Garlic (Allium spp.) viruses: detection, distribution and remediation attempts in a European garlic collection
Keywords:Allium, ELISA, meristem, RT-PCR, viruses
Garlic is an important vegetable crop in numerous countries used as food and natural based medicine. Similar to the majority of vegetatively propagated plants, garlic may be affected by several viruses that can cause severe crop losses. The present study aimed to screen 105 garlic accessions (mother plants) from 5 European countries (Germany, Czech Republic, Poland, Italy, and France) for possible presence of Onion yellow dwarf virus (OYDV), Leek yellow stripe virus (LYSV), Garlic common latent virus (GCLV) and Shallot latent virus (SLV). The occurrence of three Allexiviruses (GarV-A, GarV-B and GarV-C) in mixed assays was also investigated. Meristem-tip culture assays were performed in order to attempt eradication of the studied viruses. Garlic viruses identification was made by ELISA and RT-PCR. ELISA outcomes showed that all 105 garlic accessions were infected by different virus combinations. The OYDV and LYSV were identified, by ELISA, in all countries at 96% and 88,6% respectively and by RT-PCR at 99% and 96%. Furthermore, GCLV and SLV were detected by ELISA in about 88% and by RT-PCR at 89% and 90%, respectively with the exception of the studied Allexiviruses which were not amplified by RT-PCR with ALLEX1/ALLEX2 primers. Smaller meristem size (0,3-1,5 mm) led to better virus elimination efficiency (29%) compared to 8% obtained for the larger size (2-2,5 mm). The outcomes were opposite (16% vs. 90%) for plants regeneration. Virus elimination efficiency was linked to the virus type, e.g., OYDV and LYSV were eradicated at 90% while GCLV and Allexiviruses were difficult to eliminate (57,4% and 55,6% of eradication). Given the economic relevance of garlic crops worldwide and the frequently reported incidence of viral infections, it is important to make virus-free germplasm available. Therefore, investigating the garlic germplasm sanitary status and constantly improving it is of crucial importance aiming to increase the overall garlic production.
Adams MJ, Antoniw JF, Fauquet CM (2005). Molecular criteria for genus and species discrimination within the family. Archives of Virology 150:459-479. https://doi.org/10.1007/s00705-004-0440-6
Altieri L, Camele I, Miccolis V (2010). Diagnostic aspects of virus sanitation in local garlic accessions. Italus Hortus 17(2):48-49.
Bagi F, Stojsin V, Budakov D, ElSwaeh SMA, Gvozdanovic-Varga J (2012). Effect of onion yellow dwarf virus (OYDV) on yield components of fall garlic (Allium sativum L.) in Serbia. African Journal of Agricultural Research 7:2386-2390.
Barg E (1996). Serologische und molecular genetische Untersuchungenzur Variabilitat Allium-Arteninfizierender, filamentoser Viren [Serological and molecular genetic studies on the variability of the filamentous viruses infecting Allium species]/vorgelegt von Erhard Barg.- Clausthal-Zellerfeld: Papierflieger, 1996. Zugl.: Gottingen, Univ., Germany.
Barg E, Lesemann DE, Vetten HJ, Green SK (1997). Viruses of alliums and their distribution in different Allium crops and geographical regions. Acta Horticulturae 433:607-616. https://doi.org/10.17660/ActaHortic.1997.433.69
Bereda M, Paduch-Cichal E, Dąbrowska E (2017). Occurrence and phylogenetic analysis of allexiviruses identified on garlic from China, Spain and Poland commercially available on the polish retail market. European Journal of Plant Pathology 149:227-237. https://doi.org/10.1007/s10658-017-1171-3
Boonham N, Kreuze J, Winter S, Vlugt RV, Bergervoet J, Tomlinson J, Mumford R (2014). Methods in Virus diagnostics: From ELISA to Next Generation Sequencing. Virus Research 186:20-31. https://doi.org/10.1016/j.virusres.2013.12.007
Botti S, D'Urso F, Davino S, Bertaccini A, Branca F, Davino M (2003). RT-PCR virus detection in garlic plants in Sicily. Informatore Fitopatolologico 53(4):46-49.
Canavelli A, Nome SF, Conci VC (1998). Efecto de distintos virus en la producciòn de ajo (Allium sativum) “Rosado Paraguayo”. [Distinct effects of virus on garlic production (Allium sativum) “Rosado Paraguayo”]. Fitopatologia Brasileira 23(3):354-358.
Chen J, Chen J, Adams MJ (2001). Molecular characterization of complex mixture of viruses in garlic with mosaic symptoms in China. Archives of Virology 146:1841-1853.
Chodorska M, Nowak P, Szyndel MS, Paduch-Cichal E, Sala-Rejczak K (2012). First report of Garlic virus A, Garlic virus B and Garlic virus C in garlic in Poland. Journal of Plant Pathology 94:S4. http://dx.doi.org/10.4454/JPP.V95I4SUP.038
Chodorska M, Paduch-Cichal E, Kalinowska E, Szyndel MS (2014). First report of onion yellow dwarf virus, garlic common latent virus and Shallot latent virus on Garlic in Poland. Plant Disease 98(6):858. https://doi.org/10.1094/PDIS-11-13-1160-PDN
Chodorska M, Paduch-Cichal E, Kalinowska E, Szyndel MS (2014). Assessment of allexiviruses infection in garlic plants in Poland. Acta Scientiarum Polonorum Hortorum Cultus 13(2):179-186. Retrieved from https://czasopisma.up.lublin.pl/index.php/asphc/article/view/2711
Clark MF, Adams AN (1977). Characteristics of the microplate method of enzyme-linked immunosorbent assay for the detection of plant viruses. Journal of General Virology 34:475-483. https://doi.org/10.1099/0022-1317-34-3-475
Conci VC, Cavanelli A, Lunello P (2003). Yield losses associated with virus-infected garlic plants during five successive years. Plant Disease 87:1411-1415. https://doi.org/10.1094/PDIS.2003.87.12.1411
Cremer J, Campbell P, Steele V, Persley D, Thomas J, Harper S, Gambley C (2021). Detection and distribution of viruses infecting garlic crops in Australia. Plants 10:1013. https://doi.org/10.3390/plants10051013
Delecolle B, Lot H (1981).Virosesdel’ail: Miseenévidence et essais de caracterisation par immune électromicroscopie d’un complexe de trois virus chez différentes populations d’ailatteintes de mosaïque.[Garlic viruses: Evidence and characterization tests by immune electromicroscopy of a complex of three viruses in different populations of garlic affected by mosaic] Agronomie 1:763-769.
Dovas CI, Hatziloukas E, Salomon R, Barg E, Shiboleth Y, Katis NI (2001). Comparison of methods for virus detection in Allium spp. Journal of Phytopathology 149:731-737. https://doi.org/10.1046/j.1439-0434.2001.00705.x
Dovas CI, Hatziloukas E, Salomon R, Barg E, Shiboleth Y, Katis NI (2001). Incidence of viruses infecting Allium spp. in Greece. Phytopathology 149:1-7.
Dovas CI, Vovlas C (2003). Viruses infecting Allium spp. in Southern Italy. Journal of Plant Pathology 85:135.
Fajardo TVM, Nishijima M, Buso JA, Torres AC, Ávila AC, Resende RO (2001). Garlic viral complex: identification of Potyviruses and Carlavirus in Central Brazil. Fitopatologia Brasileira 26(3):619-626.
FAOSTAT (2020). Retrieved 2022 September 1 from: www.fao.org/faostat/en/data/
Figliuolo G, Mang SM (2010). Characterization and discrimination of Mediterranean bulb-producing garlic. In: Pacurar M, Krejci G (Eds). Garlic Consumption and Health. Nova Science Publishers Inc.: New York, NY, USA, pp. 181-197.
Filho P, Resende R, Cordeiro C, Buso J, Torres A, Dusi A (2006). Viral reinfection affecting bulb production in garlic after seven years of cultivation under field conditions. European Journal of Plant Pathology 116:95-101. https://doi.org/10.1007/s10658-006-9042-3
Fritsch RM, Friesen N (2002). Evolution, Domestication and Taxonomy. In: Rabinowitch HD, Currah L (Eds). Allium Crop Science: Recent Advances. CAB International, Swizerland, pp. 5-30.
Gadhave KR, Gautam S, Rasmussen DA, Srinivasan R (2020). Aphid transmission of Potyvirus: the largest plant-infecting RNA virus genus. Viruses 12(7):773. https://doi.org/10.3390/v12070773
Ghaemizadeh F, Dashti F, Khodakaramian G, Sarikhani H (2014). Combination of stem-disc dome culture and thermotherapy to eliminate Allexiviruses and onion yellow dwarf virus from garlic (Allium sativum cv. Hamedan). Archives of Phytopathology and Plant Protection 47(4):499-507. https://doi.org/10.1080/03235408.2013.813123
Graichen K (1976). Preventive control of virus diseases of onions and leeks. (Viruskrankheiten der Zwiebel und des Porrees vorbeugendbekampfen.). Gartnerpost 28(6):7.
Guenaoui C, Mang SM, Figliuolo G, Neffatti M (2013). Diversity in Allium ampeloprasum: From small and wild to large and cultivated. Genetic Resources and Crop Evolution 60:97-114. https://doi.org/10.1007/s10722-012-9819-5
Gutiérrez AL, Barrantes GB, Navarro MP, Monge Ortega MC, Vargas Cerdas MC, Redondo Madrigal GL, (2021). General aspects about Allium sativum – a review. Ars Pharmaceutica 62(4):471-481. https://doi.org/10.30827/ars.v62i4.20843
Hadidi A, Flores R, Candresse T, Barba M (2016). Next-generation sequencing and genome editing in plant virology. Frontiers in Microbiology 7:1325. https://doi.org/10.3389/fmicb.2016.01325
Harti H, Hidayat SH, Sobir Wiyono S (2021). Detection of major viruses infecting shallot and molecular characterization of onion yellow dwarf virus from several locations in Indonesia. Biodiversitas 21(4):1697-1701. https://doi.org/10.13057/biodiv/d210451
Haque MS, Wada T, Hattori K (1999). Anatomical changes during in vitro direct formation of shoot bud from root tips in garlic (Allium sativum L.). Plant Production Science 2(2):146-153. https://doi.org/10.1626/pps.2.146
Haque MS, Wada T, Hattori K (2003). Shoot regeneration and bulblets formation from shoot and root meristem of garlic Cv. Bangladesh local. Asian Journal of Plant Sciences 2:23-27.
Ho T, Tzanetakis IE (2014). Development of a virus detection and discovery pipeline using next generation sequencing. Virology 471:54-60. https://doi.org/10.1016/j.virol.2014.09.019
Jones S, Baizan-Edge A, MacFarlane S, Torrance L (2017). Viral diagnostics in plants using next generation sequencing: computational analysis in practice. Frontiers in Plant Science 8:1770. https://doi.org/10.3389/fpls.2017.01770
Kehoe MA, Coutts BA, Buirchell BJ, Jones RAC (2014). Plant virology and next generation sequencing: experiences with a Potyvirus. PLoS One 9(8):e104580. https://doi.org/10.1371/journal.pone.0104580
Kereša S, Kurtović K, Gortea Ban S, Vončina D, Jerčić Habuš I, Bolarić S, Godena S, Mihovilović Bošnjak A (2021). Production of virus-free plants through somatic embryogenesis. Agronomy 11(5):876. https://doi.org/10.3390/agronomy11050876
Klukáčková J, Klukáková J, Navrátil M, Duchoslav M (2007). Natural infection of garlic (Allium sativum L.) by viruses in the Czech Republic/Natürliche Infektion von Knoblauch (Allium sativum L.) durch Viren in der Tschechischen Republik. Journal of Plant Disease Protection 114(3):97-100.
Lot H, Chovelon V, Souche S, Delecolle B (1998). Effects of onion yellow dwarf and leek yellow stripe viruses on symptomatology and yield loss of three French garlic cultivars. Plant Disease 82:1381-1385. https://doi.org/10.1094/PDIS.19220.127.116.111
Luciani GF, Mary AK, Pellegrini C, Curvetto NR (2006). Effects of explants and growth regulators in garlic callus formation and plant regeneration. Plant Cell, Tissue and Organ Culture 87:139-143. https://doi.org/10.1007/s11240-006-9148-5
Lunello P, Nome S, Conci V (1999). Resultados preliminare ssobre el efecto del leek yellow stripe virus (LYSV) en elcultivo de ajo. (Abstr.) (Preliminary results on the effects of Leek yellow stripe virus (LYSV) on garlic cultivars). Fitopatologìa 34(4):178.
Lunello P, Di Rienzo J, Conci VC (2007). Yield loss in garlic caused by leek yellow stripe virus Argentinean isolate. Plant Disease 91(2):153-158. https://doi.org/10.1094/PDIS-91-2-0153
Maaβ DHI, Klass M (1995). Infraspecific differentiation of garlic (Allium sativum L.) by isoenzymeand RAPD markers. Theorethical and Applied Genetics 91:89-97. https://doi.org/10.1007/BF00220863
Mansouri F, Ryšánek P (2021). Allexivirus: review and perspectives. Phytopathologia Mediterranea 60(3):389-402. https://doi.org/10.36253/phyto-12043
Matheus REF (1991). Plant Virology. 3th Edn., Academic Press Inc., Cambridge, Massachusetts, U.S.A.
Meenakshi A, Baranwal VK, Ahlawat YS, Lokendra S (2006). RT-PCR detection and molecular characterization of onion yellow dwarf virus associated with garlic and onion. Current Science 91(9):1230-1234.
Messiaen CM, Lot H, Delecolle B (1994). Thirty years of France' experience in the production of disease-free garlic and shallot mother bulbs. Acta Horticulturae 358:275-280. https://doi.org/10.17660/ActaHortic.1994.358.45
Mitiku AD, Defegu DT, Abraham A, Mejan D, Asami P, Maina S, Holton T (2020). Molecular characterization of the coat protein gene revealed considerable diversity of viral species complex in garlic (Allium sativum L.). bioRxiv. https://doi.org/10.1101/2020.12.03.409680
Mohamed SH, Zicca S, Manglli A, Elaiderous Mohamed M, El Siddig MAR, El Husein AA, Tomassoli L (2013). Occurence and phylogenetic analysis of potyviruses, carlaviruses and allexiviruses in garlic in Sudan. Journal of Phytopathology 161:642-650. https://doi.org/10.1111/jph.12115
Murashige T, Skoog F (1962). A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiologia Plantarum 15:473-487. https://doi.org/10.1111/j.1399-3054.1962.tb08052.x
Nam M, Lee YH, Park CY, Lee MA, Bae YS, Lim S, Lee JH, Moon SJ, Lee SH (2015). Development of multiplex RT-PCR for simultaneous detection of garlic viruses and the incidence of garlic viral disease in garlic genetic resources. Plant Pathology Journal 31(1):90-96. https://doi.org/10.5423/PPJ.NT.10.2014.0114
Panattoni A, Luvisi A, Triolo E (2013). Review. Elimination of viruses in plants: twenty years of progress. Spanish Journal of Agricultural Research 11(1):173-188. https://doi.org/10.5424/sjar/2013111-3201
Paranno L, Afurian M, Pagliaccia D, Douhan G, Vidalakis G (2012). Characterization of viruses associated with garlic plants propagated from different reproductive tissues from Italy and other geographic regions. Phytopathologia Mediterranea 51(3):549-565. https://doi.org/10.14601/Phytopathol_Mediterr-10479
Prajapati MR, Manav A, Singh J, Kumar P, Kumar A, Kumar R, Prakash S, Baranwal VK (2022). Identification and Characterization of a garlic virus E genome in garlic (Allium sativum L.) using high-throughput sequencing from India. Plants 11(2):224. https://doi.org/10.3390/plants11020224
Pramesh D, Baranwal VK (2015). Production of virus-free garlic (Allium sativum L.) through meristem tip culture after solar or hot air treatment of cloves. Journal of Horticultural Sciences and Biotechnology 90(2):160-186. https://doi.org/10.1080/14620316.2015.11513170
Sala-Rejczak K, Chodorska M, Nowak P, Paduch-Cichal E, Szyndel MS, Latocha P (2012). Occurrence of garlic and actinidia viruses in Poland. Journal of Agricultural Sciences 5:101-104. http://dx.doi.org/10.4454/JPP.V95I4SUP.038
Shahid MS, SattarMN, Iqbal Z, Raza A, Al-Sadi AM (2021). Next-generation sequencing and the CRISPR-Cas Nexus: A molecular plant virology perspective. Frontiers in Microbiology 11:609376. https://doi.org/10.3389/fmicb.2020.609376
Singh J, Singh MK, Ranjan K, Kumar A, Kumar P, Sirohi A, Baranwal VK (2020). First complete genome sequence of garlic virus X infecting Allium sativum-G282 from India. Genomics 112(2):1861-1865. https://doi.org/10.1016/j.ygeno.2019.10.020
Smékalová K, Stavlíková H, Dusek K (2010). Distribution of viruses in the garlic germplasm collection of the Czech Republic. Journal of Plant Pathology 92(1):273-274.
Taglienti A, Tiberini A, Manglli A, Rea R, Paoletti S, Taviani P, Tomassoli L (2018). Molecular identification of allexiviruses in a complex mixture of garlic viruses in Latium (central Italy). European Journal of Plant Pathology 150:797-801. https://doi.org/10.1007/s10658-017-1315-5
Tsuneyoshi T, Matsumi T, Natsuaki KT, Sumi S (1998). Nucleotide sequence analysis of virus isolates indicates the presence of three potyvirus species in Allium plants. Archives of Virology 143:97-113. https://doi.org/10.1007/s007050050271
Van Dijk P (1993). Survey and characterization of potyviruses and their strains of Allium species. Netherlands Journal of Plant Pathology 99(2):1-48.
Van Dijk P (1993). Carlavirus isolates from cultivated Allium species represent three viruses. Netherlands Journal of Plant Pathology 99:233-257.
Verhoyen M, Horvat F (1973). La striure chloritique du porreau. 1. Identification de l’agent causal. [The chlorotic streak of leek. 1. Identification of the causal agent]. Parasitica 29:16-28.
Walkey DGA (1990). Virus diseases. In: Rabinowich HD, Brewster JL (Eds). Onions and Allied Crops. Vol. 2, CRC Press Inc., Boca Raton, Florida, USA. pp. 191-212.
Yang X, Li Y, Wang A (2021). Research advances in potyviruses: from the laboratory bench to the field. Annual Review of Phytopathology 59:1-29. https://doi.org/10.1146/annurev-phyto-020620-114550
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