Abstract
We demonstrated the infectivity and host adaptation of a viola isolate of Plantago asiatica mosaic virus (PlAMV-Vi) in an asymptomatic host, Nicotiana benthamiana, through long-term serial passages. Serial passaging of a green fluorescent protein–tagged full-length cDNA clone of PlAMV-Vi (PlAMV-ViGFP) in N. benthamiana plants resulted in the appearance of a new virus line inducing leaf-crinkle symptoms, the Leaf Crinkle (LC) line. Virus titers were higher for both in the LC and the 14th passage line(s) of PlAMV-ViGFP compared with the original line. The LC line was found to have seven unique nucleotide mutations that may have contributed to its higher virulence and multiplication rate in N. benthamiana.
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The datasets generated during this study are available from the corresponding author upon reasonable request.
References
Fraile A, García-Arenal F (2016) Environment and evolution modulate plant virus pathogenesis. Curr Opin Virol 17:50–56
Fuji S-i, Mochizuki T, Okuda M et al (2022) Plant viruses and viroids in Japan. J Gen Plant Pathol 88:105–127
Fujimoto Y, Keima T, Hashimoto M et al (2022) Short 5′ untranslated region enables optimal translation of plant virus tricistronic RNA via leaky scanning. J Virol 96:e02144–e02121
Furuya M, Tanai S, Hamim I et al (2023) Phylogenetic and population genetic analyses of plantago asiatica mosaic virus isolates reveal intraspecific diversification. J Gen Plant Pathol 89:224–237
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
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
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:e01906–01920
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
Malmstrom CM, Alexander HM (2016) Effects of crop viruses on wild plants. Curr Opin Virol 19:30–36
Min B-E, Feldman TS, Ali A et al (2012) Molecular characterization, ecology, and epidemiology of a novel Tymovirus in Asclepias viridis from Oklahoma. Phytopathology 102:166–176
Minato N, Komatsu K, Okano Y et al (2014) Efficient foreign gene expression in planta using a plantago asiatica mosaic virus-based vector achieved by the strong RNA-silencing suppressor activity of TGBp1. Arch Virol 159:885–896
Montes N, Vijayan V, Pagán I (2021) Host population structure for tolerance determines the evolution of plant–virus interactions. New Phytol 231:1570–1585
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
Roossinck MJ, García-Arenal F (2015) Ecosystem simplification, biodiversity loss and plant virus emergence. Curr Opin Virol 10:56–62
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
Stewart AD, Logsdon JM, Kelley SE (2005) An empirical study of the evolution of virulence under both horizontal and vertical transmission. Evolution 59:730–739
Wallis CM, Stone AL, Sherman DJ et al (2007) Adaptation of plum pox virus to a herbaceous host (Pisum sativum) following serial passages. J Gen Virol 88:2839–2845
Wren JD, Roossinck MJ, Nelson RS et al (2006) Plant virus biodiversity and ecology. PLoS Biol 4:e80
Acknowledgements
We are grateful to Mr. Kazuo Yamashita (Fukuchi Garlic R&S), Dr. Kaoru Hanada (Genetic Resources Center, the National Agriculture and Food Research Organization (NARO)), and Dr. Tamaki Uehara-Ichiki (Genetic Resources Center, NARO) for providing the virus isolates.
Funding
This research was undertaken as part of the MEXT Program on LEADER, using research equipment shared in the MEXT Project for promoting public use of advanced research infrastructure at Niigata Univ. (JPMXS0421100320). Funding support for this work was provided by the Uchida Energy Science Promotion Foundation (R4-1-035).
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All authors contributed to the study’s conception and design. Material preparation, data collection, and analysis were performed by Daisuke Nakamura, Nami Minato, Minako Furuya, Ken Komatsu, and Shin-ichi Fuji. The first draft of the manuscript was written by Daisuke Nakamura and Nami Minato, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Communicated by Ioannis E. Tzanetakis
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Nakamura, D., Minato, N., Furuya, M. et al. Long-term passages of Plantago asiatica mosaic virus alter virulence and multiplication in Nicotiana benthamiana plants. Arch Virol 169, 9 (2024). https://doi.org/10.1007/s00705-023-05934-z
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DOI: https://doi.org/10.1007/s00705-023-05934-z