Archives of Virology

, Volume 163, Issue 6, pp 1449–1454 | Cite as

Host-associated selection of a P3 mutant of zucchini yellow mosaic virus affects viral infectivity in watermelon

  • Baoshan Kang
  • Bin Peng
  • Huijie Wu
  • Lifeng Liu
  • Wanwan Wu
  • Qinsheng Gu
Original Article


In this study, we found that the infectivity of zucchini yellow mosaic virus (ZYMV) in watermelon lines H1 and K6 changed from partial to complete after propagation in the susceptible watermelon line ZXG637. When using cucumber infected with strain ZYMV-CH87 as an inoculum (named ZYMV-CH87C), the mean incidences of infection in lines H1 and K6 were 6% and 11%, respectively. However, when these lines were inoculated with ZXG637 infected with ZYMV-CH87C (named ZYMV-637), 100% of the plants became infected. Sequencing of ZYMV from these different inoculums revealed two nucleotide changes in the P3 cistron in ZYMV-637, which resulted in changes in the amino acids at positions 768 and 857 of the P3 protein, compared with the original strain ZYMV-CH87. We named this variant the M768I857-variant. The M768I857-variant was detected at low levels (3.9%) in ZYMV-CH87C. When ZYMV-CH87C was passaged with ZXG637, the M768I857-variant was selected by the host, and the original sequence was replaced entirely after two passages. These results may be explained by host-associated selection due to an unknown host-encoded factor. Using the M768I857-variant as an inoculum, 100% of the H1 and K6 plants showed systemic symptoms. These results suggest that (1) changing the individual amino acids at the end of the P3 N-terminus induces resistance-breaking, and (2) the P3 N-terminus may be involved in host recognition.



This work was funded by the Central Public-Interest Scientific Institution Basal Research Fund and by the Agricultural Science and Technology Innovation Program.

Compliance with ethical standards

Conflict of interest

All authors declare that they have no conflicts of interest.

Ethical statements

The work has not been published previously and is not under consideration for publication elsewhere. All authors have agreed to the submission and to the order of their names on the title page; this article does not contain any studies with human participants or animals performed by any of the authors.


  1. 1.
    Acosta-Leal R, Duffy S, Xiong Z, Hammond RW, Elena SF (2011) Advances in plant virus evolution: translating evolutionary insights into better disease management. Phytopathology 101:1136–1148CrossRefPubMedGoogle Scholar
  2. 2.
    Amano M, Mochizuki A, Kawagoe Y, Iwahori K, Niwa K, Svoboda J, Maeda T, Imura Y (2013) High-resolution mapping of zym, a recessive gene for Zucchini yellow mosaic virus resistance in cucumber. TAG Theor Appl Genet Theoretische und angewandte Genetik 126:2983–2993CrossRefPubMedGoogle Scholar
  3. 3.
    Cervera H, Lalic J, Elena SF (2016) Effect of host species on the topography of fitness landscape for a plant RNA virus. J Virol 90:10160–10169CrossRefPubMedCentralGoogle Scholar
  4. 4.
    Choi SH, Hagiwara-Komoda Y, Nakahara KS, Atsumi G, Shimada R, Hisa Y, Naito S, Uyeda I (2013) Quantitative and qualitative involvement of P3N-PIPO in overcoming recessive resistance against Clover yellow vein virus in pea carrying the cyv1 gene. J Virol 87:7326–7337CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Chu M, Lopez-Moya JJ, Llave-Correas C, Pirone TP (1997) Two separate regions in the genome of the tobacco etch virus contain determinants of the wilting response of Tabasco pepper. Mol Plant-Microbe Interact: MPMI 10:472–480CrossRefPubMedGoogle Scholar
  6. 6.
    Chung BY, Miller WA, Atkins JF, Firth AE (2008) An overlapping essential gene in the Potyviridae. Proc Natl Acad Sci USA 105:5897–5902CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Cui X, Wei T, Chowda-Reddy RV, Sun G, Wang A (2010) The Tobacco etch virus P3 protein forms mobile inclusions via the early secretory pathway and traffics along actin microfilaments. Virology 397:56–63CrossRefPubMedGoogle Scholar
  8. 8.
    Desbiez C, Gal-On A, Girard M, Wipf-Scheibel C, Lecoq H (2003) Increase in zucchini yellow mosaic virus symptom severity in tolerant zucchini cultivars is related to a point mutation in P3 protein and is associated with a loss of relative fitness on susceptible plants. Phytopathology 93:1478–1484CrossRefPubMedGoogle Scholar
  9. 9.
    Duffy S, Shackelton LA, Holmes EC (2008) Rates of evolutionary change in viruses: patterns and determinants. Nat Rev Genet 9:267–276CrossRefPubMedGoogle Scholar
  10. 10.
    Feuer R, Boone JD, Netski D, Morzunov SP, St Jeor SC (1999) Temporal and spatial analysis of Sin Nombre virus quasispecies in naturally infected rodents. J Virol 73:9544–9554PubMedPubMedCentralGoogle Scholar
  11. 11.
    Gal-On A (2007) Zucchini yellow mosaic virus: insect transmission and pathogenicity—the tails of two proteins. Mol Plant Pathol 8:139–150CrossRefPubMedGoogle Scholar
  12. 12.
    Garcia-Arenal F, Fraile A, Malpica JM (2001) Variability and genetic structure of plant virus populations. Annu Rev Phytopathol 39:157–186CrossRefPubMedGoogle Scholar
  13. 13.
    Holmes EC (2009) RNA virus genomics: a world of possibilities. J Clin Investig 119:2488–2495CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Jenner CE, Tomimura K, Ohshima K, Hughes SL, Walsh JA (2002) Mutations in Turnip mosaic virus P3 and cylindrical inclusion proteins are separately required to overcome two Brassica napus resistance genes. Virology 300:50–59CrossRefPubMedGoogle Scholar
  15. 15.
    Jenner CE, Wang X, Tomimura K, Ohshima K, Ponz F, Walsh JA (2003) The dual role of the potyvirus P3 protein of Turnip mosaic virus as a symptom and avirulence determinant in brassicas. Mol Plant-Microbe Interact MPMI 16:777–784CrossRefPubMedGoogle Scholar
  16. 16.
    Jerzak GV, Brown I, Shi PY, Kramer LD, Ebel GD (2008) Genetic diversity and purifying selection in West Nile virus populations are maintained during host switching. Virology 374:256–260CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Johansen IE, Lund OS, Hjulsager CK, Laursen J (2001) Recessive resistance in Pisum sativum and potyvirus pathotype resolved in a gene-for-cistron correspondence between host and virus. J Virol 75:6609–6614CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Lech WJ, Wang G, Yang YL, Chee Y, Dorman K, McCrae D, Lazzeroni LC, Erickson JW, Sinsheimer JS, Kaplan AH (1996) In vivo sequence diversity of the protease of human immunodeficiency virus type 1: presence of protease inhibitor-resistant variants in untreated subjects. J Virol 70:2038–2043PubMedPubMedCentralGoogle Scholar
  19. 19.
    Ling KS, Harris KR, Meyer JD, Levi A, Guner N, Wehner TC, Bendahmane A, Havey MJ (2009) Non-synonymous single nucleotide polymorphisms in the watermelon eIF4E gene are closely associated with resistance to zucchini yellow mosaic virus. TAG Theor Appl Genet Theoretische und angewandte Genetik 120:191–200CrossRefPubMedGoogle Scholar
  20. 20.
    Maule AJ, Caranta C, Boulton MI (2007) Sources of natural resistance to plant viruses: status and prospects. Mol Plant Pathol 8:223–231CrossRefPubMedGoogle Scholar
  21. 21.
    Merits A, Guo D, Jarvekulg L, Saarma M (1999) Biochemical and genetic evidence for interactions between potato A potyvirus-encoded proteins P1 and P3 and proteins of the putative replication complex. Virology 263:15–22CrossRefPubMedGoogle Scholar
  22. 22.
    Murphy JF, Dane F (2009) Evaluation of ‘AU-Performance’ watermelon for its response to virus inoculation. Horttechnology 19:609–612Google Scholar
  23. 23.
    Novakova S, Svoboda J, Glasa M (2014) Analysis of the complete sequences of two biologically distinct Zucchini yellow mosaic virus isolates further evidences the involvement of a single amino acid in the virus pathogenicity. Acta Virol 58:364–367CrossRefPubMedGoogle Scholar
  24. 24.
    Sanjuan R, Domingo-Calap P (2016) Mechanisms of viral mutation. Cell Mol Life Sci CMLS 73:4433–4448CrossRefPubMedGoogle Scholar
  25. 25.
    Shukla DD, Frenkel MJ, Ward CW (1991) Structure and function of the potyvirus genome with special reference to the coat protein coding region. Can J Plant Pathol = Revue Canadienne de phytopathologie 1991:178–191CrossRefGoogle Scholar
  26. 26.
    Strauss JH, Strauss EG (1988) Evolution of RNA viruses. Annu Rev Microbiol 42:657–683CrossRefPubMedGoogle Scholar
  27. 27.
    Urcuqui-Inchima S, Haenni AL, Bernardi F (2001) Potyvirus proteins: a wealth of functions. Virus Res 74:157–175CrossRefPubMedGoogle Scholar
  28. 28.
    Vassilakos N, Simon V, Tzima A, Johansen E, Moury B (2016) Genetic determinism and evolutionary reconstruction of a host jump in a plant virus. Mol Biol Evol 33:541–553CrossRefPubMedGoogle Scholar
  29. 29.
    Vijayapalani P, Maeshima M, Nagasaki-Takekuchi N, Miller WA (2012) Interaction of the trans-frame potyvirus protein P3N-PIPO with host protein PCaP1 facilitates potyvirus movement. PLoS Pathog 8:e1002639CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Xu Y, Kang D, Shi Z, Shen H, Wehner T (2004) Inheritance of resistance to zucchini yellow mosaic virus and watermelon mosaic virus in watermelon. J Hered 95:498–502CrossRefPubMedGoogle Scholar

Copyright information

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

Authors and Affiliations

  1. 1.Zhengzhou Fruit Research InstituteChinese Academy of Agricultural SciencesZhengzhouChina

Personalised recommendations