Preferred name: Cucurbit yellow stunting disorder virus
Taxonomic position: Viruses and viroids: Riboviria: Orthornavirae: Kitrinoviricota: Alsuviricetes: Martellivirales: Closteroviridae: Crinivirus
Other scientific names: CYSDV, Cucurbit yellow stunting disorder closterovirus, Cucurbit yellow stunting disorder crinivirus
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Notes on taxonomy and nomenclature EPPO Categorization: A2 list
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EPPO Code: CYSDV0

Economic hosts of CYSDV are mainly Cucurbitaceae: watermelon, melon, cucumber, courgette, pumpkin. In addition, a number of host plants in other families have been identified both in crops (e.g. lettuce, alfalfa, snap bean), and in weeds. For further details, see Abou-Jawdah et al. (2000); Berdiales et al. (1999); Célix et al. (1996); Desbiez et al. (2000); Kao et al. (2000); Louro et al. (2000); Wisler et al. (1998), Wintermantel et al. (2009), Orfanidou et al., 2019).

Host list: Amaranthus blitum, Amaranthus retroflexus, Bassia hyssopifolia, Chenopodium album, Citrullus lanatus, Cucumis melo, Cucumis sativus, Cucurbita foetidissima, Cucurbita maxima, Cucurbita pepo, Cucurbitaceae, Datura stramonium, Ecballium elaterium, Heliotropium europaeum, Lactuca sativa, Lysimachia foemina, Malva neglecta, Malva parviflora, Malvella leprosa, Medicago sativa, Phaseolus vulgaris, Physalis acutifolia, Sisymbrium irio, Sisymbrium sp., Solanum elaeagnifolium, Solanum nigrum, Solanum tuberosum, Sonchus oleraceus, Sonchus sp., Tribulus terrestris

CYSDV is present in several countries from the Mediterranean area, North America, Africa and Asia.

EPPO Region: Cyprus, Greece (mainland, Kriti), Israel, Italy (Sardegna), Jordan, Morocco, Portugal (mainland), Spain (mainland, Islas Canárias), Tunisia, Türkiye
Africa: Egypt, Morocco, Sudan, Tunisia
Asia: China (Jiangsu, Shanghai, Zhejiang), India (Uttar Pradesh), Iran, Iraq, Israel, Jordan, Lebanon, Saudi Arabia, Syria, United Arab Emirates
North America: Mexico, United States of America (Alabama, Arizona, California, Florida, Georgia, South Carolina, Texas)
Central America and Caribbean: Jamaica

The life cycle of CYSDV is strongly dependent on its vector, the whitefly Bemisia tabaci, also a regulated pest (EPPO, 2023). Adult insects acquire the virus by sucking on phloem sap, and can further transmit it to another plant when feeding. The virus does not circulate or replicate in the insect. The spread of the virus is believed to be related to the increase in distribution of the polyphagous cryptic B. tabaci species MEAM1 (Middle East Asia Minor 1 group, formally known as B biotype of B. tabaci, or B. argentifolii; Bellows et al. (1994) and MED (Mediterranean, formally known as B. tabaci biotype Q) (De Barro et al., 2011; Wisler et al., 1998; Berdiales et al., 1999).). MED possibly originated in the Iberian Peninsula, but has since spread globally (Horowitz et al., 2003; Chu et al., 2010).

Acquisition periods of 18 h or more and inoculation periods of 24 h or more are necessary for transmission rates of CYSDV of over 80% in tests using melon. However, transmission was noted after an acquisition and transmission periods of 2 h (Célix et al., 1996). CYSDV persists for at least 9 days in the vector with a 72.2-h half-life, which is the second-longest retention time of all whitefly-transmitted Closteroviridae (Martin et al., 2011; Wisler et al., 1998). CYSDV is not known to be seed-borne.

Symptoms

Cucumbers and melons affected by CYSDV show severe yellowing symptoms that start as an interveinal mottle on the older leaves and intensify as leaves age (Abou-Jawdah et al., 2000). Chlorotic leaf mottling and yellowing occur on cucumber and melon (Louro et al., 2000) and yellowing and severe stunting on melon (Kao et al., 2000). CYSDV on its own does not cause symptoms on courgette, but may cause additional symptoms in mixed infection with other viruses, such as CVYV (Gil-Salas et al., 2011)). Symptoms on cucumbers and melons are said to be indistinguishable from those caused by Beet pseudoyellows virus BPYV (Wisler et al., 1998) or by Cucurbit chlorotic yellows virus (CCYV) (Okuda et al., 2010). In experimental transmission experiments, chlorotic spots along the leaf veins of the melon cv. ‘Piel de Sapo’ were noticed after 14–20 days. Sometimes, initial symptoms also consisted of prominent yellowing sectors of a leaf. Symptoms evolved later to complete yellowing of the leaf lamina, except the veins, and rolling and brittleness of the leaves (Célix et al., 1996). Non-cucurbits hosts and weeds are often symptomless (Wintermantel et al., 2009; Orfanidou et al., 2019).

Morphology

Flexuous, filamentous virus particles with estimated lengths of 800–850 nm have been found in infected plants (Liu et al. ,2000). The virus has a bipartite positive sense single-stranded RNA genome with an RNA-1 containing 9126 nucleotides and an RNA-2 of 7281 nucleotides (Livieratos & Coutts, 2002; Aguilar et al., 2003; Coutts & Livieratos, 2003). The coat protein gene contains 756 nucleotides and encodes the coat protein of 28.5 kDa (Livieratos et al., 1999).

Detection and inspection methods

CYSDV can be detected in infected plants using conventional and real-time RT-PCR (Berdiales et al., 1999; Célix et al., 1996; Gil-Salas et al., 2012) and by dot–blot hybridization analysis using CYSDV-specific probes (Ruiz et al., 2002 ; Rubio et al., 1999; Tian et al., 1996). Antiserum has been produced and used in both immunoblot and indirect ELISA assays (Livieratos et al., 1999; Cotillon et al., 2005).

Plants for planting may be inspected as described in EPPO Standard PM 3/077 (EPPO, 2022).

Within cucurbit crops, natural spread of CYSDV occurs through its vector, B. tabaci. Adults of B. tabaci do not fly very efficiently but, once airborne, can be transported long distances in air currents, and thus represent the main pathway of local and natural dispersal. Internationally, infected young plants of cucurbits intended for planting are the most likely pathway to introduce or spread the disease (EFSA, 2013). Viruliferous (infected) adult stages of B. tabaci can be carried on traded plant materials but they are not likely to remain viruliferous long enough to constitute a significant pathway for long-distance movement if the plants are not infested (EFSA, 2013; Pasquali et al., 2015). CYSDV is not known to be seed-borne.

Economic impact

CYSDV has been associated with yellowing diseases transmitted by whiteflies in cucumbers and melons grown in 16 000 ha of polyethylene-covered glasshouses in South-East Spain, ever since the early 1990s. The disease led to an approximate yield reduction of 30–50 % in Spain and Lebanon (Célix et al., 1996; Hourani and Abou-Jawdah, 2003). In Arizona, the outbreak of CYSDV in 2006 caused an estimated 60 % reduction in marketable melon yield and a subsequent USD 18 million loss (McGinley, 2008; EFSA, 2018). In Greece and Cyprus, CYSDV has become the most prevalent virus on cucurbits (Orfanidou et al., 2019) replacing Beet pseudo-yellows virus (BPYV).

Control

The control of CYSDV centres on the control of its vector B. tabaci, and elimination of sources of infection. In particular, cucurbit seedlings for planting should come from disease-free stocks.

Cultural control: roguing infected cucurbit plants and removing overwintering crops early in the spring prior to the emergence of adult whiteflies may prove useful. To be effective, this sort of control measure should be applied over a whole area and preferably where there is no continuous production in glasshouses, which are often the sites of whitefly activity and active virus spread throughout the year. Weeds in and surrounding glasshouses should also be destroyed as they could act as hosts for B. tabaci. In Israel, covering the soil with a mulch of sawdust, fresh wheat straw or yellow polyethylene sheets has markedly reduced populations of B. tabaci. Whiteflies are attracted to the yellow colour and are killed by the heat. The fading of the mulch colour and changes in the ratio of canopy to mulch area is believed to cause a reduction in control. Interplanting with a species that is a good host for the vector, but not the virus may reduce virus incidence. In Lebanon and Spain, insect-proof nets and sticky yellow traps are used for control (Abou-Jawdah et al., 2000; Janssen et al., 2009). Growing plants under physical barriers, such as low mesh tunnels and shade-cloth, may also have a positive effect.

Chemical control of populations of B. tabaci to levels that result in a significant drop in disease incidence has proved difficult. In general, chemical control of the vectors of Closteroviridae has not been effective in preventing the spread of the diseases they cause (Berdiales et al., 1999). Some of the difficulties are the wide host range of the vector, the presence of the whitefly on the undersides of leaves, the extreme motility of adults and the ability of B. tabaci to develop resistance to most classes of existing insecticides (EPPO, 2023, Horowitz et al., 2020).

Biological control: The predator Amblyseius swirskii, the parasite Encarsia formosa and the fungus Verticillium lecanii can be used as biological agents against B. tabaci, but are unlikely to directly affect virus transmission. A. swirskii does not prevent the primary infection from whitefly-transmitted tomato leaf curl New Delhi virus in courgette but it can reduce the reproduction of the vector and the secondary viral spread within crops so this could apply as well to other whitefly-transmitted viruses such as CYSDV (Tellez et al. 2017 cited in CABI, 2023).

Several commercial cucumber varieties show intermediate resistance to CYSDV, and provided efficient virus control especially when combined with the use of insect-proof nets (Janssen et al., 2003). To date there are no resistant commercial melon varieties available, but partially resistant genotypes have been identified (Sese et al., 1999; Marco et al., 2003; Martin and Pico, 2021).

Phytosanitary risk

Cucurbits are important crops in the EPPO region, both in the field and under glass, and CYSDV causes a serious disease notably on cucumbers and melons in Greece, Spain, Portugal, Türkiye and the Middle East. Within Europe, cucurbit production is significant; in 2021, 6.14 million tonnes of cucumber and gherkin harvested in the EU. Spain and the Netherlands were the biggest producers, harvesting 746 000 and 440 000 tonnes, respectively, according to FAO. Economic losses from CYSDV that could be expected in glasshouse-grown cucurbits, especially cucumber, in Northern Europe are difficult to predict, but are likely to be substantial. Spread of the pest is likely to be much facilitated by the presence of its vector B. tabaci in glasshouses in many countries of the EPPO region. Control of CYSDV is especially difficult when the virus is transmitted by insecticide-resistant B. tabaci whiteflies. A breakdown of efficacy of insecticides could result in serious problems. There is a strong probability that CYSDV will become a serious threat to host crops in other Mediterranean countries and in Northern Europe, if introduced. In this case, commercial varieties of intermediate resistance to CYSDV can limit possible losses in cucumber.

International trade in young host plants for planting seems the main pathway. Seedlings should be protected from infection before entering trade. Visual inspections of export material may not detect the virus since it is asymptomatic in some hosts and may take some time to express symptoms in others. Suitable measures for host plants for planting from areas where CYSDV occurs are as follows: crop or place of production freedom from the virus and exclusion of the vector B. tabaci.

Abou-Jawdah Y, Sobh H, Fayad A, Lecoq H, Delécolle B & Trad-Ferré J (2000) Cucurbit yellow stunting disorder virus – a new threat to cucurbits in Lebanon. Journal of Plant Pathology 82, 55–60.

Aguilar JM, Franco M, Marco CF, Berdiales B, Rodriguez-Cerezo E, Truniger V & Aranda MA (2003) Further variability within the genus Crinivirus, as revealed by determination of the complete RNA genome sequence of Cucurbit yellow stunting disorder virus. Journal of General Virology 84, 2555-2564.

Bellows TS, Perring TM, Gill RJ & Headrick DH (1994) Description of a species of Bemisia. Annals of the Entomological Society of America 87, 195–206.

Berdiales B, Bernal JJ, Sáez E, Woudt B, Beitia F & Rodríguez-Cerezo E (1999) Occurrence of cucurbit yellow stunting disorder virus (CYSDV) and beet pseudo-yellows virus in cucurbit crops in Spain and transmission of CYSDV by two biotypes of Bemisia tabaci. European Journal of Plant Pathology 105, 211–215.

Célix A, López-Sesé A, Almarza N, Gómez-Guillamón ML & Rodríguez-Cerezo E (1996) Characterization of cucurbit yellow stunting disorder virus, a Bemisia tabaci-transmitted closterovirus. Phytopathology 86, 1370–1376.

Cotillon AC, Desbiez C, Bouyer S, Wipf‐Scheibel C, Gros C, Delécolle B & Lecoq H (2005) Production of a polyclonal antiserum against the coat protein of Cucurbit yellow stunting disorder crinivirus expressed in Escherichia coli. EPPO Bulletin 35, 99-103.

Coutts RHA & Livieratos IC (2003) Nucleotide sequence and genome organization of Cucurbit yellow stunting disorder virus RNA1. Archives of Virology 148, 2055-2062.

De Barro PJ, Liu SS, Boykin LM & Dinsdale AB (2011) Bemisia tabaci: a statement of species status. Annual Review of Entomology 56, 1-19.

Desbiez C, Lecoq H, Aboulama S & Peterschmitt M (2000) First report of Cucurbit yellow stunting disorder virus in Morocco. Plant Disease 84, 596.

EFSA Panel on Plant Health (2013) Scientific Opinion on the risks to plant health posed by Bemisia tabaci species complex and viruses it transmits for the EU territory. EFSA Journal 11(4), 3162. [302 pp.] https://doi.org/10.2903/j.efsa.2013.3162.

EPPO (2023) Bemisia tabaci. EPPO datasheets on pests recommended for regulation. https://gd.eppo.int/taxon/BEMITA/datasheet (accessed 2023-06-09).

EPPO (2022) EPPO Standard PM3/077(2) Vegetable plants for planting under protected conditions – inspection of places of production. EPPO Bulletin 52(3), 526-543. https://doi.org/10.1111/epp.12888

Gil-Salas FM, Peters J, Boonham N, Cuadrado IM, Janssen D (2011) Yellowing disease in zucchini squash produced by mixed infections of Cucurbit yellow stunting disorder virus and Cucumber vein yellowing virus. Phytopathology 101(11), 1365-1372. https://doi.org/10.1094/PHYTO-12-10-0343

Gil‐Salas FM, Peters J, Boonham N, Cuadrado IM & Janssen D (2012) Co‐infection with Cucumber vein yellowing virus and Cucurbit yellow stunting disorder virus leading to synergism in cucumber. Plant Pathology 61, 468-478. https://doi.org/10.1111/j.1365-3059.2011.02545.x

Hassan AA & Duffus JE (1991) A review of a yellowing stunting disorder of cucurbits in the United Arab Emirates. Emirates Journal of Agricultural Science 2, 1–16.

Horowitz AR, Denholm I, Gorman K, Cenis JL, Kontsedalov S & Ishaaya I (2003) Biotype Q of Bemisia tabaci identified in Israel. Phytoparasitica 31, 94–98.

Horowitz AR, Ghanim M, Roditakis E, Nauen R &Ishaaya I (2020) Insecticide resistance and its management in Bemisia tabaci species. Journal of Pest Science 93, 893-910

Hourani H & Abou-Jawdah Y (2003) Immunodiagnosis of Cucurbit yellow stunting disorder virus using polyclonal antibodies developed against recombinant coat protein. Journal of Plant Pathology 85, 197–204.

Chu D, Wan FH, Zhang YJ & Brown JK (2010) Change in the biotype composition of Bemisia tabaci in Shandong Province of China from 2005 to 2008. Environmental Entomology 39, 1028–1036.

Janssen D, García MC, Belmonte A, Pascual F, García T, Bretones G, Gil FM & Cuadrado IM (2009) Integrated pest control using indoor screenhouses within plastic greenhouses. IOBC/wprs Bulletin 49, 79-84.

Janssen D, Ruiz L, Cano M, Belmonte A, Martin G, Segundo E & Cuadrado IM (2003) Physical and genetic control of Bemisia tabaci-transmitted Cucurbit yellow stunting disorder virus and Cucumber vein yellowing virus in cucumber. IOBC/WPRS Bulletin 26, 101-106.

Kao J, Jia L, Tian T, Rubio L & Falk BW (2000) First report of Cucurbit yellow stunting disorder virus (genus Crinivirus) in North America. Plant Disease 84, 101.

Liu HY, Wisler GC & Duffus JE (2000) Particle lengths of whitefly-transmitted criniviruses. Plant Disease 84, 803–805.

Livieratos IC & Coutts RHA (2002). Nucleotide sequence and phylogenetic analysis of Cucurbit yellow stunting disorder virus RNA 2. Virus Genes 24, 225-230.

Livieratos IC, Avgelis AD & Coutts RHA (1999) Molecular characterization of the cucurbit yellow stunting disorder virus coat protein. Phytopathology 89, 1050–1055.

Louro D, Vicente M, Vaira AM, Accotto GP & Nolasco G (2000) Cucurbit yellow stunting disorder virus (Genus Crinivirus) associated with the yellowing disease of cucurbit crops in Portugal. Plant Disease 84, 1156.

Marco CF, Aguilar JM, Abad J, Gomez-Guillamon ML & Aranda MA (2003) Melon resistance to Cucurbit yellow stunting disorder virus is characterized by reduced virus accumulation. Phytopathology 93, 844-852.

Martín G, Cuadrado I M & Janssen D (2011) Bean yellow disorder virus: parameters of transmission by Bemisia tabaci and host plant range. Insect Science 18, 50-56.

Martín-Hernández AM & Picó B (2021) Natural resistances to viruses in cucurbits. Agronomy 11, 23. https://doi.org/10.3390/agronomy11010023

McGinley S (2008) Fighting a melon virus in Yuma County: a cooperative program with growers. Agricultural Experiment Station Research Report, 10-11.

Orfanidou CG, Papayiannis LC, Pappi PG, Katis NI, Maliogka VI (2019) Criniviruses associated with cucurbit yellows disease in Greece and Cyprus: an ever-changing scene. Plant Pathology 68(4), 764-774.

Okuda M, Okazaki S, Yamasaki S, Okuda S & Sugiyama M (2010) Host range and complete genome sequence of Cucurbit chlorotic yellows virus, a new member of the genus Crinivirus. Phytopathology 100, 560-566.

Pasquali S, Gilioli G, Janssen D, Winter S. (2015) Optimal strategies for interception, detection, and eradication in plant biosecurity. Risk Analysis 35(9), 1663-1673.

Rubio L, Soong J, Kao J & Falk BW (1999) Geographic distribution and molecular variation of isolates of three whitefly-borne closteroviruses of cucurbits: lettuce infectious yellows virus, cucurbit yellow stunting disorder virus, and beet pseudo-yellows virus. Phytopathology 89, 707–711.

Rubio L, Abou-Jawdah Y, Lin H & Falk BW (2001) Geographically distant isolates of the crinivirus Cucurbit yellow stunting disorder virus show very low genetic diversity in the coat protein gene. Journal of General Virology 82, 929–933.

Ruiz L, Janssen D, Velasco L, Segundo E & Cuadrado IM (2002) Quantitation of cucurbit yellow stunting disorder virus in Bemisia tabaci (Genn.) using digoxigenin-labelled hybridisation probes. Journal of virological methods 101, 95-103.

Sesé AIL, Sánchez F & Gómez-Guillamón ML (1999) Evaluation of melon F hybrids resistant to cucurbit yellowing stunting disorder virus (CYSDV). Acta Horticulturae 492, 341-347.

Tellez MM, Simon A, Rodriguez E & Janssen D (2017) Control of Tomato leaf curl New Delhi virus in zucchini using the predatory mite Amblyseius swirskii. Biological Control 114, 106–113.

Tian T, Klaassen VA, Soong J, Wisler G, Duffus JE & Falk BW (1996) Generation of cDNAs specific to lettuce infectious yellows closterovirus and other whitefly-transmitted viruses by RT-PCR and degenerate oligonucleotide primers corresponding to the closterovirus gene encoding the heat shock protein 70 homolog. Phytopathology 86, 1167–1173.

Yakoubi S, Desbiez C, Fakhfakh H, Wipf-Scheibel C, Marrakchi M & Lecoq H (2007) Occurrence of Cucurbit yellows stunting disorder virus and Cucumber vein yellowing virus in Tunisia. Journal of Plant Pathology 89, 417-420.

Wintermantel WM, Hladky LL, Cortez AA, Natwick ET (2009) A new expanded host range of Cucurbit yellow stunting disorder virus includes three agricultural crops. Plant Disease 93(7), 685-690.

Wisler GC, Duffus JE, Liu HY & Li RH (1998) Ecology and epidemiology of whitefly-transmitted closteroviruses. Plant Disease 82, 270–280.

CABI resources used when preparing this datasheet

CABI (2023) Datasheet on Cucurbit yellow stunting disorder virus, Online https://doi.org/10.1079/cabicompendium.17070

This datasheet was extensively revised in 2023 by Dirk Janssen, IFAPA, ES. His valuable contribution is gratefully acknowledged.

EPPO (2024) Cucurbit yellow stunting disorder virus. EPPO datasheets on pests recommended for regulation. https://gd.eppo.int (accessed 2024-04-28)

This datasheet was first published in the EPPO Bulletin in 2005 and revised in 2023. It is now maintained in an electronic format in the EPPO Global Database. The sections on 'Identity', ‘Hosts’, and 'Geographical distribution' are automatically updated from the database. For other sections, the date of last revision is indicated on the right.

EPPO (2005) Data sheets on quarantine pests. Cucurbit yellow stunting disorder crinivirus. EPPO Bulletin 35(3), 442–444. https://doi.org/10.1111/j.1365-2338.2005.00847.x