Potato Virus Y: Comparison
Please note this is a comparison between Version 2 by Rita Xu and Version 1 by Michael Taliansky.

Potato virus Y origin, emergence and evolution

Potato virus Y origin, emergence and evolution.

  • Potato virus Y, plant virus, antivirus resistance

Note:All the information in this draft can be edited by authors. And the entry will be online only after authors edit and submit it.

1. Introduction

Potato virus Y (PVY) is the type species of the genus Potyvirus, one of the largest groups of plant viruses, containing c. 160 species [1,2][1][2]. Potyviruses are transmitted by aphids and cause economically damaging diseases in crop plants. PVY exists as several strains and has become one of the most economically important pathogens of potato and the most important virus [3], and it occurs commonly wherever potatoes are grown. The Andean region of South America is the centre of origin of potato and many wild and domesticated species grow there (Figure 1a). After the discovery and colonization of the Americas by Europeans in the 16th century, tubers of one species of domesticated potato, Solanum tuberosum, were taken to Europe, and from there, over time, to the rest of the world [4,5][4][5]. Potato consumption grew in popularity in the 19th century, and it became an established staple food in many countries. Potatoes are vegetatively propagated, with progeny “seed” tubers being used to establish the next crop, and, unknown at the time, potato viruses were also transported with tubers. Potato viruses were first identified in the 1930s [6[6][7],7], and now more than 50 viruses affecting potato are known, although only a few, including PVY, cause economically important diseases [3]. Potato is the world’s third most important staple food crop and an important crop supporting food security in developing countries, where potato production now exceeds that in the developed world, and viruses are major constraints on potato production systems [3,8][3][8].

Figure 1 (a) Potato cultivation in the high Andes of Bolivia; (b) symptoms of O (ordinary) strain Potato virus Y (PVYO) on leaves of Solanum tuberosum Group Phureja (c) necrotic local lesions (indicated by white arrow heads) elicited by PVYO in the inoculated leaves of potato cv Atlantic; (d) necrotic symptoms induced by N (necrotic) strain Potato virus Y (PVYN) in tobacco leaves.

Human activity has played a major part in the spread of PVY from the South American Andes to the rest of the world, particularly through trade in plant material of unknown disease status. Since emerging from the Andean region, PVY has also become a major pathogen of tobacco and solanaceous vegetable crops [9–13][9][10][11][12][13]. This review highlights current knowledge of PVY population structure, epidemiology and economic impacts, mostly drawn from research on virus infections in potato. We believe that to effectively control the virus and prevent the emergence of new strains in key crops, future research should be strongly focused on host resistance and factors driving virus evolution and spread. Therefore, we also describe natural resistance mechanisms to PVY and how they can be modulated by rising temperatures under global warming. Modern biotechnology can play a role by developing genetically edited PVY-resistant crops as well as producing “vaccinated” plants by priming their antiviral defences through RNA silencing.

2. PVY Population Structure

PVY was first identified by Smith [6], and several strains infecting potato were subsequently described in the early 20th century. Five major strain groups have now been recognised [14–16][14][15][16]. The first strains to be recognised were the O (ordinary) (Figure 1b), N (necrotic) and C (common) strains. These strains were characterised by biological properties and symptoms in potato hosts carrying strain-specific resistance genes (hypersensitive (HR) or N genes) [16–18][16][17][18]. The O, N and C strains were distinguished using potato cultivars carrying the genes Ny or Nc, which displayed necrotic spots on leaves when inoculated with O or C, respectively (Figure 1d) [17]. The N strain induces a systemic veinal necrosis in tobacco (Figure 1c) but generally no HR and only mild or no symptoms in potato leaves, and the C strain (PVYC) causes economically important diseases in other solanaceous crops including tobacco, tomato and pepper. In the 1980s, additional strains were reported where although mild or no symptoms were observed in leaves, some induced severe symptoms in potato tubers, such as potato tuber necrotic ringspot disease (PTNRD) [19,20][19][20]. Genome sequencing has revealed that the virus genomes of these isolates comprise sequences derived from O and N strains, these recombinant isolates included PVYNTN and PVYN-Wi [19,21–23][19][21][22][23]. The resistance gene Nz is effective against PVYZ (shown to be the recombinant NTN). However, other recombinant strains such as PVYN-Wi were not controlled by Nz, and they induce mild foliar symptoms with no PTNRD [18].

Phylogenetic analysis of 460 whole-genome sequences of PVY, collected from infected plants worldwide, showed that PVY originated in the Andes of South America, the centre of origin of the potato and where potatoes were first domesticated [14,15][14][15]. The date of origin (time to most recent common potyvirus ancestor) of the PVY population was estimated to be 1860 YBP. The maximum likelihood tree analysis largely supported the previous classification of strains based on host reactions, and five phylogroups were identified. Analysis of the nonrecombinant sequences produced three main lineages: the N phylogroup, which is widespread in South America and may only have spread to the rest of the world recently; the O phylogroup, isolates of which were found mostly from plants outside South America, and a branch of O, the C phylogroup, with no isolates found among South American samples. Moreover, the C isolates were often found in non-potato hosts, suggesting they may have diverged outside the Andes, possibly in Europe [15]. The analysis suggests that diversification and emergence of some of the current strains of PVY may have occurred outside South America, possibly in Europe. The first potato breeding programmes were based on a narrow genetic foundation of only a few introductions of potato, developing varieties through in-breeding and selection [4,14][4][14]. The introduction of new germplasm to combat susceptibility to late blight into potato breeding programmes in the mid-19th century probably led to PVY strain diversification, as this material also contained PVY resistance genes. Approximately half of the sequences analysed in the study by Fuentes et al. [15] comprised recombinants from N and O sequences and formed two further lineages, the R1 and R2 phylogroups. Recombinant isolates came to prominence in the 1980s and quickly spread, displacing other PVY strains in potato production systems, probably because they were uncontrolled by N genes and the mild foliar symptoms in many modern varieties enabled them to proliferate in seed crops because they escaped visual inspections [18]. Thus, since PVY was distributed from the Andes in potato tubers, the PVY population has evolved, with new strains emerging to infect non-potato hosts as well as overcome resistance of potato hosts, and human activity has been an important driver of this process [18].

References

  1. Wylie, J.; Adams, M.; Chalam, C.; Kreuze, J.; López-Moya, J.J.; Ohshima, K.; Praveen, S.; Rabenstein, F.; Stenger, D.; Wang, A.; et al. ICTV Virus Taxonomy Profile: Potyviridae. J. Gen. Virol. 2017, 98, 352.
  2. ICTV Report on Virus Classification and Taxon Positive-sense RNA Viruses > Potyviridae. Genus Potyvirus. Available online: https://talk.ictvonline.org/ictv-reports/ictv_online_report/positive-sense-rna-viruses/w/potyviridae/572/genus-potyvirus (accessed on 13 November 2020).
  3. Kreuze, F.; Souza-Dias, J.A.C.; Jeevalatha, A.; Figueira, A.R.; Valkonen, J.P.T.; Jones, R.A.C. Viral Diseases in Potato. In The Potato Crop: Its Agricultural, Nutritional and Social Contribution to Humankind; Campos, H., Ortiz, O., Eds.; Springer: Berlin/Heidelberg, Germany, 2020; pp. 389–430.
  4. Bradshaw, E. Potato-breeding strategy. In Potato Biology and Biotechnology: Advances and Perspectives; Vreugdenhil, D., Ed.; Elsevier: Amsterdam, The Netherlands, 2007; pp. 157–177.
  5. Gibbs, J.; Hajizadeh, M.; Ohshima, K.; Jones, R.A.C. The Potyviruses: An Evolutionary Synthesis Is Emerging. Viruses 2020, 12, 132.
  6. Smith, M. On the composite nature of certain potato virus diseases of the mosaic group as revealed by the use of plant indicators and selective methods of transmission. Proc. R. Soc. Lond. 1931, 109, 251–266.
  7. Salaman, N. Crinkle ‘A’ an infectious disease of the potato. Proc. R. Soc. B 1930, doi:10.1098/rspb.1930.0011.
  8. Devaux, ; Goffart, J.-P.; Petsakos, A.; Kromann, P.; Gatto, M.; Okello, J.; Suarez, V.; Hareau, G. Global Food Security, contributions form sustainable potato Agri-food systems. In The Potato Crop: Its Agricultural, Nutritional and Social Contribution to Humankind; Campos, H., Ortiz, O., Eds.; Springer: Berlin/Heidelberg, Germany, 2020; pp. 3–36.
  9. Kerlan, C.; Moury, Potato virus, Y. In Encyclopedia of Virology, 3rd ed.; Mahy, B.M.J., van Regenmortel, M.H.V., Eds.; Elsevier: Amsterdam, The Netherlands, 2008.
  10. Scholthof, B.; Adkins, S.; Czosnek, H.; Palukaitis, P.; Jacquot, E.; Hohn, T.; Hohn, B.; Saunders, K.; Candresse, T.; Ahlquist, P.; et al. Top 10 plant viruses in molecular plant pathology. Mol. Plant Pathol. 2011, 12, 938–954.
  11. Romero, ; Blanco-Urgoiti, B.; Soto, M.J.; Fereres, A.; Ponz, F. Characterization of typical pepper-isolates of PVY reveals multiple pathotypes within 381 a single genetic strain. Virus Res. 2001, 79, 71–80.
  12. Morel, ; Gognalons, P.; Guilbaud, L.; Caranta, C.; Gebre-Selassie, K.; Marchoux, G.; Jacquemond, M. Biological and molecular characterization of two tomato strains of potato virus Y (PVY). Acta Physiol. Plant 2000, 22, 336–343.
  13. Latorre, A.; Flores, V.; Marholz, G. Effect of potato virus Y on growth, yield, and chemical composition of flue-cured tobacco in Chile. Plant Dis. 1984, 68, 884–886.
  14. Gibbs, J.; Ohshima, K.; Yasaka, R.; Mohammadi, M.; Gibbs, M.J.; Jones, R.A.C. The phylogenetics of the global population of potato virus Y and its necrogenic recombinants. Virus Evol. 2017, 3, 1–12.
  15. Fuentes, ; Jones, R.A.C.; Matsuoka, H.; Ohshima, K.; Kreuze, J.; Gibbs, A.J. Potato virus, Y.; the Andean connection. Virus Evol. 2019, 5, vez037, doi:10.1093/ve/vez037.
  16. Jones, A.C.; Vincent, S.J. Strain-specific hypersensitive and extreme resistance phenotypes elicited by potato virus Y among 39 potato cultivars released in three world regions over a 117 Yyar period’. Plant Dis. 2018, 102 185–196.
  17. Jones, A.C. Strain group specific and virus specific hypersensitive reactions to infection with potyviruses in potato cultivars’. Ann. Appl. Biol. 1990, 117, 93–105.
  18. Gray, S.; Power, G. Anthropogenic influences on emergence of vector-borne plant viruses: The persistent problem of potato virus Y. Curr. Opin. Virol. 2018, 33, 177–183.
  19. Gray, ; De Boer, S.H.; Lorenzen, J.; Karasev, A.V.; Whitworth, J.; Nolte, P.; Singh, R.; Boucher, A.; Xu, H. Potato virus Y: An evolving concern for potato crops in the United States and Canada. Plant Dis. 2010, 94, 1384–1397.
  20. Barker, ; McGeachy, K.; Toplak, N.; Gruden, K.; Žel, J.; Browning, I. Comparison of genome sequence of PVY isolates with biological properties. Am. J. Potato Res. 2009, 86, 227–238.
  21. Glais, ; Tribodet, M.; Kerlan, C. Genomic variability in Potato potyvirus Y (PVY): Evidence that PVY(N)W and PVY(NTN) variants are single to multiple recombinants between PVY(O) and PVY(N) isolates. Arch. Virol. 2002, 147, 363–378.
  22. Green, J.; Brown, C.J.; Gray, S.M.; Karasev, A.V. Phylogenetic study of recombinant strains of Potato virus Y. Virology 2017, 507, 40–52.
  23. Karasev, V.; Hu, X.J.; Brown, C.J.; Kerlan, C.; Nikolaeva, O.V.; Crosslin, J.M.; Gray, S.M. Genetic diversity of the ordinary strain of Potato virus Y (PVY) and origin of recombinant PVY strains. Phytopathology 2011, 101, 778–785.

References

  1. Wylie, J.; Adams, M.; Chalam, C.; Kreuze, J.; López-Moya, J.J.; Ohshima, K.; Praveen, S.; Rabenstein, F.; Stenger, D.; Wang, A.; et al. ICTV Virus Taxonomy Profile: Potyviridae. J. Gen. Virol. 2017, 98, 352.
  2. ICTV Report on Virus Classification and Taxon Positive-sense RNA Viruses > Potyviridae. Genus Potyvirus. Available online: https://talk.ictvonline.org/ictv-reports/ictv_online_report/positive-sense-rna-viruses/w/potyviridae/572/genus-potyvirus (accessed on 13 November 2020).
  3. Kreuze, F.; Souza-Dias, J.A.C.; Jeevalatha, A.; Figueira, A.R.; Valkonen, J.P.T.; Jones, R.A.C. Viral Diseases in Potato. In The Potato Crop: Its Agricultural, Nutritional and Social Contribution to Humankind; Campos, H., Ortiz, O., Eds.; Springer: Berlin/Heidelberg, Germany, 2020; pp. 389–430.
  4. Bradshaw, E. Potato-breeding strategy. In Potato Biology and Biotechnology: Advances and Perspectives; Vreugdenhil, D., Ed.; Elsevier: Amsterdam, The Netherlands, 2007; pp. 157–177.
  5. Gibbs, J.; Hajizadeh, M.; Ohshima, K.; Jones, R.A.C. The Potyviruses: An Evolutionary Synthesis Is Emerging. Viruses 2020, 12, 132.
  6. Smith, M. On the composite nature of certain potato virus diseases of the mosaic group as revealed by the use of plant indicators and selective methods of transmission. Proc. R. Soc. Lond. 1931, 109, 251–266.
  7. Salaman, N. Crinkle ‘A’ an infectious disease of the potato. Proc. R. Soc. B 1930, doi:10.1098/rspb.1930.0011.
  8. Devaux, ; Goffart, J.-P.; Petsakos, A.; Kromann, P.; Gatto, M.; Okello, J.; Suarez, V.; Hareau, G. Global Food Security, contributions form sustainable potato Agri-food systems. In The Potato Crop: Its Agricultural, Nutritional and Social Contribution to Humankind; Campos, H., Ortiz, O., Eds.; Springer: Berlin/Heidelberg, Germany, 2020; pp. 3–36.
  9. Kerlan, C.; Moury, Potato virus, Y. In Encyclopedia of Virology, 3rd ed.; Mahy, B.M.J., van Regenmortel, M.H.V., Eds.; Elsevier: Amsterdam, The Netherlands, 2008.
  10. Scholthof, B.; Adkins, S.; Czosnek, H.; Palukaitis, P.; Jacquot, E.; Hohn, T.; Hohn, B.; Saunders, K.; Candresse, T.; Ahlquist, P.; et al. Top 10 plant viruses in molecular plant pathology. Mol. Plant Pathol. 2011, 12, 938–954.
  11. Romero, ; Blanco-Urgoiti, B.; Soto, M.J.; Fereres, A.; Ponz, F. Characterization of typical pepper-isolates of PVY reveals multiple pathotypes within 381 a single genetic strain. Virus Res. 2001, 79, 71–80.
  12. Morel, ; Gognalons, P.; Guilbaud, L.; Caranta, C.; Gebre-Selassie, K.; Marchoux, G.; Jacquemond, M. Biological and molecular characterization of two tomato strains of potato virus Y (PVY). Acta Physiol. Plant 2000, 22, 336–343.
  13. Latorre, A.; Flores, V.; Marholz, G. Effect of potato virus Y on growth, yield, and chemical composition of flue-cured tobacco in Chile. Plant Dis. 1984, 68, 884–886.
  14. Gibbs, J.; Ohshima, K.; Yasaka, R.; Mohammadi, M.; Gibbs, M.J.; Jones, R.A.C. The phylogenetics of the global population of potato virus Y and its necrogenic recombinants. Virus Evol. 2017, 3, 1–12.
  15. Fuentes, ; Jones, R.A.C.; Matsuoka, H.; Ohshima, K.; Kreuze, J.; Gibbs, A.J. Potato virus, Y.; the Andean connection. Virus Evol. 2019, 5, vez037, doi:10.1093/ve/vez037.
  16. Jones, A.C.; Vincent, S.J. Strain-specific hypersensitive and extreme resistance phenotypes elicited by potato virus Y among 39 potato cultivars released in three world regions over a 117 Yyar period’. Plant Dis. 2018, 102 185–196.
  17. Jones, A.C. Strain group specific and virus specific hypersensitive reactions to infection with potyviruses in potato cultivars’. Ann. Appl. Biol. 1990, 117, 93–105.
  18. Gray, S.; Power, G. Anthropogenic influences on emergence of vector-borne plant viruses: The persistent problem of potato virus Y. Curr. Opin. Virol. 2018, 33, 177–183.
  19. Gray, ; De Boer, S.H.; Lorenzen, J.; Karasev, A.V.; Whitworth, J.; Nolte, P.; Singh, R.; Boucher, A.; Xu, H. Potato virus Y: An evolving concern for potato crops in the United States and Canada. Plant Dis. 2010, 94, 1384–1397.
  20. Barker, ; McGeachy, K.; Toplak, N.; Gruden, K.; Žel, J.; Browning, I. Comparison of genome sequence of PVY isolates with biological properties. Am. J. Potato Res. 2009, 86, 227–238.
  21. Glais, ; Tribodet, M.; Kerlan, C. Genomic variability in Potato potyvirus Y (PVY): Evidence that PVY(N)W and PVY(NTN) variants are single to multiple recombinants between PVY(O) and PVY(N) isolates. Arch. Virol. 2002, 147, 363–378.
  22. Green, J.; Brown, C.J.; Gray, S.M.; Karasev, A.V. Phylogenetic study of recombinant strains of Potato virus Y. Virology 2017, 507, 40–52.
  23. Karasev, V.; Hu, X.J.; Brown, C.J.; Kerlan, C.; Nikolaeva, O.V.; Crosslin, J.M.; Gray, S.M. Genetic diversity of the ordinary strain of Potato virus Y (PVY) and origin of recombinant PVY strains. Phytopathology 2011, 101, 778–785.
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