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Molecular analysis of Greek isolates of cucumber mosaic virus from vegetables shows a low prevalence of satellite RNAs and suggests the presence of host-associated virus strains

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Abstract

Cucumber mosaic virus (CMV) is a generalist pathogen that infects many economically important crops in Greece. The present study was designed to evaluate the genetic variability of Greek CMV isolates in combination with their satellite RNAs (satRNAs). To achieve this goal, 77 CMV isolates were collected from symptomatic Greek vegetables, mainly tomatoes and cucurbits, alongside their neighboring crops, during a four-year period from 2015 to 2018. Phylogenetic analysis of a partial coat protein (CP) gene segment revealed that all of the isolates belong to CMV subgroups IA and IB and that they are closely related to previously reported Greek isolates. It should be noted, however, that the latter mainly included tomato isolates. Network analysis of the evolutionary relationships among the CP sequences of the Greek isolates in comparison to the corresponding sequences obtained from the GenBank database indicated two predominant common ancestors and at least three differentiated peripherals, and possibly host-associated (tomatoes, legumes, cucurbits) haplogroups (strain groups). More specifically, host-adaptive evolution can be postulated regarding the tomato isolates in subgroup IB. Necrogenic or non-necrogenic satRNAs were detected in four samples from tomato and melon, and this is the first report of non-necrogenic satRNAs in CMV in Greece.

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References

  1. Ali A, Li H, Schneider WL, Sherman DJ, Gray S, Smith D, Roossinck MJ (2006) Analysis of genetic bottlenecks during horizontal transmission of Cucumber mosaic virus. J Gen Virol 80(17):8345–8350

    Article  CAS  Google Scholar 

  2. Ali A, Roossinck MJ (2008) Genetic bottlenecks. In: Roossinck MJ (ed) Plant virus evolution. Springer, Berlin, pp 123–131

  3. Alonso-Prados JL, Aranda MA, Malpica JM, García-Arenal F, Fraile A (1998) Satellite RNA of cucumber mosaic cucumovirus spreads epidemically in natural populations of its helper virus. Phytopathology 88:520–524

    Article  CAS  PubMed  Google Scholar 

  4. Andika IB, Wei S, Cao C, Salaipeth L, Kondo H, Sun L (2017) Phytopathogenic fungus hosts a plant virus: A naturally occurring cross-kingdom viral infection. Proc Natl Acad Sci USA 114(46):12267–12272

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Aramburu J, Galipienso L, Lopez C (2007) Reappearance of Cucumber mosaic virus isolates belonging to subgroup IB in tomato plants in North- Eastern Spain. J Phytopathol 155(9):513–518

    Article  CAS  Google Scholar 

  6. Aranda MA, Fraile A, Dopazo J, Malpica JM, García-Arenal F (1997) Contribution of mutation and RNA recombination to the evolution of a plant pathogenic RNA. J Mol Evol 44:81–88

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Ben Tamarzizt H, Montarry J, Girardot G, Fakhfakh H, Tepfer M, Jacquemond M (2013) Cucumber mosaic virus populations in Tunisian pepper crops are mainly composed of virus reassortants with resistance-breaking properties. Plant Pathol 62(6):1415–1428

    Article  CAS  Google Scholar 

  8. Betancourt M, Escriu F, Fraile A, García-Arenal F (2013) Virulence evolution of a generalist plant virus in a heterogeneous host system. Evol Appl 6(6):875–890

    Article  PubMed  PubMed Central  Google Scholar 

  9. Betancourt M, Fereres A, Fraile A, García-Arenal F (2008) Estimation of the effective number of founders that initiate an infection after aphid transmission of a multipartite plant virus. J Virol 82(24):12416–12421

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Betancourt M, Fraile A, García-Arenal F (2011) Cucumber mosaic virus satellite RNAs that induce similar symptoms in melon plants show large differences in fitness. J Gen Virol 92(8):1930–1938

    Article  CAS  PubMed  Google Scholar 

  11. Betancourt M, Fraile A, Milgroom MG, García-Arenal F (2016) Aphid vector population density determines the emergence of necrogenic satellite RNAs in populations of Cucumber mosaic virus. J Gen Virol 97(6):1453–1457

    Article  CAS  PubMed  Google Scholar 

  12. Bonnet J, Fraile A, Sacristán S, Malpica JM, García-Arenal F (2005) Role of recombination in the evolution of natural populations of Cucumber mosaic virus, a tripartite RNA plant virus. Virology 332(1):359–368

    Article  CAS  PubMed  Google Scholar 

  13. Carmo-Sousa M, Moreno A, Garzo E, Fereres A (2014) A non-persistently transmitted-virus induces a pull-push strategy in its aphid vector to optimize transmission and spread. Virus Res 186:38–46

    Article  CAS  PubMed  Google Scholar 

  14. Chatzivassiliou EK, Giakountis A, Kumari SG, Makkouk KM (2016) Viruses affecting lentil (Lens culinaris Medik.) in Greece; incidence and genetic variability of Bean leafroll virus and Pea enation mosaic virus. Phytopath Mediterr 55(2):239–252

  15. Chatzivassiliou ΕK, Efthimiou K, Drossos E, Papadopoulou A, Poimenidis G, Katis NI (2004) Α survey of tobacco viruses in tobacco crops and native flora in Greece. E J Plant Pathol 110(10):1011–1023

    Article  Google Scholar 

  16. Davino S, Panno S, Rangel EA, Davino M, Bellardi MG, Rubio L (2012) Population genetics of Cucumber mosaic virus infecting medicinal, aromatic and ornamental plants from northern Italy. Arch Virol 157(4):739–745

    Article  CAS  PubMed  Google Scholar 

  17. Del Toro FJ, Aguilar E, Hernández-Walias FJ, Tenllado F, Chung BN, Canto T (2015) High temperature, high ambient CO2 affect the interactions between three positive-sense RNA viruses and a compatible host differentially, but not their silencing suppression efficiencies. PLoS One 10(8): e0136062 

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Eiras M, Boari AJ, Colariccio A, Chaves ALR, Briones MRS, Figueira AR, Harakava R (2004) Characterization of isolates of the cucumovirus Cucumber mosaic virus present in Brazil. J Plant Pathol 86(1):61–69

    CAS  Google Scholar 

  19. Escriu F, Fraile A, García-Arenal F (2000) Evolution of virulence in natural populations of the satellite RNA of Cucumber mosaic virus. Phytopathology 90(5):480–485

    Article  CAS  PubMed  Google Scholar 

  20. Escriu F, Fraile A, García-Arenal F (2003) The evolution of virulence in a plant virus. Evolution 57(4):755–765

    PubMed  Google Scholar 

  21. Fraile A, Alonso-Prados JL, Aranda MA, Bernal JJ, Malpica JM, García-Arenal F (1997) Genetic exchange by recombination or reassortment is infrequent in natural populations of a tripartite RNA plant virus. J Virol 71(2):934–940

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Fraile A, García-Arenal F (1991) Secondary structure as a constraint on the evolution of a plant viral satellite RNA. J Mol Biol 221(4):1065–1069

    Article  CAS  PubMed  Google Scholar 

  23. Gallitelli D (2000) The ecology of Cucumber mosaic virus and sustainable agriculture. Virus Res 71(1–2):9–21

    Article  CAS  PubMed  Google Scholar 

  24. García-Arenal F, Escriu F, Aranda MA, Alonso-Prados JL, Malpica JM, Fraile A (2000) Molecular epidemiology of Cucumber mosaic virus and its satellite RNA. Virus Res 71(1–2):1–8

    Article  PubMed  Google Scholar 

  25. García-Arenal F, Palukaitis P (1999) Structure and functional relationships of satellite RNAs of Cucumber mosaic virus. Curr Top Microbiol Immunol 239:37–63

    PubMed  Google Scholar 

  26. Giakountis A, Tsarmpopoulos I, Chatzivassiliou EK (2018) Cucumber mosaic virus isolates from Greek legumes are associated with satellite RNAs that are necrogenic for tomato. Plant Dis 102(11):2268–2276

    Article  PubMed  Google Scholar 

  27. Grieco F, Lanave C, Gallitelli D (1997) Evolutionary dynamics of Cucumber mosaic virus satellite RNA during natural epidemics in Italy. Virology 229(1):166–174

    Article  CAS  PubMed  Google Scholar 

  28. Hasiów-Jaroszewska B, Budzyńska D, Rymelska N, Korpys P, Borodynko-Filas N (2018) Phylogenetic evidence of natural reassortants in the Cucumber mosaic virus population in Poland. Can J Plant Pathol 40(4):587–593

    Article  CAS  Google Scholar 

  29. Heo K-J, Kwon S-J, Kim M-K, Kwak H-R, Han S-J, Kwon M-J, Rao ALN, Seo J-K (2020) Newly emerged resistance-breaking variants of cucumber mosaic virus represent ongoing host-interactive evolution of an RNA virus. Virus Evol. 2020;6(2):veaa070

  30. Hong JS, Masuta C, Nakano M, Abe J, Uyeda I (2003) Adaptation of Cucumber mosaic virus soybean strains (SSVs) to cultivated and wild soybeans. Theor Appl Genet 107(1):49–53

    Article  CAS  PubMed  Google Scholar 

  31. Hsu HT, Barzuna L, Hsu YH, Bliss W, Perry KL (2000) Identification and subgrouping of Cucumber mosaic virus with mouse monoclonal antibodies. Phytopathology 90(6):615–620

    Article  CAS  PubMed  Google Scholar 

  32. Jacquemond M (2012) Cucumber mosaic virus. Adv Virus Res 84:439–504

    Article  PubMed  Google Scholar 

  33. Kim MK, Seo JK, Kwak HR, Kim JS, Kim KH, Cha BJ, Choi HS (2014) Molecular genetic analysis of cucumber mosaic virus populations infecting pepper suggests unique patterns of evolution in Korea. Phytopathol 104(9):993–1000

    Article  CAS  Google Scholar 

  34. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874

  35. Kyriakopoulou PE, Perdikis DC, Sclavounos AP, Girgis SM, Lykouressis DP, Tsitsipis JA, Christaki PA (2000) Cucumber mosaic cucumovirus incidence in open-field tomato in the Olympia area and trap captures of alate aphids. Bull OEPP 30(2):305–315

    Article  Google Scholar 

  36. Lee J-A, Choi S-K, Yoon J-Y, Hong JS, Ryu G-H, Lee SY, Choi J-K (2007) Variation in the pathogenicity of lily isolates of Cucumber mosaic virus. Plant Path J 23(4):251–259

    Article  Google Scholar 

  37. Leigh JW, Bryant D (2015) POPART: full-feature software for haplotype network construction. Methods Ecol Evol 6(9):1110–1116

    Article  Google Scholar 

  38. Lin HX, Rubio L, Smythe AB, Falk BW (2004) Molecular population genetics of Cucumber mosaic virus in California: evidence for founder effects and reassortment. J Virol 78(12):6666–6675

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Lin HX, Rubio L, Smythe AB, Jiminez M, Falk BW (2003) Genetic diversity and biological variation among California isolates of Cucumber mosaic virus. J Gen Virol 84:249–258

    Article  CAS  PubMed  Google Scholar 

  40. Liu YY, Yu SL, Lan YF, Zhang CL, Hou SS, Li XD, Chen XZ, Zhu XP (2009) Molecular variability of five Cucumber mosaic virus isolates from China. Acta Virol 53(2):89–97

    Article  CAS  PubMed  Google Scholar 

  41. Malpica JM, Sacristán S, Fraile A, García-Arenal F (2006) Association and host selectivity in multi-host pathogens. PLoS One 1(1):e41

    Article  PubMed  PubMed Central  Google Scholar 

  42. Martin DP, Lemey P, Lott M, Moulton V, Posada D, Lefeuvre P (2010) RDP3: A flexible and fast computer program for analyzing recombination. Bioinformatics 26(19):2462–2463

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Mauck KE, De Moraes CM, Mescher MC (2010) Deceptive chemical signals induced by a plant virus attract insect vectors to inferior hosts. Proc Natl Acad Sci USA 107(8):3600–3605

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Mochizuki T, Ohki ST (2012) Cucumber mosaic virus: viral genes as virulence determinants. Mol Plant Pathol 13(3):217–225

    Article  CAS  PubMed  Google Scholar 

  45. Moriones E, Fraile A, García-Arenal F (1991) Host-associated selection of sequence variants from a satellite RNA of Cucumber mosaic virus. Virology 184(1):465–468

    Article  CAS  PubMed  Google Scholar 

  46. Murphy JF, Masiri J, Hadi BAR, Dute RR (2016) Recovery from Cucumber mosaic virus infection for ‘Calwonder’ bell pepper plants does not counter negative impacts on plant growth. J Phytopathol 164(10):840–846

    Article  Google Scholar 

  47. Nouri S, Arevalo R, Falk BW, Groves RL (2014) Genetic structure and molecular variability of Cucumber mosaic virus isolates in the United States. PLoS One 9(5):e96582

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  48. Ohshima K, Matsumoto K, Yasaka R, Nishiyama M, Soejima K, Korkmaz S, Ho SY, Gibbs AJ, Takeshita M (2016) Temporal analysis of reassortment and molecular evolution of Cucumber mosaic virus: Extra clues from its segmented genome. Virology 487:188–197

    Article  CAS  PubMed  Google Scholar 

  49. Palukaitis P (2019) Genome structure and expression. In: Palukaitis P, García-Arenal F (eds) Cucumber mosaic virus. APS Press, Minnesota, pp 113–121

  50. Palukaitis P, García-Arenal F (2003) Cucumoviruses. Adv Virus Res 62:241–323

    Article  CAS  PubMed  Google Scholar 

  51. Palukaitis P, Roossinck MJ, Dietzgen RG, Francki RI (1992) Cucumber mosaic virus. Adv Virus Res 41:281–348

    Article  CAS  PubMed  Google Scholar 

  52. Perry KL, Zhang L, Palukaitis P (1998) Amino acid changes in the coat protein of Cucumber mosaic virus differentially affect transmission by the aphids Myzus persicae and Aphis gossypii. Virology 242(1):204–210

    Article  CAS  PubMed  Google Scholar 

  53. Rhee SJ, Watt LG, Cazar Bravo A, Murphy AM, Carr JP (2020) Effects of the cucumber mosaic virus 2a protein on aphid-plant interactions in Arabidopsis thaliana. Mol Plant Pathol 21:1248–1254

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Roossinck MJ (1997) Mechanisms of plant virus evolution. Annu Rev Phytopathol 35:191–209

    Article  CAS  PubMed  Google Scholar 

  55. Roossinck MJ (2002) Evolutionary history of Cucumber mosaic virus deduced by phylogenetic analyses. J Virol 76(7):3382–3387

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Roossinck MJ, Palukaitis P (1991) Differential replication in zucchini squash of a Cucumber mosaic virus satellite RNA maps to RNA 1 of the helper virus. Virology 181(1):371–373

    Article  CAS  PubMed  Google Scholar 

  57. Roossinck MJ, Zhang L, Hellwald K-H (1999) Rearrangements in the 5-nontranslated region and phylogenetic analyses of Cucumber mosaic virus RNA 3 indicate radial evolution of three subgroups. J Virol 73(8):6752–6758

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Rybicki EP (2015) A top ten list for economically important plant viruses. Arch Virol 160(1):17–20

    Article  CAS  PubMed  Google Scholar 

  59. Scholthof KBG, Adkins S, Czosnek H, Palukaitis P, Jacquot E, Hohn T, Hohn B, Saunders K, Candresse T, Ahlquist P, Hemenway C, Foster GD (2011) Top 10 plant viruses in molecular plant pathology. Mol Plant Pathol 12(9):938–954

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Sclavounos AP, Voloudakis AE, Arabatzis Ch, Kyriakopoulou PE (2006) A severe Hellenic CMV tomato isolate: Symptom variability in tobacco, characterization and discrimination of variants. E J Plant Pathol 115:163–172

    Article  Google Scholar 

  61. Shintaku M (1991) Coat protein gene sequences of two Cucumber mosaic virus strains reveal a single amino acid change correlating with chlorosis induction. J Gen Virol 72:2587–2589

    Article  CAS  PubMed  Google Scholar 

  62. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–2729

  63. Tepfer M, Girardot G, Fénéant L, Tamarzizt HB, Verdin E, Moury B, Jacquemond M (2016) A genetically novel, narrow-host-range isolate of Cucumber mosaic virus (CMV) from rosemary. Arch Virol 161(7):2013–2017

    Article  CAS  PubMed  Google Scholar 

  64. Thompson JR, Langenhan JL, Fuchs M, Perrya KL (2015) Genotyping of Cucumber mosaic virus isolates in western New York State during epidemic years. Characterization of an emergent plant virus population. Virus Res 210:169–177

    Article  CAS  PubMed  Google Scholar 

  65. Varveri C, Boutsika K (1999) Characterization of cucumber mosaic cucumovirus isolates in Greece. Plant Pathol 48(1):95–100

    Article  Google Scholar 

  66. Vovlas C, Di Franco A (2004) Cucumber mosaic virus in Nicotiana glauca in Greece. J Plant Pathol 86:91–92

    Google Scholar 

  67. White JL, Tousignant ME, Geletka LM, Kaper JM (1995) The replication of a necrogenic Cucumber mosaic virus satellite is temperature-sensitive in tomato. Arch Virol 140(1):53–63

    Article  CAS  PubMed  Google Scholar 

  68. Woolhouse MEJ, Taylor LH, Haydon DT (2001) Population biology of multihost pathogens. Science 292:1109–1112

    Article  CAS  PubMed  Google Scholar 

  69. Xanthis CK, Maliogka VI, Katis NI (2015) First report of Cucumber mosaic virus in Anemone sp in Greece. J Plant Pathol 97(3):541

    Google Scholar 

  70. Xanthis CK, Maliogka VI, Lecoq H, Dezbiez C, Tsvetkov I, Katis NI (2015) First report of Cucumber mosaic virus infecting watermelon in Greece and Bulgaria. J Plant Pathol 97(2):399

    Google Scholar 

  71. Xu P, Roossinck MJ (2000) Cucumber mosaic virus D Satellite RNA-induced programmed cell death in tomato. Plant Cell 12(7):1079–1092

    CAS  PubMed  PubMed Central  Google Scholar 

  72. Yoon J-H, Palukaits P, Choi S-K (2019) Host range. In: Palukaitis P, García-Arenal F (eds) Cucumber mosaic virus. APS Press, Minnesota, pp 15–18

  73. Zhang L, Hanada K, Palukaitis P (1994) Mapping local and systemic symptom determinants of cucumber mosaic cucumovirus in tobacco. J Gen Virol 75:3185–3191

    Article  CAS  PubMed  Google Scholar 

  74. Zhao F, Li Y, Chen L, Zhu L, Ren H, Lin H, Xi D (2016) Temperature dependent defense of Nicotiana tabacum against Cucumber mosaic virus and recovery occurs with the formation of dark green islands. J Plant Biol 59:293–301

    Article  CAS  Google Scholar 

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Acknowledgements

The authors wish to thank Prof. Nikolaos Katis (Aristotle University of Thessaloniki, School of Agriculture, Laboratory of Plant Pathology, Thessaloniki, Greece) for providing some infected samples/isolates.

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  1. Christos A. Valachas and Ioannis A. Giantsis contributed equally to this manuscript.

Authors and Affiliations

  1. Department of Crop Science, Plant Pathology Laboratory, School of Agricultural Production, Infrastructure and Environment, Agricultural University of Athens, Iera Odos 75, 11855, Athens, Greece

    Christos A. Valachas, Kyriaki Sareli, Eleanna Zelezniakof, Zoi Pentheroudaki & Elisavet K. Chatzivassiliou

  2. Department of Animal Science, Faculty of Agricultural Sciences, University of Western Macedonia, 53100, Florina, Greece

    Ioannis A. Giantsis

  3. Leibniz-Institute DSMZ-German Collection of Microorganisms and Cell Cultures GmbH, 38124, Braunschweig, Germany

    Stephan Winter

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  1. Christos A. Valachas
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Valachas, C.A., Giantsis, I.A., Sareli, K. et al. Molecular analysis of Greek isolates of cucumber mosaic virus from vegetables shows a low prevalence of satellite RNAs and suggests the presence of host-associated virus strains. Arch Virol 166, 2199–2208 (2021). https://doi.org/10.1007/s00705-021-05115-w

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