Diversity and Pathobiology of an Ilarvirus Unexpectedly Detected in Diverse Plants and Global Sequencing Data.

Ilarvirus; Serratus; Solanaceae; histopathology; phylogenetics; pollen; symptomatology; virion morphology; virus diversity; virus transmission; Phylogeny; Plant Diseases; Nicotiana; Solanum; Tobacco; Agronomy and Crop Science; Plant Science

Abstract :

[en] High-throughput sequencing (HTS) and sequence mining tools revolutionized virus detection and discovery in recent years, and implementing them with classical plant virology techniques results in a powerful approach to characterize viruses. An example of a virus discovered through HTS is Solanum nigrum ilarvirus 1 (SnIV1) (Bromoviridae), which was recently reported in various solanaceous plants from France, Slovenia, Greece, and South Africa. It was likewise detected in grapevines (Vitaceae) and several Fabaceae and Rosaceae plant species. Such a diverse set of source organisms is atypical for ilarviruses, thus warranting further investigation. In this study, modern and classical virological tools were combined to accelerate the characterization of SnIV1. Through HTS-based virome surveys, mining of sequence read archive datasets, and a literature search, SnIV1 was further identified from diverse plant and non-plant sources globally. SnIV1 isolates showed relatively low variability compared with other phylogenetically related ilarviruses. Phylogenetic analyses showed a distinct basal clade of isolates from Europe, whereas the rest formed clades of mixed geographic origin. Furthermore, systemic infection of SnIV1 in Solanum villosum and its mechanical and graft transmissibility to solanaceous species were demonstrated. Near-identical SnIV1 genomes from the inoculum (S. villosum) and inoculated Nicotiana benthamiana were sequenced, thus partially fulfilling Koch's postulates. SnIV1 was shown to be seed-transmitted and potentially pollen-borne, has spherical virions, and possibly induces histopathological changes in infected N. benthamiana leaf tissues. Overall, this study provides information to better understand the diversity, global presence, and pathobiology of SnIV1; however, its possible emergence as a destructive pathogen remains uncertain. [Formula: see text] Copyright © 2023 The Author(s). This is an open access article distributed under the CC BY 4.0 International license.

Disciplines :

Biochemistry, biophysics & molecular biology

Author, co-author :

Rivarez, Mark Paul Selda ; Department of Biotechnology and Systems Biology, National Institute of Biology, Ljubljana, 1000, Slovenia

Faure, Chantal; University of Bordeaux, INRAE, UMR 1332 Biologie du Fruit et Pathologie, Villenave d'Ornon, 33882, France

Svanella-Dumas, Laurence; University of Bordeaux, INRAE, UMR 1332 Biologie du Fruit et Pathologie, Villenave d'Ornon, 33882, France

Pecman, Anja; Department of Biotechnology and Systems Biology, National Institute of Biology, Ljubljana, 1000, Slovenia

Tušek-Žnidaric, Magda; Department of Biotechnology and Systems Biology, National Institute of Biology, Ljubljana, 1000, Slovenia

Schönegger, Deborah; University of Bordeaux, INRAE, UMR 1332 Biologie du Fruit et Pathologie, Villenave d'Ornon, 33882, France

De Jonghe, Kris; Plant Sciences Unit, Flanders Research Institute for Agriculture, Fisheries and Food, Merelbeke, 9820, Belgium

Blouin, Arnaud ; Plant Pathology Laboratory, TERRA-Gembloux Agro-Bio Tech, University of Liège, Gembloux, 5030, Belgium

Rasmussen, David A; Department of Entomology and Plant Pathology, North Carolina State University, Raleigh, 27606, U.S.A

Massart, Sébastien ; Université de Liège - ULiège > TERRA Research Centre > Gestion durable des bio-agresseurs

More authors (4 more)

Language :

English

Title :

Diversity and Pathobiology of an Ilarvirus Unexpectedly Detected in Diverse Plants and Global Sequencing Data.

Publication date :

September 2023

Journal title :

Phytopathology

ISSN :

0031-949X

eISSN :

1943-7684

Publisher :

American Phytopathological Society, United States

Volume :

113

Issue :

Pages :

1729 - 1744

Peer reviewed :

Peer Reviewed verified by ORBi

Additional URL :

https://apsjournals.apsnet.org/doi/pdf/10.1094/PHYTO-12-22-0465-V

Funders :

EU - European Union
FPS Health Federal Public Service Health, Food Chain Safety and Environment

Funding text :

Funding: Support for this work was mainly provided by the Horizon 2020 Marie Skłodowska-Curie Actions Innovative Training Network (H2020 MSCA-ITN) project “Innovative Network for Next Generation Training and Sequencing of Virome (INEXTVIR)” (grant GA 813542) under the management of the European Commission-Research Executive Agency and the Administration of the Republic of Slovenia for Food Safety, Veterinary Sector and Plant Protection and Slovenian Research Agency (grants P4-0165, P4-0407, and J4-4553). Support in Belgium was provided by the Belgian FPS Health Food Chain Safety and Environment (Project RT18/3 SEVIPLANT). M. P. S. Rivarez received funding from the Department of Science and Technology–Philippine Council for Agriculture, Aquatic, and Natural Resources Research and Development (DOST–PCAARRD) of the Republic of the Philippines (Balik Scientist Program [Republic Act 11035]).Funding: Support for this work was mainly provided by the Horizon 2020 Marie Skłodowska-Curie Actions Innovative Training Network (H2020 MSCAITN) project “Innovative Network for Next Generation Training and Sequencing of Virome (INEXTVIR)” (grant GA 813542) under the management of the European Commission-Research Executive Agency and the Administration of the Republic of Slovenia for Food Safety, Veterinary Sector and Plant Protection and Slovenian Research Agency (grants P4-0165, P4-0407, and J4-4553). Support in Belgium was provided by the Belgian FPS Health Food Chain Safety and Environment (Project RT18/3 SEVIPLANT). M. P. S. Rivarez received funding from the Department of Science and Technology–Philippine Council for Agriculture, Aquatic, and Natural Resources Research and Development (DOST–PCAARRD) of the Republic of the Philippines (Balik Scientist Program [Republic Act 11035]).

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Bibliography

Adams, M. J., and Antoniw, J. F. 2006. DPVweb: A comprehensive database of plant and fungal virus genes and genomes. Nucleic Acids Res. 34: D382-D385.
Adkins, S., Baker, C. A., Badillo-Vargas, I. E., Frantz, G., Mellinger, H. C., Roe, N., and Funderburk, J. E. 2015. Necrotic streak disease of tomato in Florida caused by a new ilarvirus species related to Tulare apple mosaic virus. New Dis. Rep. 31:16.
Aparicio, F., Aramburu, J., Herranz, M. C., Pallás, V., and López, C. 2018. Parietaria mottle virus: A potential threat for tomato crops? Acta Hortic. 1207:261-268.
Aparicio, F., Sánchez-Pina, M. A., Sánchez-Navarro, J. A., and Pallás, V. 1999. Location of prunus necrotic ringspot ilarvirus within pollen grains of infected nectarine trees: Evidence from RT-PCR, dot-blot and in situ hybridisation. Eur. J. Plant Pathol. 105:623-627.
Aramburu, J., Galipienso, L., Aparicio, F., Soler, S., and López, C. 2010. Mode of transmission of parietaria mottle virus. J. Plant Pathol. 92:679-684.
Arnoux, S. 2019. Comparative analyses of the molecular footprint of domestication in three Solanaceae species: Eggplant, pepper and tomato. Ph.D. Thesis. https://tel.archives-ouvertes.fr/tel-02185095v2/document
Auber, R. P., Suttiyut, T., McCoy, R. M., Ghaste, M., Crook, J. W., Pendleton, A. L., Widhalm, J. R., and Wisecaver, J. H. 2020. Hybrid de novo genome assemblyofredgromwell(Lithospermumerythrorhizon)revealsevolutionary insight into shikonin biosynthesis. Hortic. Res. 7:82.
Badillo-Vargas, I. E., Baker, C. A., Turechek, W. W., Frantz, G., Mellinger, H. C., Funderburk, J. E., and Adkins, S. 2016. Genomic and biological characterization of tomato necrotic streak virus, a novel subgroup 2 ilarvirus infecting tomato in Florida. Plant Dis. 100:1046-1053.
Bester, R., and Maree, H. J. 2023. First report of the plum marbling disease associated agent, plum viroid I, in apricots (Prunus armeniaca) in South Africa. Plant Dis. 107:1956.
Bouckaert, R., Vaughan, T. G., Barido-Sottani, J., Duchêne, S., Fourment, M., Gavryushkina, A., Heled, J., Jones, G., Kühnert, D., De Maio, N., Matschiner, M., Mendes, F. K., Müller, N. F., Ogilvie, H. A., du Plessis, L., Popinga, A., Rambaut, A., Rasmussen, D., Siveroni, I., Suchard, M. A., Wu, C.-H., Xie, D., Zhang, C., Stadler, T., and Drummond, A. J. 2019. BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. PLoS Comput. Biol. 15:e1006650.
Bratsch, S. A., Creswell, T. C., and Ruhl, G. E. 2018. First report of tomato necroticspotvirusinfectingtomatoinIndiana.PlantHealthProg.19:224-225.
Bratsch, S. A., Grinstead, S., Creswell, T. C., Ruhl, G. E., and Mollov, D. 2019. Characterization of tomato necrotic spot virus, a subgroup 1 ilarvirus causing necrotic foliar, stem, and fruit symptoms in tomatoes in the United States. Plant Dis. 103:1391-1396.
Bristow, P. R., and Martin, R. R. 1999. Transmission and the role of honeybees in field spread of blueberry shock ilarvirus, a pollen-borne virus of highbush blueberry. Phytopathology 89:124-130.
Buzkan, N., Chiumenti, M., Massart, S., Sarpkaya, K., Karada g, S., and Minafra, A. 2019. A new emaravirus discovered in Pistacia from Turkey. Virus Res. 263:159-163.
Card, S. D., Pearson, M. N., and Clover, G. R. G. 2007. Plant pathogens transmitted by pollen. Australas. Plant Pathol. 36:455-461.
Carroll, D., Daszak, P., Wolfe, N. D., Gao, G. F., Morel, C. M., Morzaria, S., Pablos-Méndez, A., Tomori, O., and Mazet, J. A. K. 2018. The Global Virome Project. Science 359:872-874.
Chang, S., Puryear, J., and Cairney, J. 1993. A simple and efficient method for isolating RNA from pine trees. Plant Mol. Biol. Rep. 11:113-116.
Chen, X., Yang, Q., Li, H., Li, H., Hong, Y., Pan, L., Chen, N., Zhu, F., Chi, X., Zhu, W., Chen, M., Liu, H., Yang, Z., Zhang, E., Wang, T., Zhong, N., Wang, M., Liu, H., Wen, S., Li, X., Zhou, G., Li, S., Wu, H., Varshney, R., Liang, X., and Yu, S. 2016. Transcriptome-wide sequencing provides insights into geocarpy in peanut (Arachis hypogaea L.). Plant Biotechnol. J. 14:1215-1224.
Chiapello, M., Rodriguez-Romero, J., Ayllon, M., and Turina, M. 2019. A report on the virome of obligatory biotrophs. https://ec.europa.eu/research/participants/documents/downloadPublic?documentIds= 080166e5c8e77dab&appId=PPGMS (accessed February 7, 2022).
Chiapello, M., Rodríguez-Romero, J., Nerva, L., Forgia, M., Chitarra, W., Ayllón, M. A., and Turina, M. 2020. Putative new plant viruses associated with Plasmopara viticola-infected grapevine samples. Ann. Appl. Biol. 176:180-191.
Coady, K. K., Burgoon, L., Doskey, C., and Davis, J. W. 2020. Assessment of transcriptomic and apical responses of Daphnia magna exposed to a polyethylene microplastic in a 21-d chronic study. Environ. Toxicol. Chem. 39:1578-1589.
Costa, C. P., Duennes, M. A., Fisher, K., Der, J. P., Watrous, K. M., Okamoto, N., Yamanaka, N., and Woodard, S. H. 2020. Transcriptome analysis reveals nutrition- and age-related patterns of gene expression in the fat body of preoverwintering bumble bee queens. Mol. Ecol. 29:720-737.
Deboutte, W., Beller, L., Yinda, C. K., Maes, P., de Graaf, D. C., and Matthijnssens, J. 2020. Honey-bee–associated prokaryotic viral communities reveal wide viral diversity and a profound metabolic coding potential. Proc. Natl. Acad. Sci. 117:10511-10519.
de Klerk, A., Swanepoel, P., Lourens, R., Zondo, M., Abodunran, I., Lytras, S., MacLean, O. A., Robertson, D., Kosakovsky Pond, S. L., Zehr, J. D., Kumar, V., Stanhope, M. J., Harkins, G., Murrell, B., and Martin, D. P. 2022. Conserved recombination patterns across coronavirus subgenera. Virus Evol. 8:1-15.
Dias, N. P., Hu, R., Hensley, D. D., Hansen, Z. R., Domier, L. L., and Hajimorad, M. R. 2022. A survey for viruses and viroids of peach in Tennessee orchards by RNA sequencing. Plant Health Prog. 23:265-268.
Digiaro, M., and Savino, V. 1992. Role of pollen and seeds in the spread of ilarviruses in almond. Adv. Hortic. Sci. 6:134-136.
Edgar, R. C. 2004. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797.
Edgar, R. C., Taylor, J., Lin, V., Altman, T., Barbera, P., Meleshko, D., Lohr, D., Novakovsky, G., Buchfink, B., Al-Shayeb, B., Banfield, J. F., de la Peña, M., Korobeynikov, A., Chikhi, R., and Babaian, A. 2022. Petabase-scale sequence alignment catalyses viral discovery. Nature 602:142-147.
Fetters, A. M., Cantalupo, P. G., Wei, N., Robles, M. T. S., Stanley, A., Stephens, J. D., Pipas, J. M., and Ashman, T.-L. 2022. The pollen virome of wild plants and its association with variation in floral traits and land use. Nat. Commun. 13:523.
Foissac, X., Svanella-Dumas, L., Gentit, P., Dulucq, M.-J., Marais, A., and Candresse, T. 2005. Polyvalent degenerate oligonucleotides reverse transcription-polymerase chain reaction: A polyvalent detection and characterization tool for trichoviruses, capilloviruses, and foveaviruses. Phytopathology 95:617-625.
Fontdevila, N., Khalili, M., Maachi, A., Rivarez, M. P. S., Rollin, R., Salavert, F., Temple, C., Aranda, M. A., Boonham, N., Botermans, M., Candresse, T., Fox, A., Hernando, Y., Kutnjak, D., Marais, A., Petter, F., Ravnikar, M., Selmi, I., Tahzima, R., Trontin, C., Wetzel, T., and Massart, S. 2023. Managing the deluge of newly discovered plant viruses and viroids: An optimized scientific and regulatory framework for their characterization and risk analysis. Front. Microbiol. 14.
Fox, A. 2020. Reconsidering causal association in plant virology. Plant Pathol. 69:956-961.
Gaafar, Y. Z. A., Herz, K., Hartrick, J., Fletcher, J., Blouin, A. G., MacDiarmid, R., and Ziebell, H. 2020. Investigating the pea virome in Germany—Old friends and new players in the field(s). Front. Microbiol. 11:2605.
George, J. A., and Davidson, T. R. 1963. Pollen transmission of necrotic ring spot and sour cherry yellows viruses from tree to tree. Can. J. Plant Sci. 43:276-288.
Gilmer, R., and Way, R. 1960. Pollen transmission of necrotic ringspot and prune dwarf viruses in sour cherry. Phytopathology 50:624-625.
Greber, R. S., Klose, M. J., Milne, J. R., and Teakle, D. S. 1991. Transmission of prunus necrotic ringspot virus using plum pollen and thrips. Ann. Appl. Biol. 118:589-593.
Gregory, A. C., Zayed, A. A., Conceição-Neto, N., Temperton, B., Bolduc, B., Alberti, A., Ardyna, M., Arkhipova, K., Carmichael, M., Cruaud, C., Dimier, C., Domínguez-Huerta, G., Ferland, J., Kandels, S., Liu, Y., Marec, C., Pesant, S., Picheral, M., Pisarev, S., Poulain, J., Tremblay, J.-É., Vik, D., Babin, M., Bowler, C., Culley, A. I., de Vargas, C., Dutilh, B. E., Iudicone, D., Karp-Boss, L., Roux, S., Sunagawa, S., Wincker, P., Sullivan, M. B., Acinas, S. G., Babin, M., Bork, P., Boss, E., Bowler, C., Cochrane, G., de Vargas, C., Follows, M., Gorsky, G., Grimsley, N., Guidi, L., Hingamp, P., Iudicone, D., Jaillon, O., Kandels-Lewis, S., Karp-Boss, L., Karsenti, E., Not, F., Ogata, H., Pesant, S., Poulton, N., Raes, J., Sardet, C., Speich, S., Stemmann, L., Sullivan, M. B., Sunagawa, S., and Wincker, P. 2019. Marine DNA viral macro- and microdiversity from pole to pole. Cell 177:1109-1123.e14.
Hamilton, R. I. 1977. Surface contamination of pollen by plant viruses. Phytopathology 77:395.
Hammond, J., Adams, I. P., Fowkes, A. R., McGreig, S., Botermans, M., Oorspronk, J. J. A., Westenberg, M., Verbeek, M., Dullemans, A. M., Stijger, C. C. M. M., Blouin, A. G., Massart, S., De Jonghe, K., Heyneman, M., Walsh, J. A., and Fox, A. 2020. 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.
Haselmair-Gosch, C., Miosic, S., Nitarska, D., Roth, B. L., Walliser, B., Paltram, R., Lucaciu, R. C., Eidenberger, L., Rattei, T., Olbricht, K., Stich, K., and Halbwirth, H. 2018. Great cause—Small effect: Undeclared genetically engineered orange petunias harbor an inefficient dihydroflavonol 4-reductase. Front. Plant Sci. 9:149.
Hou, W., Li, S., and Massart, S. 2020. Is there a “biological desert” with the discovery of new plant viruses? A retrospective analysis for new fruit tree viruses. Front. Microbiol. 11:592816.
Hou, X., He, Y., Fang, P., Mei, S.-Q., Xu, Z., Wu, W.-C., Tian, J.-H., Zhang, S., Zeng, Z.-Y., Gou, Q.-Y., Xin, G.-Y., Le, S.-J., Xia, Y.-Y., Zhou, Y.-L., Hui, F.-M., Pan, Y.-F., Eden, J.-S., Yang, Z.-H., Han, C., Shu, Y.-L., Guo, D., Li, J., Holmes, E. C., Li, Z.-R., and Shi, M. 2023. Artificial intelligence redefines RNA virus discovery. bioRxiv 537342.
Howe, A., Stopnisek, N., Dooley, S. K., Yang, F., Grady, K. L., and Shade, A. 2023. Seasonal activities of the phyllosphere microbiome of perennial crops. Nat. Commun. 14:1039.
ICTV. 2023. Current ICTV Taxonomy Release. https://ictv.global/taxonomy (accessed April 10, 2023).
Jaspers, M. V., Falloon, P. G., and Pearson, M. N. 2015. Seed and pollen transmission of asparagus virus 2. Eur. J. Plant Pathol. 142:173-183.
Kawamura, R., Shimura, H., Mochizuki, T., Ohki, S. T., and Masuta, C. 2014. Pollen transmission of asparagus virus 2 (AV-2) may facilitate mixed infection by two AV-2 isolates in asparagus plants. Phytopathology 104:1001-1006.
Khalili, M., Candresse, T., Koloniuk, I., Safarova, D., Brans, Y., Faure, C., Delmas, M., Massart, S., Aranda, M. A., Caglayan, K., Decroocq, V., Drogoudi, P., Glasa, M., Pantelidis, G., Navratil, M., Latour, F., Spak, J., Pribylova, J., Mihalik, D., Palmisano, F., Saponari, A., Necas, T., Sedlak, J., and Marais, A. 2023. The expanding menagerie of Prunus-infecting luteoviruses. Phytopathology 113:345-354.
Kibbe, W. A. 2007. OligoCalc: An online oligonucleotide properties calculator. Nucleic Acids Res. 35:W43-W46.
Kumar, S., Kumar, G. S., Maitra, S. S., Malý, P., Bharadwaj, S., Sharma, P., and Dwivedi, V. D. 2022. Viral informatics: Bioinformatics-based solution for managing viral infections. Brief. Bioinform. 23:1-36.
Kumar, S., Stecher, G., Li, M., Knyaz, C., and Tamura, K. 2018. MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Mol. Biol. Evol. 35:1547-1549.
Kutnjak, D., Tamisier, L., Adams, I., Boonham, N., Candresse, T., Chiumenti, M., De Jonghe, K., Kreuze, J. F., Lefebvre, M., Silva, G., Malapi-Wight, M., Margaria, P., Mavrič Pleško, I., McGreig, S., Miozzi, L., Remenant, B., Reynard, J.-S., Rollin, J., Rott, M., Schumpp, O., Massart, S., and Haegeman, A. 2021. A primer on the analysis of high-throughput sequencing data for detection of plant viruses. Microorganisms 9:841.
Lauber, C., and Seitz, S. 2022. Opportunities and challenges of data-driven virus discovery. Biomolecules 12:1073.
Lebas, B., Adams, I., Al Rwahnih, M., Baeyen, S., Bilodeau, G. J., Blouin, A. G., Boonham, N., Candresse, T., Chandelier, A., De Jonghe, K., Fox, A., Gaafar, Y. Z. A., Gentit, P., Haegeman, A., Ho, W., Hurtado-Gonzales, O., Jonkers, W., Kreuze, J., Kutjnak, D., Landa, B., Liu, M., Maclot, F., Malapi-Wight, M., Maree, H. J., Martoni, F., Mehle, N., Minafra, A., Mollov, D., Moreira, A., Nakhla, M., Petter, F., Piper, A. M., Ponchart, J., Rae, R., Remenant, B., Rivera, Y., Rodoni, B., Roenhorst, J. W., Rollin, J., Saldarelli, P., Santala, J., Souza-Richards, R., Spadaro, D., Studholme, D. J., Sultmanis, S., van der Vlugt, R., Tamisier, L., Trontin, C., Vazquez-Iglesias, I., Vicente, C. S. L., Vossenberg, B. T. L. H., Wetzel, T., Ziebell, H., and Massart, S. 2022. Facilitating the adoption of high-throughput sequencing technologies as a plant pest diagnostic test in laboratories: A step-by-step description. EPPO Bull. 52:394-418.
Ledón-Rettig, C. C., Zattara, E. E., and Moczek, A. P. 2017. Asymmetric interactions between doublesex and tissue- and sex-specific target genes mediate sexual dimorphism in beetles. Nat. Commun. 8:14593.
Lee, B. D., Neri, U., Roux, S., Wolf, Y. I., Camargo, A. P., Krupovic, M., Simmonds, P., Kyrpides, N., Gophna, U., Dolja, V. V., and Koonin, E. V. 2023. Mining metatranscriptomes reveals a vast world of viroid-like circular RNAs. Cell 186:646-661.e4.
Letunic, I., and Bork, P. 2021. Interactive Tree Of Life (iTOL) v5: An online tool for phylogenetic tree display and annotation. Nucleic Acids Res. 49: W293-W296.
Ma, Y., Marais, A., Lefebvre, M., Faure, C., and Candresse, T. 2020. Metagenomic analysis of virome cross-talk between cultivated Solanum lycopersicum and wild Solanum nigrum. Virology 540:38-44.
Ma, Y., Marais, A., Lefebvre, M., Theil, S., Svanella-Dumas, L., Faure, C., and Candresse, T. 2019. Phytovirome analysis of wild plant populations: Comparison of double-stranded RNA and virion-associated nucleic acid metagenomic approaches. J. Virol. 94:e01462-19.
Maclot, F., Candresse, T., Filloux, D., Malmstrom, C. M., Roumagnac, P., van der Vlugt, R., and Massart, S. 2020. Illuminating an ecological blackbox: Using high throughput sequencing to characterize the plant virome across scales. Front. Microbiol. 11:578064.
Mahlanza, T., Pierneef, R. E., Makwarela, L., Roberts, R., and van der Merwe, M. 2022. Metagenomic analysis for detection and discovery of plant viruses in wild Solanum spp. in South Africa. Plant Pathol. 71: 1633-1644.
Marais, A., Faure, C., Couture, C., Bergey, B., Gentit, P., and Candresse, T. 2014. Characterization by deep sequencing of divergent plum bark necrosis stem pitting-associated virus (PBNSPaV) isolates and development of a broad-spectrum PBNSPaV detection assay. Phytopathology 104: 660-666.
Martin, D. P., Varsani, A., Roumagnac, P., Botha, G., Maslamoney, S., Schwab, T., Kelz, Z., Kumar, V., and Murrell, B. 2021. RDP5: A computer program for analyzing recombination in, and removing signals of recombination from, nucleotide sequence datasets. Virus Evol. 7:veaa087.
Massart, S., Candresse, T., Gil, J., Lacomme, C., Predajna, L., Ravnikar, M., Reynard, J.-S., Rumbou, A., Saldarelli, P., Škorić, D., Vainio, E. J., Valkonen, J. P. T., Vanderschuren, H., Varveri, C., and Wetzel, T. 2017. A framework for the evaluation of biosecurity, commercial, regulatory, and scientific impacts of plant viruses and viroids identified by NGS technologies. Front Microbiol. 8:45.
McLeish, M. J., Fraile, A., and García-Arenal, F. 2021. Population genomics of plant viruses: The ecology and evolution of virus emergence. Phytopathology 111:32-39.
Meurens, F., Dunoyer, C., Fourichon, C., Gerdts, V., Haddad, N., Kortekaas, J., Lewandowska, M., Monchatre-Leroy, E., Summerfield, A., Wichgers Schreur, P. J., van der Poel, W. H. M., and Zhu, J. 2021. Animal board invited review: Risks of zoonotic disease emergence at the interface of wildlife and livestock systems. Animal 15:100241.
Mifsud, J. C. O., Gallagher, R. V., Holmes, E. C., and Geoghegan, J. L. 2022. Transcriptome mining expands knowledge of RNA viruses across the plant kingdom. J. Virol. 96:e00260-22.
Mink, G. I. 1993. Pollen and seed-transmitted viruses and viroids. Annu. Rev. Phytopathol. 31:375-402.
Morens, D. M., Daszak, P., Markel, H., and Taubenberger, J. K. 2020. Pandemic COVID-19 joins history’s pandemic legion. mBio 11:e00812-20.
Muhire, B. M., Varsani, A., and Martin, D. P. 2014. SDT: A virus classification tool based on pairwise sequence alignment and identity calculation. PLoS One 9:e108277.
Natsume, S., Takagi, H., Shiraishi, A., Murata, J., Toyonaga, H., Patzak, J., Takagi, M., Yaegashi, H., Uemura, A., Mitsuoka, C., Yoshida, K., Krofta, K., Satake, H., Terauchi, R., and Ono, E. 2015. The draft genome of hop (Humulus lupulus), an essence for brewing. Plant Cell Physiol. 56:428-441.
Neri, U., Wolf, Y. I., Roux, S., Camargo, A. P., Lee, B., Kazlauskas, D., Chen, I. M., Ivanova, N., Zeigler Allen, L., Paez-Espino, D., Bryant, D. A., Bhaya, D., Krupovic, M., Dolja, V. V., Kyrpides, N. C., Koonin, E. V., Gophna, U., Narrowe, A. B., Probst, A. J., Sczyrba, A., Kohler, A., Séguin, A., Shade, A., Campbell, B. J., Lindahl, B. D., Reese, B. K., Roque, B. M., DeRito, C., Averill, C., Cullen, D., Beck, D. A. C., Walsh, D. A., Ward, D. M., Wu, D., Eloe-Fadrosh, E., Brodie, E. L., Young, E. B., Lilleskov, E. A., Castillo, F. J., Martin, F. M., LeCleir, G. R., Attwood, G. T., Cadillo-Quiroz, H., Simon, H. M., Hewson, I., Grigoriev, I. V., Tiedje, J. M., Jansson, J. K., Lee, J., VanderGheynst, J. S., Dangl, J., Bowman, J. S., Blanchard, J. L., Bowen, J. L., Xu, J., Banfield, J. F., Deming, J. W., Kostka, J. E., Gladden, J. M., Rapp, J. Z., Sharpe, J., McMahon, K. D., Treseder, K. K., Bidle, K. D., Wrighton, K. C., Thamatrakoln, K., Nusslein, K., Meredith, L. K., Ramirez, L., Buee, M., Huntemann, M., Kalyuzhnaya, M. G., Waldrop, M. P., Sullivan, M. B., Schrenk, M. O., Hess, M., Vega, M. A., O’Malley, M. A., Medina, M., Gilbert, N. E., Delherbe, N., Mason, O. U., Dijkstra, P., Chuckran, P. F., Baldrian, P., Constant, P., Stepanauskas, R., Daly, R. A., Lamendella, R., Gruninger, R. J., McKay, R. M., Hylander, S., Lebeis, S. L., Esser, S. P., Acinas, S. G., Wilhelm, S. S., Singer, S. W., Tringe, S. S., Woyke, T., Reddy, T. B. K., Bell, T. H., Mock, T., McAllister, T., Thiel, V., Denef, V. J., Liu, W.-T., Martens-Habbena, W., Allen Liu, X.-J., Cooper, Z. S., and Wang, Z. 2022. Expansion of the global RNA virome reveals diverse clades of bacteriophages. Cell 185:4023-4037.e18.
Orfanidou, C. G., Katiou, D., Papadopoulou, E., Katis, N. I., and Maliogka, V. I. 2022. A known ilarvirus is associated with a novel viral disease in pepper. Plant Pathol. 71:1901-1909.
Palanga, E., Filloux, D., Martin, D. P., Fernandez, E., Gargani, D., Ferdinand, R., Zabré, J., Bouda, Z., Neya, J. B., Sawadogo, M., Traore, O., Peterschmitt, M., and Roumagnac, P. 2016. Metagenomic-based screening and molecular characterization of cowpea-infecting viruses in Burkina Faso. PLoS One 11:e0165188.
Pallas, V., Aparicio, F., Herranz, M. C., Amari, K., Sanchez-Pina, M. A., Myrta, A., and Sanchez-Navarro, J. A. 2012. Ilarviruses of Prunus spp.: A continued concern for fruit trees. Phytopathology 102:1108-1120.
Parrella, G., Troiano, E., Cherchi, C., and Giordano, P. 2020. Severe outbreaks of Parietaria mottle virus in tomato in Sardinia, Southern Italy. J. Plant Pathol. 102:915-915.
Pecman, A., Adams, I., Gutiérrez-Aguirre, I., Fox, A., Boonham, N., Ravnikar, M., and Kutnjak, D. 2022. Systematic comparison of Nanopore and Illumina sequencing for the detection of plant viruses and viroids using total RNA sequencing approach. Front. Microbiol. 13:1424.
Pecman, A., Kutnjak, D., Gutiérrez-Aguirre, I., Adams, I., Fox, A., Boonham, N., and Ravnikar, M. 2017. Next generation sequencing for detection and discovery of plant viruses and viroids: Comparison of two approaches. Front. Microbiol. 8:1-10.
Poudel, B., Ho, T., Laney, A., Khadgi, A., and Tzanetakis, I. E. 2014. Epidemiology of Blackberry chlorotic ringspot virus. Plant Dis. 98:547-550.
Rai, A., Nakaya, T., Shimizu, Y., Rai, M., Nakamura, M., Suzuki, H., Saito, K., and Yamazaki, M. 2018. De novo transcriptome assembly and characterization of Lithospermum officinale to discover putative genes involved in specialized metabolites biosynthesis. Planta Med. 84:920-934.
Ristaino, J. B., Anderson, P. K., Bebber, D. P., Brauman, K. A., Cunniffe, N. J., Fedoroff, N. V., Finegold, C., Garrett, K. A., Gilligan, C. A., Jones, C. M., Martin, M. D., MacDonald, G. K., Neenan, P., Records, A., Schmale, D. G., Tateosian, L., and Wei, Q. 2021. The persistent threat of emerging plant disease pandemics to global food security. Proc. Natl. Acad. Sci. 118:e2022239118.
Rivarez, M. P. S., Pecman, A., Bačnik, K., Maksimović, O., Vučurović, A., Seljak, G., Mehle, N., Gutiérrez-Aguirre, I., Ravnikar, M., and Kutnjak, D. 2023. In-depth study of tomato and weed viromes reveals undiscovered plant virus diversity in an agroecosystem. Microbiome 11:60.
Rivarez, M. P. S., Vučurović, A., Mehle, N., Ravnikar, M., and Kutnjak, D. 2021. Global advances in tomato virome research: Current status and the impact of high-throughput sequencing. Front. Microbiol. 12:671925.
Roberts, J. M. K., Ireland, K. B., Tay, W. T., and Paini, D. 2018. Honey bee-assisted surveillance for early plant virus detection. Ann. Appl. Biol. 173: 285-293.
Roux, B., Rodde, N., Jardinaud, M.-F., Timmers, T., Sauviac, L., Cottret, L., Carrère, S., Sallet, E., Courcelle, E., Moreau, S., Debellé, F., Capela, D., de Carvalho-Niebel, F., Gouzy, J., Bruand, C., and Gamas, P. 2014. An integrated analysis of plant and bacterial gene expression in symbiotic root nodules using laser-capture microdissection coupled to RNA sequencing. Plant J. 77:817-837.
Rozas, J., Ferrer-Mata, A., Sánchez-DelBarrio, J. C., Guirao-Rico, S., Librado, P., Ramos-Onsins, S. E., and Sánchez-Gracia, A. 2017. DnaSP 6: DNA Sequence Polymorphism Analysis of Large Data Sets. Mol. Biol. Evol. 34:3299-3302.
Schönegger, D. 2023. Analysis of the virome and reciprocal transfers of viruses between cultivated and wild carrot populations. Ph.D. Thesis. https://theses.hal.science/tel-04033935
Sdoodee, R., and Teakle, D. 1988. Seed and pollen transmission of tobacco streak virus in tomato (Lycopersicon esculentum cv. Grosse Lisse). Aust. J. Agric. Res. 39:469.
Sdoodee, R., and Teakle, D. S. 1993. Studies on the mechanism of transmission of pollen-associated tobacco streak ilarvirus virus by Thrips tabaci. Plant Pathol. 42:88-92.
Sharman, M., Thomas, J. E., and Persley, D. M. 2015. Natural host range, thrips and seed transmission of distinct Tobacco streak virus strains in Queensland, Australia. Ann. Appl. Biol. 167:197-207.
Simkovich, A., Kohalmi, S. E., and Wang, A. 2021. Ilarviruses (Bromoviridae). Pages 439-446 in: Encyclopedia of Virology (Fourth Edition). D. H. Bamford and M. Zuckerman, eds. Academic Press, Oxford, U.K.
Sproviero, D., Gagliardi, S., Zucca, S., Arigoni, M., Giannini, M., Garofalo, M., Olivero, M., Dell’Orco, M., Pansarasa, O., Bernuzzi, S., Avenali, M., Cotta Ramusino, M., Diamanti, L., Minafra, B., Perini, G., Zangaglia, R., Costa, A., Ceroni, M., Perrone-Bizzozero, N. I., Calogero, R. A., and Cereda, C. 2021. Different miRNA profiles in plasma derived small and large extracellular vesicles from patients with neurodegenerative diseases. Int. J. Mol. Sci. 22:2737.
Stewart, C., Kon, T., Rojas, M., Graham, A., Martin, D., Gilbertson, R., and Roye, M. 2014. The molecular characterisation of a Sida-infecting begomovirus from Jamaica. Arch. Virol. 159:375-378.
Subramanian, S. 2016. The effects of sample size on population genomic analyses – Implications for the tests of neutrality. BMC Genomics 17:123.
Svanella-Dumas, L., Candresse, T., Lefebvre, M., Lluch, J., Valiere, S., Larignon, P., and Marais, A. 2022. First report of grapevine virus L infecting grapevine in Southeast France. Plant Dis. 106:1536.
Tauber, J. P., McMahon, D., Ryabov, E. V., Kunat, M., Ptaszyńska, A. A., and Evans, J. D. 2022. Honeybee intestines retain low yeast titers, but no bacterial mutualists, at emergence. Yeast 39:95-107.
Temple, C., Blouin, A. G., Boezen, D., Botermans, M., Durant, L., Jonghe, K. D., de Koning, P., Goedefroit, T., Minet, L., Steyer, S., Verdin, E., Zwart, M., and Massart, S. 2023. Biological characterization of an emergent virus infecting vegetables in diversified production systems: Physostegia chlorotic mottle virus. BioRxiv 535357.v2.
Temple, C., Blouin, A. G., De Jonghe, K., Foucart, Y., Botermans, M., Westenberg, M., Schoen, R., Gentit, P., Visage, M., Verdin, E., Wipf-Scheibel, C., Ziebell, H., Gaafar, Y. Z. A., Zia, A., Yan, X.-H., Richert-Pöggeler, K. R., Ulrich, R., Rivarez, M. P. S., Kutnjak, D., Vučurović, A., and Massart, S. 2022. Biological and genetic characterization of physostegia chlorotic mottle virus in Europe based on host range, location, and time. Plant Dis. 106:2797-2807.
Vannette, R. L., Mohamed, A., and Johnson, B. R. 2015. Forager bees (Apis mellifera) highly express immune and detoxification genes in tissues associated with nectar processing. Sci. Rep. 5:16224.
Vargas-Asencio, J., McLane, H., Bush, E., and Perry, K. L. 2013. Spinach latent virus infecting tomato in Virginia, United States. Plant Dis. 97:1663.
Verhoeven, A., Kloth, K. J., Kupczok, A., Oymans, G. H., Damen, J., Rijnsburger, K., Jiang, Z., Deelen, C., Sasidharan, R., van Zanten, M., and van der Vlugt, R. A. A. 2023. Arabidopsis latent virus 1, a comovirus widely spread in Arabidopsis thaliana collections. New Phytol. 237:1146-1153.
Wu, M., Kostyun, J. L., Hahn, M. W., and Moyle, L. C. 2018. Dissecting the basis of novel trait evolution in a radiation with widespread phylogenetic discordance. Mol. Ecol. 27:3301-3316.
Xu, C., Sun, X., Taylor, A., Jiao, C., Xu, Y., Cai, X., Wang, X., Ge, C., Pan, G., Wang, Q., Fei, Z., and Wang, Q. 2017. Diversity, distribution, and evolution of tomato viruses in China uncovered by small RNA sequencing. J. Virol. 91:e00173-17.
Zayed, A. A., Wainaina, J. M., Dominguez-Huerta, G., Pelletier, E., Guo, J., Mohssen, M., Tian, F., Pratama, A. A., Bolduc, B., Zablocki, O., Cronin, D., Solden, L., Delage, E., Alberti, A., Aury, J.-M., Carradec, Q., da Silva, C., Labadie, K., Poulain, J., Ruscheweyh, H.-J., Salazar, G., Shatoff, E., Bundschuh, R., Fredrick, K., Kubatko, L. S., Chaffron, S., Culley, A. I., Sunagawa, S., Kuhn, J. H., Wincker, P., Sullivan, M. B., Acinas, S. G., Babin, M., Bork, P., Boss, E., Bowler, C., Cochrane, G., de Vargas, C., Gorsky, G., Guidi, L., Grimsley, N., Hingamp, P., Iudicone, D., Jaillon, O., Kandels, S., Karp-Boss, L., Karsenti, E., Not, F., Ogata, H., Poulton, N., Pesant, S., Sardet, C., Speich, S., Stemmann, L., Sullivan, M. B., Sungawa, S., and Wincker, P. 2022. Cryptic and abundant marine viruses at the evolutionary origins of Earth’s RNA virome. Science 376:156-162.