Skip to main content

Advertisement

Log in

Phylogenetic and population genetic analyses of plantago asiatica mosaic virus isolates reveal intraspecific diversification

  • Viral and Viroid Diseases
  • Published:
Journal of General Plant Pathology Aims and scope Submit manuscript

Abstract

Plantago asiatica mosaic virus (PlAMV) infects ornamental lilies and causes severe necrotic symptoms. PlAMV has also been isolated from several perennial weeds, including Plantago asiatica. While multiple isolates from cultivated lilies have been identified and shown to share a high degree of sequence identity with one another, there have been few studies of PlAMV isolates from weeds. Furthermore, a comprehensive phylogenetic analysis of PIAMV isolates from both lilies and weeds has not been performed. Here, we performed phylogenetic and population genetic analyses of the full-length genome sequences of 36 PlAMV isolates, including 14 new isolates obtained in this study. These analyses suggested intraspecific diversification of PlAMV isolates into five clades, including a clade consisting of ornamental lily isolates (Lily clade) and four other clades consisting of isolates from weeds or medicinal plants. The specific clade membership identified by the phylogenetic analysis was mainly correlated with the geographical location of the members of each clade. All PlAMV isolates except those in the Lily clade had a high level of genetic diversity. The Lily clade had a higher level of genetic differentiation from the other clades. The neutrality test suggested that genetic drift contributed to shaping PlAMV isolates in the Lily clade. Infectivity tests with infectious clones of the representative PIAMV isolates to four plant species, including lilies and P. asiatica, showed that isolates in different phylogenetic clades had variation in infectivity to the subset of plant species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abe S, Neriya Y, Noguchi K et al (2019) First report of the complete genomic sequences from Indonesian isolates of bamboo mosaic virus and detection of genomic recombination events. J Gen Plant Pathol 85:158–161

    Article  CAS  Google Scholar 

  • Abrahamian P, Hammond J, Hammond RW (2020) Complete genome sequence of an American isolate of pepino mosaic virus. Microbiol Resour Announc 9:e01124-e1219

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anderson PK, Cunningham AA, Patel NG et al (2004) Emerging infectious diseases of plants: pathogen pollution, climate change and agrotechnology drivers. Trends Ecol Evol 19:535–544

    Article  PubMed  Google Scholar 

  • Darriba D, Posada D, Kozlov AM et al (2019) ModelTest-NG: a new and scalable tool for the selection of DNA and protein evolutionary models. Mol Biol Evol 37:291–294

    Article  PubMed Central  Google Scholar 

  • de Kock M, Kok BJ, van Aanholt JTM, et al (2013) Aanvullend onderzoek naar verspreidingsroutes en mogelijkheden voor beheersing vam PIAMV. https://edepot.wur.nl/302540 Cited 17 May 2023 (in Dutch)

  • Decroocq V, Sicard O, Alamillo JM et al (2006) Multiple resistance traits control Plum pox virus infection in Arabidopsis thaliana. Mol Plant Microbe Interact 19:541–549

    Article  CAS  PubMed  Google Scholar 

  • Draghici H-K, Pilot R, Thiel H, Varrelmann M (2009) Functional mapping of PVX RNA-dependent RNA-replicase using pentapeptide scanning mutagenesis-Identification of regions essential for replication and subgenomic RNA amplification. Virus Res 143:114–124

    Article  CAS  PubMed  Google Scholar 

  • Fuentes S, Gibbs AJ, Hajizadeh M et al (2021) The phylogeography of potato virus X shows the fingerprints of its human vector. Viruses 13:644

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fuji S-I, Mochizuki N, Fujinaga M et al (2007) Incidence of viruses in Alstroemeria plants cultivated in Japan and characterization of Broad bean wilt virus-2, Cucumber mosaic virus and Youcai mosaic virus. J Gen Plant Pathol 73:216–221

    Article  Google Scholar 

  • Fuji S-I, Mochizuki T, Okuda M et al (2022) Plant viruses and viroids in Japan. J Gen Plant Pathol 88:105–127

    Article  CAS  Google Scholar 

  • Gómez P, Sempere RN, Elena SF, Aranda MA (2009) Mixed infections of Pepino mosaic virus strains modulate the evolutionary dynamics of this emergent virus. J Virol 83:12378–12387

    Article  PubMed  PubMed Central  Google Scholar 

  • Gong J, Ju H-K, Kim I-H et al (2019) Sequence variations among 17 new radish isolates of turnip mosaic virus showing differential pathogenicity and infectivity in nicotiana benthamiana, brassica rapa, and raphanus sativus. Phytopathology 109:904–912

    Article  CAS  PubMed  Google Scholar 

  • Hammond J, Adams IP, Fowkes AR et al (2021) Sequence analysis of 43-year old samples of Plantago lanceolata show that Plantain virus X is synonymous with Actinidia virus X and is widely distributed. Plant Pathol 70:249–258

    Article  CAS  Google Scholar 

  • Hammond J, Reinsel MD (2018) Sequence variability between Plantago asiatica mosaic virus isolates. Acta Hortic 1–8

  • Hančinský R, Mihálik D, Mrkvová M, et al (2020) Plant Viruses Infecting Solanaceae Family Members in the Cultivated and Wild Environments: A Review. Plants 9.: https://doi.org/10.3390/plants9050667

  • Hasiów-Jaroszewska B, Kuzniar A, Peters SA et al (2010) Evidence for RNA recombination between distinct isolates of Pepino mosaic virus. Acta Biochim Pol 57:385–388

    Article  PubMed  Google Scholar 

  • Hasiów-Jaroszewska B, Czerwoniec A, Pospieszny H, Elena SF (2011) Tridimensional model structure and patterns of molecular evolution of Pepino mosaic virus TGBp3 protein. Virol J 8:318

    Article  PubMed  PubMed Central  Google Scholar 

  • Hincapie M, Sood S, Mollov D et al (2021) Eight species of poaceae are hosting different genetic and pathogenic strains of sugarcane mosaic virus in the everglades agricultural area. Phytopathology 111:1862–1869

    Article  CAS  PubMed  Google Scholar 

  • Honjo MN, Emura N, Kawagoe T et al (2020) Seasonality of interactions between a plant virus and its host during persistent infection in a natural environment. ISME J 14:506–518

    Article  CAS  PubMed  Google Scholar 

  • Hudson RR, Slatkin M, Maddison WP (1992) Estimation of levels of gene flow from DNA sequence data. Genetics 132:583–589

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    Article  CAS  PubMed  Google Scholar 

  • Hughes PL, Harper F, Zimmerman MT, Scott SW (2005) Nandina mosaic virus is an isolate of Plantago asiatica mosaic virus. Eur J Plant Pathol 113:309–313

    Article  CAS  Google Scholar 

  • Jones RAC, Naidu RA (2019) Global Dimensions of Plant Virus Diseases: Current Status and Future Perspectives. Annu Rev Virol 6:387–409

    Article  CAS  PubMed  Google Scholar 

  • Jridi C, Martin J-F, Marie-Jeanne V et al (2006) Distinct viral populations differentiate and evolve independently in a single perennial host plant. J Virol 80:2349–2357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Komatsu K, Hammond J (2022) Plantago asiatica mosaic virus: An emerging plant virus causing necrosis in lilies and a new model RNA virus for molecular research. Mol Plant Pathol 23:1401–1414

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Komatsu K, Yamaji Y, Ozeki J et al (2008) Nucleotide sequence analysis of seven Japanese isolates of Plantago asiatica mosaic virus (PlAMV): a unique potexvirus with significantly high genomic and biological variability within the species. Arch Virol 153:193–198

    Article  CAS  PubMed  Google Scholar 

  • Komatsu K, Hashimoto M, Maejima K et al (2011) A necrosis-inducing elicitor domain encoded by both symptomatic and asymptomatic Plantago asiatica mosaic virus isolates, whose expression is modulated by virus replication. Mol Plant Microbe Interact 24:408–420

    Article  CAS  PubMed  Google Scholar 

  • Komatsu K, Yamashita K, Sugawara K et al (2017) Complete genome sequences of two highly divergent Japanese isolates of Plantago asiatica mosaic virus. Arch Virol 162:581–584

    Article  CAS  PubMed  Google Scholar 

  • Komatsu K, Sasaki N, Yoshida T et al (2021) Identification of a proline-kinked amphipathic α-helix downstream from the methyltransferase domain of a potexvirus replicase and its role in virus replication and perinuclear complex formation. J Virol 95:e0190620

    Article  PubMed  Google Scholar 

  • Kozlov AM, Darriba D, Flouri T et al (2019) RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 35:4453–4455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kwak H-R, Kim M, Kim J et al (2018) First Report of Plantago asiatica mosaic virus in Rehmannia glutinosa in Korea. Plant Dis 102:1046–1046

    Article  Google Scholar 

  • Lefkowitz EJ, Dempsey DM, Hendrickson RC et al (2018) Virus taxonomy: the database of the International Committee on Taxonomy of Viruses (ICTV). Nucleic Acids Res 46:D708–D717

    Article  CAS  PubMed  Google Scholar 

  • Malmstrom CM, Bigelow P, Trębicki P et al (2017) Crop-associated virus reduces the rooting depth of non-crop perennial native grass more than non-crop-associated virus with known viral suppressor of RNA silencing (VSR). Virus Res 241:172–184

    Article  CAS  PubMed  Google Scholar 

  • Martin DP, Murrell B, Golden M, et al (2015) RDP4: Detection and analysis of recombination patterns in virus genomes. Virus Evol 1:vev003

  • Moreno-Pérez MG, Pagán I, Aragón-Caballero L et al (2014) Ecological and genetic determinants of Pepino Mosaic Virus emergence. J Virol 88:3359–3368

    Article  PubMed  PubMed Central  Google Scholar 

  • Muhire BM, Varsani A, Martin DP (2014) SDT: a virus classification tool based on pairwise sequence alignment and identity calculation. PLoS ONE 9:e108277

    Article  PubMed  PubMed Central  Google Scholar 

  • Murray GGR, Kosakovsky Pond SL, Obbard DJ (2013) Suppressors of RNAi from plant viruses are subject to episodic positive selection. Proc Biol Sci 280:20130965

    PubMed  PubMed Central  Google Scholar 

  • Murrell B, Wertheim JO, Moola S et al (2012) Detecting individual sites subject to episodic diversifying selection. PLoS Genet 8:e1002764

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Novianti F, Sasaki N, Arie T, Komatsu K (2021) Acibenzolar-S-methyl-mediated restriction of loading of plantago asiatica mosaic virus into vascular tissues of Nicotiana benthamiana. Virus Res 306:198585

    Article  CAS  PubMed  Google Scholar 

  • Ohshima K, Yamaguchi Y, Hirota R et al (2002) Molecular evolution of Turnip mosaic virus: evidence of host adaptation, genetic recombination and geographical spread. J Gen Virol 83:1511–1521

    Article  CAS  PubMed  Google Scholar 

  • Ozeki J, Takahashi S, Komatsu K et al (2006) A single amino acid in the RNA-dependent RNA polymerase of Plantago asiatica mosaic virus contributes to systemic necrosis. Arch Virol 151:2067–2075

    Article  CAS  PubMed  Google Scholar 

  • Ozeki J, Hashimoto M, Komatsu K et al (2009) The N-terminal region of the Plantago asiatica mosaic virus coat protein is required for cell-to-cell movement but is dispensable for virion assembly. Mol Plant Microbe Interact 22:677–685

    Article  CAS  PubMed  Google Scholar 

  • Pond SLK, Frost SDW, Muse SV (2005) HyPhy: hypothesis testing using phylogenies. Bioinformatics 21:676–679

    Article  CAS  PubMed  Google Scholar 

  • Revers F, Guiraud T, Houvenaghel M-C et al (2003) Multiple resistance phenotypes to Lettuce mosaic virus among Arabidopsis thaliana accessions. Mol Plant Microbe Interact 16:608–616

    Article  CAS  PubMed  Google Scholar 

  • Roossinck MJ, García-Arenal F (2015) Ecosystem simplification, biodiversity loss and plant virus emergence. Curr Opin Virol 10:56–62

    Article  PubMed  PubMed Central  Google Scholar 

  • Roossinck MJ, Martin DP, Roumagnac P (2015) Plant virus metagenomics: advances in virus discovery. Phytopathology 105:716–727

    Article  CAS  PubMed  Google Scholar 

  • Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC et al (2017) DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol 34:3299–3302

    Article  CAS  PubMed  Google Scholar 

  • Senshu H, Ozeki J, Komatsu K et al (2009) Variability in the level of RNA silencing suppression caused by triple gene block protein 1 (TGBp1) from various potexviruses during infection. J Gen Virol 90:1014–1024

    Article  CAS  PubMed  Google Scholar 

  • Solovyev AG, Novikov VK, Merits A et al (1994) Genome characterization and taxonomy of Plantago asiatica mosaic potexvirus. J Gen Virol 75:259–267

    Article  CAS  PubMed  Google Scholar 

  • Spielman SJ, Weaver S, Shank SD et al (2019) Evolution of viral genomes: interplay between selection, recombination, and other forces. Methods Mol Biol 1910:427–468

    Article  CAS  PubMed  Google Scholar 

  • Stobbe AH, Roossinck MJ (2014) Plant virus metagenomics: what we know and why we need to know more. Front Plant Sci 5:150

    Article  PubMed  PubMed Central  Google Scholar 

  • Tanaka M, Verbeek M, Takehara M et al (2019) Differences in infectivity and pathogenicity of two Plantago asiatica mosaic virus isolates in lilies. Eur J Plant Pathol 153:813–823

    Article  Google Scholar 

  • Torres C, Fernández MDB, Flichman DM et al (2013) Influence of overlapping genes on the evolution of human hepatitis B virus. Virology 441:40–48

    Article  CAS  PubMed  Google Scholar 

  • Tsuda S, Sano T (2014) Threats to Japanese agriculture from newly emerged plant viruses and viroids. J Gen Plant Pathol 80:2–14

    Article  Google Scholar 

  • Uehara-Ichiki T, Nakazono-Nagaoka E, Yamaguchi M et al (2018) Next-generation sequencing and bioassay of viruses in Rehmannia glutinosa. Jpn J Phytopathol 84:151–157

    Article  Google Scholar 

Download references

Acknowledgements

We are grateful to Dr. Tsutomu Arie for discussion and support, Mr. Hideaki Otsuka for inoculation experiments, and Mr. Takashi Moriyama and Mr. Tsutomu Moriyama for their kind support. We thank Dr. Nobumitsu Sasaki and Dr. Richard Nelson for critical reading of the manuscript. We are also grateful to the Institute of Global Innovation Research at Tokyo University of Agriculture and Technology (GIR-TUAT), Japan for the Special Research Fund. This work was supported in part by Grants-in-Aid for Scientific Research 19K06048 for KK and by Grants-in-aid for JSPS fellow (20F20392) for IH, from the Japan Society for the Promotion of Science.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ken Komatsu.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Ethics approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 371 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Furuya, M., Tanai, S., Hamim, I. et al. Phylogenetic and population genetic analyses of plantago asiatica mosaic virus isolates reveal intraspecific diversification. J Gen Plant Pathol 89, 224–237 (2023). https://doi.org/10.1007/s10327-023-01129-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10327-023-01129-1

Keywords

Navigation