, R.W.; Dijkstra, J. Distribution and localization of bean common mosaic virus and bean black root virus in stems of doubly infected bean plants. Arch. Virol. 1994, 138, 95–104.
  25. Otulak, K.; Garbaczewska, G. Cytopathological potato virus Y structures during Solanaceous plants infection. Micron 2012, 43, 839–850.
  26. Gergerich, R.C.; Scott, H.A. Evidence that virus translocation and virus infection of non-wounded cells are associated with transmissibility by leaf-feeding beetles. J. Gen. Virol. 1988, 69, 2935–2938.
  27. Opalka, N.; Brugidou, C.; Bonneau, C.; Nicole, M.; Beachy, R.N.; Yeager, M.; Fauquet, C. Movement of rice yellow mottle virus between xylem cells through pit membranes. Proc. Natl. Acad. Sci. USA 1998, 95, 3323–3328.
  28. Schneider, I.R.; Worley, J.F. Rapid entry of infectious particles of southern bean mosaic virus into living cells following transport of the particles in the water stream. Virology 1959, 8, 243–249.
  29. Appiano, A.; D’Agostino, G. Distribution of tomato bushy stunt virus in root tips of systemically infected Gomphrena globosa. J. Ultrastruct. Res. 1983, 85, 239–248.
  30. Manabayeva, S.A.; Shamekova, M.; Park, J.W.; Ding, X.S.; Nelson, R.S.; Hsieh, Y.C.; Omarov, R.T.; Scholthof, H.B. Differential requirements for Tombusvirus coat protein and P19 in plants following leaf versus root inoculation. Virology 2013, 439, 89–96.
  31. Russo, M.; Martelli, G.P.; Quacquarelli, A. Occurrence of artichoke mottle crinkle virus in leaf vein xylem. Virology 1967, 33, 555–558.
  32. Verchot, J.; Driskel, B.A.; Zhu, Y.; Hunger, R.M.; Littlefield, L.J. Evidence that soilborne wheat mosaic virus moves long distance through the xylem in wheat. Protoplasma 2001, 218, 57–66.
  33. Jones, R.A.C. Systemic movement of Potato mop-top virus in tobacco may occur through the xylem. J. Phytopathol. 1975, 82, 352–355.
  34. Moreno, I.M.; Thompson, J.R.; Garcia-Arenal, F. Analysis of the systemic colonization of cucumber plants by Cucumber green mottle mosaic virus. J. Gen. Virol. 2004, 85, 749–759.
  35. Fribourg, C.E.; Koenig, R.; Lesemann, D.-E. A new tobamovirus from Passiflora edulis in Peru. Phytopathology 1987, 77, 486–491.
  36. Garbaczewska, G.; Otulak, K.; Chouda, M.; Chrzanowska, M. Ultrastructural studies of plasmodesmatal and vascular translocation of tobacco rattle virus (TRV) in tobacco and potato. Acta Physiol. Plant. 2012, 34, 1229–1238.
  37. Rasheed, M.S.; Selth, L.A.; Koltunow, A.M.G.; Randles, J.W.; Rezaian, M.A. Single-stranded DNA of Tomato leaf curl virus accumulates in the cytoplasm of phloem cells. Virology 2006, 348, 120–132.
More
Information
Subjects: Virology
Contributors MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register : , ,
View Times: 613
Revisions: 2 times (View History)
Update Date: 08 Aug 2022
1000/1000
Video Production Service