[en] Saffron (Crocus sativus L.) is a vegetatively propagated crop of high economic and cultural value, potentially affected by viral infections that may impact its productivity. Despite Iran's dominance in global saffron production, knowledge of its virome remains limited. In this study, we conducted the first nationwide virome survey of saffron in Iran employing a high-throughput sequencing (HTS) approach on pooled samples obtained from eleven provinces in Iran and one location in Afghanistan. Members of three virus families were detected-Potyviridae (Potyvirus), Solemoviridae (Polerovirus), and Geminiviridae (Mastrevirus)-as well as one satellite from the family Alphasatellitidae (Clecrusatellite). A novel Potyvirus, tentatively named saffron Iran virus (SaIRV) and detected in three provinces, shares less than 68% nucleotide identity with known Potyvirus species, thus meeting the ICTV criteria for designation as a new species. Genetic diversity analyses revealed substantial intrapopulation SNP variation but no clear geographical clustering. Among the two wild Crocus species sampled, only Crocus speciosus harbored turnip mosaic virus. Virome network and phylogenetic analyses confirmed widespread viral circulation likely driven by corm-mediated propagation. Our findings highlight the need for targeted certification programs and biological characterization of key viruses to mitigate potential impacts on saffron yield and quality.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Valouzi, Hajar ; Department of Plant Protection, Faculty of Agriculture, University College of Agriculture & Natural Resources, University of Tehran, Karaj 7787131587, Iran
Dizadji, Akbar ; Department of Plant Protection, Faculty of Agriculture, University College of Agriculture & Natural Resources, University of Tehran, Karaj 7787131587, Iran
Golnaraghi, Alireza; Department of Plant Protection, Faculty of Agricultural Sciences and Food Industries, Science and Research Branch, Islamic Azad University, Tehran 1477893855, Iran ; Department of Earth, Ocean & Atmospheric Sciences, University of British Columbia, Vancouver, BC V6T 1Z4, Canada ; Department of Biodiversity, BoomZista Institute, Vancouver, BC V6M 3W4, Canada
Salami, Seyed Alireza; Department of Horticultural Science, Faculty of Agriculture, University of Tehran, Karaj 7787131587, Iran
Fontdevila Pareta, Nuria ; Integrated and Urban Plant Pathology Laboratory, TERRA Teaching and Research Centre, Gembloux Agro-Bio Tech, University of Liège, 5030 Gembloux, Belgium ; Plant Protection Department, Agroscope, 1260 Nyon, Switzerland
Önder, Serkan ; Integrated and Urban Plant Pathology Laboratory, TERRA Teaching and Research Centre, Gembloux Agro-Bio Tech, University of Liège, 5030 Gembloux, Belgium ; Department of Plant Protection, Faculty of Agriculture, Eskişehir Osmangazi University, Eskişehir 26160, Türkiye
Selmi, Ilhem; Integrated and Urban Plant Pathology Laboratory, TERRA Teaching and Research Centre, Gembloux Agro-Bio Tech, University of Liège, 5030 Gembloux, Belgium
Rollin, Johan ; Integrated and Urban Plant Pathology Laboratory, TERRA Teaching and Research Centre, Gembloux Agro-Bio Tech, University of Liège, 5030 Gembloux, Belgium ; DNAVision, 6041 Gosselies, Belgium
Berhal, Chadi ; Integrated and Urban Plant Pathology Laboratory, TERRA Teaching and Research Centre, Gembloux Agro-Bio Tech, University of Liège, 5030 Gembloux, Belgium
Tamisier, Lucie ; GAFL (Genetics and Improvement of Fruit and Vegetables), INRAE, Montfavet, 84140 Avignon, France
Maclot, François ; Integrated and Urban Plant Pathology Laboratory, TERRA Teaching and Research Centre, Gembloux Agro-Bio Tech, University of Liège, 5030 Gembloux, Belgium ; UMR 1332 Biologie du Fruit et Pathologie (BFP), INRAE, Department of Environmental Sciences, University of Bordeaux, CS20032, 33882 Villenave d'Ornon Cedex, France
Wang, Long; Archaeal Biology Center, Institute for Advanced Study, Shenzhen University, Shenzhen 518060, China ; Shenzhen Key Laboratory of Marine Microbiome Engineering, Institute for Advanced Study, Shenzhen University, Shenzhen 518060, China
Zhang, Rui ; Archaeal Biology Center, Institute for Advanced Study, Shenzhen University, Shenzhen 518060, China ; Shenzhen Key Laboratory of Marine Microbiome Engineering, Institute for Advanced Study, Shenzhen University, Shenzhen 518060, China
INSF - Iran National Science Foundation University of Tehran FNS - Fonds National Suisse de la Recherche scientifique
Funding text :
This research was funded by the Iran National Science Foundation (INSF, Grant No. 4000914), the University of Tehran (Grant No. 73148924/6/19), the Fonds National de la Recherche Scientifique (FNRS, Belgium, Grant No. J.0149.20), the Second Tibetan Plateau Scientific Expedition and Research Program (STEP) (2024QZKK02010304), the Innovation Team Project of Universities in Guangdong Province (2023KCXTD028), and the Scientific Instrument Developing Project of Shenzhen University (2024YQ004).
Hill T. The Contemporary Encyclopedia of Herbs & Spices: Seasonings for the Global Kitchen Wiley Hoboken, NJ, USA 2004 464p
Taheri-Dehkordi A. Naderi R. Martinelli F. Salami S.A. A robust workflow for indirect somatic embryogenesis and cormlet production in saffron (Crocus sativus L.) and its wild allies; C. caspius and C. speciosus Heliyon 2020 6 e05841 10.1016/j.heliyon.2020.e05841
Lopez-Corcoles H. Brasa-Ramos A. Montero-Garcia F. Romero-Valverde M. Montero-Riquelme F. Phenological growth stages of saffron plant (Crocus sativus L.) according to the BBCH Scale Span. J. Agric. Res. 2015 13 e09SC01 10.5424/sjar/2015133-7340
Shahnoushi N. Abolhassani L. Kavakebi V. Reed M. Saghaian S. Economic analysis of saffron production Saffron Elsevier Amsterdam, The Netherlands 2020 337 356
Salehi A. Shariatifar N. Pirhadi M. Zeinali T. An overview on different detection methods of saffron (Crocus sativus L.) adulterants J. Food Meas. Charact. 2022 16 4996 5006 10.1007/s11694-022-01586-w
Yousefi M. Shafaghi K. Saffron in Persian traditional medicine Saffron Elsevier Amsterdam, The Netherlands 2020 393 404
Fekrat H. The application of crocin and saffron ethanol-extractable components in formulation of health care and beauty care products I International Symposium on Saffron Biology and Biotechnology 650 ISHS Leuven, Belgium 2003 365 368
Kyriakoudi A. Ordoudi S. Roldán-Medina M. Tsimidou M. Saffron, a functional spice Austin J. Nutr. Food Sci. 2015 3 1059
Jafari S.-M. Tsimidou M.Z. Rajabi H. Kyriakoudi A. Bioactive ingredients of saffron: Extraction, analysis, applications Saffron Woodhead Publishing–Elsevier Duxford, UK 2020 261 290
Vahedi M. Kabiri M. Salami S.A. Rezadoost H. Mirzaie M. Kanani M.R. Quantitative HPLC-based metabolomics of some Iranian saffron (Crocus sativus L.) accessions Ind. Crops Prod. 2018 118 26 29 10.1016/j.indcrop.2018.03.024
Ahrazem O. Rubio-Moraga A. Castillo-López R. Trapero-Mozos A. Gómez-Gómez L. Crocus sativus pathogens and defence responses Functional Plant Science and Biotechnology Global Science Book Isleworth, UK 2010 81 90
Russo M. Martelli G. Cresti M. Ciampolini F. Bean yellow mosaic virus in saffron/il virus del mosaico giallo del fagiolo in zafferano Phytopathol. Mediterr. 1979 18 189 191
Chen J. Occurrence and control of mosaic disease [turnip mosaic virus] in saffron (Crocus sativus) Zhejiang Nongye Kexue 2000 3 132 135
Liao F.R. Lin W.Z. Chen X.H. Chen Q. Chen H.Y. Huang P.Y. Fang Z.P. Wu Y. Shen J.G. Lin S.M. Molecular identification and sequence analysis of Ornithogalum mosaic virus in saffron (Crocus sativus) corms Sci. Agric. Sin. 2017 50 4046 4054
Parizad S. Dizadji A. Koohi Habibi M. Winter S. Kalantari S. Movi S. García-Arenal F. Ayllón M.A. Description and genetic variation of a distinct species of Potyvirus infecting saffron (Crocus sativus L.) plants in major production regions in Iran Ann. Appl. Biol. 2018 173 233 242 10.1111/aab.12456
Zheng H. Wu X. Han K. Chen Z. Song X. Peng J. Lu Y. Lin L. Chen J. Yan F. First Report of Beet western yellows virus Infecting Crocus sativus in China Plant Dis. 2018 102 1471 10.1094/PDIS-10-17-1579-PDN
Tavoosi M. Molecular Detection and Investigation of Irish severe mosaic virus in Saffron, Fields of Razavi and South Khorasan J. Saffron Res. 2022 9 323 334
Tavoosi M. Moradi Z. Mehrvar M. Virome analysis of potyvirus populations infecting saffron in Iran: The discovery of a novel potyvirus Eur. J. Plant Pathol. 2024 168 453 466 10.1007/s10658-023-02767-z
Ágoston J. Almási A. Pinczés D. Sáray R. Salánki K. Palkovics L. First report of saffron latent virus in Crocus sativus from Hungary Plant Dis. 2024 108 540 10.1094/PDIS-09-23-1765-PDN
Martinez-Fajardo C. Navarro-Simarro P. Morote L. Rubio-Moraga Á. Mondéjar-López M. Niza E. Argandoña J. Ahrazem O. Gómez-Gómez L. López-Jiménez A.J. Exploring the viral landscape of saffron through metatranscriptomic analysis Virus Res. 2024 345 199389 10.1016/j.virusres.2024.199389 38714217
Atefeh Hosseini S. Julian C. Galzi S. Filloux D. Roumagnac P. First report of saffron-associated mastrevirus 1 from saffron in Iran Plant Dis. 2025 109 513 10.1094/PDIS-11-24-2462-PDN
Valouzi H. Dizadji A. Golnaraghi A. Salami S. Selmi I. Fontdevila Pareta N. Önder S. Massart S. First detection of saffron dwarf virus, wheat dwarf virus, wheat dwarf virus-associated alphasatellite and a new putative potyvirus species in saffron in Iran New Dis. Rep. 2025 51 70022 10.1002/ndr2.70022
Tavoosi M. Moradi Z. Mehrvar M. Zakiaghl M. First identification and complete genomic characterization of saffron dwarf virus from Iran, a novel mastrevirus infecting Crocus sativus Eur. J. Plant Pathol. 2025 163 1 11 10.1007/s10658-025-03051-y
Parizad S. Dizadji A. Habibi M.K. Winter S. Kalantari S. Movi S. Tendero C.L. Alonso G.L. Moratalla-Lopez N. The effects of geographical origin and virus infection on the saffron (Crocus sativus L.) quality Food Chem. 2019 295 387 394 10.1016/j.foodchem.2019.05.116
Moratalla-López N. Parizad S. Habibi M.K. Winter S. Kalantari S. Bera S. Lorenzo C. García-Rodríguez M.V. Dizadji A. Alonso G.L. Impact of two different dehydration methods on saffron quality, concerning the prevalence of Saffron latent virus (SaLV) in Iran Food Chem. 2021 337 127786 10.1016/j.foodchem.2020.127786
Shamshiri M. Sánchez C. Rico S. Mokhtassi-Bidgoli A. Ayyari M. Rezadoost H. Shams-Bakhsh M. Molecular, Metabolic, and Physiological Responses to Progressive Biotic Stress Caused by Cucumber Mosaic Virus and Turnip Mosaic Virus in Saffron Horticulturae 2025 11 96 10.3390/horticulturae11010096
MacDiarmid R. Rodoni B. Melcher U. Ochoa-Corona F. Roossinck M. Biosecurity implications of new technology and discovery in plant virus research PLoS Pathog. 2013 9 e1003337 10.1371/journal.ppat.1003337
Muluneh M.G. Impact of climate change on biodiversity and food security: A global perspective—A review article Agric. Food Secur. 2021 10 36 10.1186/s40066-021-00318-5
Massart S. Olmos A. Jijakli H. Candresse T. Current impact and future directions of high throughput sequencing in plant virus diagnostics Virus Res. 2014 188 90 96 10.1016/j.virusres.2014.03.029 24717426
Al Rwahnih M. Daubert S. Golino D. Islas C. Rowhani A. Comparison of next-generation sequencing versus biological indexing for the optimal detection of viral pathogens in grapevine Phytopathology 2015 105 758 763 10.1094/PHYTO-06-14-0165-R 25689518
Hou W. Li S. Massart S. Is there a “biological desert” with the discovery of new plant viruses? A retrospective analysis for new fruit tree viruses Front. Microbiol. 2020 11 592816 10.3389/fmicb.2020.592816
Temple C. Blouin A.G. De Jonghe K. Foucart Y. Botermans M. Westenberg M. Schoen R. Gentit P. Visage M. Verdin E. Biological and genetic characterization of Physostegia chlorotic mottle virus in Europe based on host range, location, and time Plant Dis. 2022 106 2797 2807 10.1094/PDIS-12-21-2800-RE
Rivarez M.P.S. Pecman A. Bačnik K. Maksimović O. Vučurović A. Seljak G. Mehle N. Gutiérrez-Aguirre I. Ravnikar M. Kutnjak D. In-depth study of tomato and weed viromes reveals undiscovered plant virus diversity in an agroecosystem Microbiome 2023 11 60 10.1186/s40168-023-01500-6
Roossinck M.J. Martin D.P. Roumagnac P. Plant virus metagenomics: Advances in virus discovery Phytopathology 2015 105 716 727 10.1094/PHYTO-12-14-0356-RVW
Maclot F. Debue V. Malmstrom C.M. Filloux D. Roumagnac P. Eck M. Tamisier L. Blouin A.G. Candresse T. Massart S. Long-term anthropogenic management and associated loss of plant diversity deeply impact virome richness and composition of Poaceae communities Microbiol. Spectr. 2023 11 e04850-22 10.1128/spectrum.04850-22
Olmos A. Boonham N. Candresse T. Gentit P. Giovani B. Kutnjak D. Liefting L. Maree H. Minafra A. Moreira A. High-throughput sequencing technologies for plant pest diagnosis: Challenges and opportunities EPPO Bull. 2018 48 219 224 10.1111/epp.12472
Licciardello G. Ferraro R. Scuderi G. Russo M. Catara A.F. A simulation of the use of high throughput sequencing as pre-screening assay to enhance the surveillance of citrus viruses and viroids in the EPPO region Agriculture 2021 11 400 10.3390/agriculture11050400
Claverie S. Varsani A. Hoareau M. Filloux D. Roumagnac P. Martin D.P. Lefeuvre P. Lett J.-M. Sorghum mastrevirus-associated alphasatellites: New geminialphasatellites associated with an African streak mastrevirus infecting wild Poaceae plants on Reunion Island Arch. Virol. 2020 165 1925 1928 10.1007/s00705-020-04685-5
Maclot F. Candresse T. Filloux D. Malmstrom C.M. Roumagnac P. Van der Vlugt R. Massart S. Illuminating an ecological blackbox: Using high throughput sequencing to characterize the plant virome across scales Front. Microbiol. 2020 11 578064 10.3389/fmicb.2020.578064 33178159
Kutnjak D. Tamisier L. Adams I. Boonham N. Candresse T. Chiumenti M. De Jonghe K. Kreuze J.F. Lefebvre M. Silva G. A primer on the analysis of high-throughput sequencing data for detection of plant viruses Microorganisms 2021 9 841 10.3390/microorganisms9040841
Moubset O. François S. Maclot F. Palanga E. Julian C. Claude L. Fernandez E. Rott P. Daugrois J.-H. Antoine-Lorquin A. Virion-associated nucleic acid-based metagenomics: A decade of advances in molecular characterization of plant viruses Phytopathology 2022 112 2253 2272 10.1094/PHYTO-03-22-0096-RVW
Claverie S. Ouattara A. Hoareau M. Filloux D. Varsani A. Roumagnac P. Martin D.P. Lett J.-M. Lefeuvre P. Exploring the diversity of Poaceae-infecting mastreviruses on Reunion Island using a viral metagenomics-based approach Sci. Rep. 2019 9 12716 10.1038/s41598-019-49134-9 31481704
Poutaraud A. Desbiez C. Lemaire O. Lecoq H. Herrbach E. Characterisation of a new potyvirus species infecting meadow saffron Colchicum autumnale Arch. Virol. 2004 149 1267 1277 10.1007/s00705-004-0307-x
Massart S. Lebas B. Chabirand A. Chappé A.M. Dreo T. Faggioli F. Harrison C. Macarthur R. Mehle N. Mezzalama M. Guidelines for improving statistical analyses of validation datasets for plant pest diagnostic tests EPPO Bull. 2022 52 419 433 10.1111/epp.12862
Maclot F.J. Debue V. Blouin A.G. Pareta N.F. Tamisier L. Filloux D. Massart S. Identification, molecular and biological characterization of two novel secovirids in wild grass species in Belgium Virus Res. 2021 298 198397 10.1016/j.virusres.2021.198397
Rong W. Rollin J. Hanafi M. Roux N. Massart S. Validation of high-throughput sequencing as virus indexing test for Musa germplasm: Performance criteria evaluation and contamination monitoring using an alien control Phyto. Front. 2023 3 91 102 10.1094/PHYTOFR-03-22-0030-FI
Palanga E. Filloux D. Martin D.P. Fernandez E. Gargani D. Ferdinand R. Zabré J. Bouda Z. Neya J.B. Sawadogo M. Metagenomic-based screening and molecular characterization of cowpea-infecting viruses in Burkina Faso PLoS ONE 2016 11 e0165188 10.1371/journal.pone.0165188
François S. Filloux D. Fernandez E. Ogliastro M. Roumagnac P. Viral metagenomics approaches for high-resolution screening of multiplexed arthropod and plant viral communities Viral Metagenomics: Methods and Protocols Springer New York, NY, USA 2018 77 95
Lebas B. Adams I. Al Rwahnih M. Baeyen S. Bilodeau G.J. Blouin A.G. Boonham N. Candresse T. Chandelier A. De Jonghe K. Facilitating the adoption of high-throughput sequencing technologies as a plant pest diagnostic test in laboratories: A step-by-step description EPPO Bull. 2022 52 394 418 10.1111/epp.12863
Rollin J. Demultiplexing: Diagnostic Existing Demultiplexing Issue in Metagenomic Virus. GitHub 2020 Available online: https://github.com/johrollin/demultiplexing (accessed on 22 August 2022)
Altschul S.F. Madden T.L. Schäffer A.A. Zhang J. Zhang Z. Miller W. Lipman D.J. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs Nucleic Acids Res. 1997 25 3389 3402 10.1093/nar/25.17.3389
Afgan E. Baker D. Batut B. Van Den Beek M. Bouvier D. Čech M. Chilton J. Clements D. Coraor N. Grüning B.A. The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2018 update Nucleic Acids Res. 2018 46 W537 W544 10.1093/nar/gky379
Tamura K. Stecher G. Kumar S. MEGA11: Molecular evolutionary genetics analysis version 11 Mol. Biol. Evol. 2021 38 3022 3027 10.1093/molbev/msab120 33892491
Letunic I. Bork P. Interactive Tree Of Life (iTOL) v5: An online tool for phylogenetic tree display and annotation Nucleic Acids Res. 2021 49 W293 W296 10.1093/nar/gkab301 33885785
Nyirakanani C. Tamisier L. Bizimana J.P. Rollin J. Nduwumuremyi A. Bigirimana V.d.P. Selmi I. Lasois L. Vanderschuren H. Massart S. Going beyond consensus genome sequences: An innovative SNP-based methodology reconstructs different Ugandan cassava brown streak virus haplotypes at a nationwide scale in Rwanda Virus Evol. 2023 9 vead053 10.1093/ve/vead053 37692897
Nelson C.W. Moncla L.H. Hughes A.L. SNPGenie: Estimating evolutionary parameters to detect natural selection using pooled next-generation sequencing data Bioinformatics 2015 31 3709 3711 10.1093/bioinformatics/btv449
Farzadfar S. Tomitaka Y. Ikematsu M. Golnaraghi A.R. Pourrahim R. Ohshima K. Molecular characterisation of Turnip mosaic virus isolates from Brassicaceae weeds Eur. J. Plant Pathol. 2009 124 45 55 10.1007/s10658-008-9390-2
Parizad S. Dizadji A. Habibi M.K. Winter S. Kalantari S. Garcıa-Arenal F. Ayllón M. Prevalence of saffron latent virus (SaLV), a new Potyvirus species, in saffron fields of Iran J. Plant Pathol. 2017 99 799 818
Keremane M. Singh K. Ramadugu C. Krueger R.R. Skaggs T.H. Next generation sequencing, and development of a pipeline as a tool for the detection and discovery of citrus pathogens to facilitate safer germplasm exchange Plants 2024 13 411 10.3390/plants13030411
Parizipour M.H.G. Schubert J. Behjatnia S.A.A. Afsharifar A. Habekuß A. Wu B. Phylogenetic analysis of Wheat dwarf virus isolates from Iran Virus Genes 2017 53 266 274 10.1007/s11262-016-1412-0 27900587
Köklü G. Ramsell J.N. Kvarnheden A. The complete genome sequence for a Turkish isolate of Wheat dwarf virus (WDV) from barley confirms the presence of two distinct WDV strains Virus Genes 2007 34 359 366 10.1007/s11262-006-0029-0
Huang A. Svanella-Dumas L. Vitry C. Marais A. Faure C. Candresse T. A new geminialphasatellite associated with wheat dwarf virus identified in winter barley in France Arch. Virol. 2024 169 162 10.1007/s00705-024-06090-8
Briddon R.W. Martin D.P. Roumagnac P. Navas-Castillo J. Fiallo-Olivé E. Moriones E. Lett J.-M. Zerbini F.M. Varsani A. Alphasatellitidae: A new family with two subfamilies for the classification of geminivirus-and nanovirus-associated alphasatellites Arch. Virol. 2018 163 2587 2600 10.1007/s00705-018-3854-2
Inoue-Nagata A.K. Jordan R. Kreuze J. Li F. López-Moya J.J. Mäkinen K. Ohshima K. Wylie S.J. Consortium I.R. ICTV virus taxonomy profile: Potyviridae 2022 J. Gen. Virol. 2022 103 001738 10.1099/jgv.0.001738
Ho S. Fukagawa H. Gibbs A. Golnaraghi A. Ikematsu M. Katis N. Korkmaz S. Ohshima K. Soda H. Yasaka R. The Timescale of Emergence and Spread of Turnip Mosaic Potyvirus Sci. Rep. 2017 7 4240 10.1038/s41598-017-01934-7 28652582
Ohshima K. Mitoma S. Gibbs A.J. The genetic diversity of narcissus viruses related to turnip mosaic virus blur arbitrary boundaries used to discriminate potyvirus species PLoS ONE 2018 13 e0190511 10.1371/journal.pone.0190511
Zhang B. Li Q. Hu J. Zhang L. Dong X. Ji P. Dong J. Complete genome sequence analysis of a new potyvirus isolated from Paris polyphylla var. yunnanensis Arch. Virol. 2023 168 43 10.1007/s00705-022-05655-9
de Vries J.J. Brown J.R. Couto N. Beer M. Le Mercier P. Sidorov I. Papa A. Fischer N. Oude Munnink B.B. Rodriquez C. Recommendations for the introduction of metagenomic next-generation sequencing in clinical virology, part II: Bioinformatic analysis and reporting J. Clin. Virol. 2021 138 104812 10.1016/j.jcv.2021.104812 33819811
López-Labrador F.X. Brown J.R. Fischer N. Harvala H. Van Boheemen S. Cinek O. Sayiner A. Madsen T.V. Auvinen E. Kufner V. Recommendations for the introduction of metagenomic high-throughput sequencing in clinical virology, part I: Wet lab procedure J. Clin. Virol. 2021 134 104691 10.1016/j.jcv.2020.104691
Nizamani M.M. Zhang Q. Muhae-Ud-Din G. Wang Y. High-throughput sequencing in plant disease management: A comprehensive review of benefits, challenges, and future perspectives Phytopathol. Res. 2023 5 44 10.1186/s42483-023-00199-5
François S. Bernardo P. Filloux D. Roumagnac P. Yaverkovski N. Froissart R. Ogliastro M. A novel itera-like densovirus isolated by viral metagenomics from the sea barley Hordeum marinum Genome Announc. 2014 2 e01196-14 10.1128/genomeA.01196-14
Filloux D. Fernandez E. Comstock J.C. Mollov D. Roumagnac P. Rott P. Viral metagenomic-based screening of sugarcane from Florida reveals occurrence of six sugarcane-infecting viruses and high prevalence of Sugarcane yellow leaf virus Plant Dis. 2018 102 2317 2323 10.1094/PDIS-04-18-0581-RE
Schönegger D. Moubset O. Margaria P. Menzel W. Winter S. Roumagnac P. Marais A. Candresse T. Benchmarking of virome metagenomic analysis approaches using a large, 60+ members, viral synthetic community J. Virol. 2023 97 e01300 e01323 10.1128/jvi.01300-23
Bernardo P. Charles-Dominique T. Barakat M. Ortet P. Fernandez E. Filloux D. Hartnady P. Rebelo T.A. Cousins S.R. Mesleard F. Geometagenomics illuminates the impact of agriculture on the distribution and prevalence of plant viruses at the ecosystem scale ISME J. 2018 12 173 184 10.1038/ismej.2017.155
Ma Y. Marais A. Lefebvre M. Theil S. Svanella-Dumas L. Faure C. Candresse T. Phytovirome analysis of wild plant populations: Comparison of double-stranded RNA and virion-associated nucleic acid metagenomic approaches J. Virol. 2019 94 e01462-19 10.1128/JVI.01462-19 31597769
Masangwa J.I.G. Pareta N.F. Moses P. Hřibová E. Doležel J. Fandika I. Massart S. Surveillance and molecular characterization of banana viruses and their association with Musa germplasm in Malawi bioRxiv 2024 10.1101/2024.06.24.600487
Ren Y. Xu Y. Lee W.M. Di Bisceglie A.M. Fan X. In-depth serum virome analysis in patients with acute liver failure with indeterminate etiology Arch. Virol. 2020 165 127 135 10.1007/s00705-019-04466-9
Gorbalenya A.E. Lauber C. Siddell S.G. Taxonomy of Viruses Reference Module in Biomedical Sciences Elsevier Amsterdam, The Netherlands 2019 10.1016/B978-0-12-801238-3.99237-7
Futschik A. Schlötterer C. The next generation of molecular markers from massively parallel sequencing of pooled DNA samples Genetics 2010 186 207 218 10.1534/genetics.110.114397 20457880
Technow F. Gerke J. Parent-progeny imputation from pooled samples for cost-efficient genotyping in plant breeding PLoS ONE 2017 12 e0190271 10.1371/journal.pone.0190271 29272307
Ko B. Van Raamsdonk J.M. RNA sequencing of pooled samples effectively identifies differentially expressed genes Biology 2023 12 812 10.3390/biology12060812 37372097
Matthews A.E. Boves T.J. Percy K.L. Schelsky W.M. Wijeratne A.J. Population Genomics of Pooled Samples: Unveiling Symbiont Infrapopulation Diversity and Host–Symbiont Coevolution Life 2023 13 2054 10.3390/life13102054
Tabasi M. Mehrabian A. Sayadi S. Distribution patterns and conservation status of Crocus species in Iran, one of the diversity centers of Crocus in the Middle East Folia Oecologica 2021 48 156 168 10.2478/foecol-2021-0016
Movi S. Dizadji A. Parizad S. Zarghani S.N. Biological characteristics and genetic variation analyses of saffron latent virus (SaLV) based on genomic P1-Pro and P3 regions Eur. J. Plant Pathol. 2022 164 299 312 10.1007/s10658-022-02561-3
Maachi A. Donaire L. Hernando Y. Aranda M.A. Genetic differentiation and migration fluxes of viruses from melon crops and crop edge weeds J. Virol. 2022 96 e00421 e00422 10.1128/jvi.00421-22
Schönegger D. Marais A. Babalola B.M. Faure C. Lefebvre M. Svanella-Dumas L. Brázdová S. Candresse T. Carrot populations in France and Spain host a complex virome rich in previously uncharacterized viruses PLoS ONE 2023 18 e0290108 10.1371/journal.pone.0290108
Tavoosi M. Moradi Z. Mehrvar M. First report of Turnip mosaic virus infecting saffron in Iran Virus Dis. 2022 33 489 491 10.1007/s13337-022-00798-4 36447818
Tatineni S. Hein G.L. Plant viruses of agricultural importance: Current and future perspectives of virus disease management strategies Phytopathology 2023 113 117 141 10.1094/PHYTO-05-22-0167-RVW
Khatun M.F. Kwak M. Kwon M. Hossain M.M. Kil E.-J. New insights into viral threats in soybean (Glycine max) crops from Bangladesh, including a novel crinivirus Front. Microbiol. 2025 16 1523767 10.3389/fmicb.2025.1523767
Fontdevila Pareta N. Khalili M. Maachi A. Rivarez M.P.S. Rollin J. Salavert F. Temple C. Aranda M.A. Boonham N. Botermans M. Managing the deluge of newly discovered plant viruses and viroids: An optimized scientific and regulatory framework for their characterization and risk analysis Front. Microbiol. 2023 14 1181562 10.3389/fmicb.2023.1181562
Lorenzo C. Shadmani G. Valouzi H. Moratalla-López N. Bahlolzada H. Sánchez-Gómez R. Dizadji A. Alonso G.L. Saffron Stigmas Apocarotenoid Contents from Saffron Latent Virus (SaLV)-Infected Plants with Different Origins and Dehydration Temperatures Horticulturae 2023 9 933 10.3390/horticulturae9080933
Navalinskienė M. Samuitienė M. Viruses affecting some bulb and corm flower crops Biologija 2001 47 84 86
Alavi-Siney S.M. Saba J. Siahpirani A.F. Nasiri J. ISSR-assisted spatial genetic structure, population admixture, and biodiversity estimates across locally adopted saffron ecotypes from 18 different provenances of Iran J. Appl. Res. Med. Aromat. Plants 2023 35 100467 10.1016/j.jarmap.2023.100467
Bazoobandi M. Rahimi H. Karimi-Shahri M.R. Saffron crop protection Saffron Koocheki A. Khajeh-Hosseini M. Elsevier Amsterdam, The Netherlands 2020 169 185
Nigam D. LaTourrette K. Souza P.F. Garcia-Ruiz H. Genome-wide variation in potyviruses Front. Plant Sci. 2019 10 1439 10.3389/fpls.2019.01439 31798606
Yang X. Li Y. Wang A. Research advances in potyviruses: From the laboratory bench to the field Annu. Rev. Phytopathol. 2021 59 1 29 10.1146/annurev-phyto-020620-114550
