Cucurbit yellow stunting disorder virus

Cucurbit yellow stunting disorder virus (CYSDV) is a crinivirus that is non-circulative, semi-persistently transmitted by the whitefly Bemisia tabaci. It multiplies in cucurbitaceous plant species but not inside its insect vector. The main pathways of CYSDV introduction and long-distance spread are through infected plants for planting. Short-distance spread is predominantly through viruliferous (infected) adults of B. tabaci. CYSDV is considered an 'emerging virus' and is increasingly recorded from a number of European, American and Asiatic countries. Infected cucurbit crops display yellowing symptoms on the leaves and this damage leads 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 US$ 18 million loss (McGinley, 2008; James, 2011). CYSDV was added to the EPPO A2 List in 2004.

Cucurbits are important crops in the field, under glass, and in plastic greenhouses in the European and Mediterranean region, and CYSDV causes a serious disease notably on cucumbers and melons in Spain, Portugal, Turkey and the Middle East. Within the EU, 1,76 million t of melon were harvested during 2017, led by Spain and Italy, with 656,000 and 606,000 t, respectively. Cucumber and gherkin production in the EU is more significant and in 2017, 2.82 million t were harvested. Spain, Poland and the Netherlands were the biggest producers, harvesting 635,000, 544,000 and 400,000 t, 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 Bemisia tabaci in glasshouses in many countries of the European and Mediterranean region. Control of CYSDV is difficult due to the ability of the vector B. tabaci rapidly to become resistant to insecticides. A breakdown of efficacy of insecticides could result in serious problems. There is a strong probability that CYSDV will become a serious problem in other Mediterranean countries and in northern Europe, if introduced.

The natural hosts of CYSDV are restricted to the Cucurbitaceae: watermelon, melon, cucumber and courgette. Wintermantel et al. (2009) also identified natural infections in snap bean, alfalfa and London rocket (Sisymbrium irio). In addition, the following experimental host plants have been identified: Cucurbita maxima and Lactuca sativa. For further details, see Célix et al. (1996), Wisler et al. (1998), Berdiales et al. (1999), Abou-Jawdah et al. (2000), Desbiez et al. (2000), Kao et al. (2000) and Louro et al. (2000).

The life cycle of CYSDV is strongly dependent on its vector, the whitefly Bemisia tabaci. In Portugal, the first symptoms of CYSDV in a field plot of cucumber were associated with heavy infestations of B. tabaci (Louro et al., 2000). High populations were also associated with symptoms on melon in the USA (Kao et al., 2000). The spread of the virus may be related to the increase in distribution of the polyphagous B. tabaci MEAM1 (B biotype) (Bellows et al., 1994). This moves readily from one host species to the next and is estimated to have a host range of around 600 species. Transmission of CYSDV by MEAM1 is greater than by biotype A (Wisler et al., 1998). However, MED (biotype Q) transmits as efficiently as MEAM1 (Berdiales et al., 1999).

Within the European and Mediterranean region, B. tabaci has been reported from most of the countries and in the cases where species identification was conducted, the two major invasive B. tabaci cryptic species, MEAM1 and MED, were almost exclusively found. In northern Europe, B. tabaci occurrence is in protected crop production systems only whereas in southern Europe it is present in greenhouses and in open fields. Except in the Mediterranean coastal region (Cyprus, Greece, Malta, Italy, south of France, certain parts of Spain and Portugal), B. tabaci occurrence is restricted to greenhouses (EFSA Panel on Plant Health, 2013). In some European countries, MED predominates and MEAM1 is almost absent, like in Spain (Simón et al., 2007), the mainland of Greece (Orfanidou et al., 2019) and France where MEAM1 has only been reported once occurring in a botanical garden in Nice (Dalmon et al., 2008). In contrast, MEAM1 is reported from Cyprus as the only species present (Orfanidou et al., 2019) while MED and MEAM1 have been found in determined Greek islands, such as Rhodes and Samos (Orfanidou et al., 2019), and in the warmer areas of Italy, including the southern regions (Sardinia and Sicily) and the north-western coast (Liguria) (Parrella et al., 2012).

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 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. This is the longest retention time of all whitefly-transmitted viruses of the Closteroviridae (Wisler et al., 1998).

General

• Research model

CYSDV in infected tissue can be identified by conventional and real-time RT-PCR detection assay (Célix et al., 1996; Berdiales et al., 1999; Gil-Salas et al., 2012) and by dot-blot hybridization analysis using CYSDV-specific probes (Tian et al., 1996; Rubio et al., 1999; Ruiz et al., 2002). Antiserum has been produced and used in both immunoblot and indirect ELISA assays (Livieratos et al., 1999; Desbiez et al., 2003; Cotillon et al., 2005).

Symptoms on cucurbit crops are very similar to those of Beet pseudoyellows virus (BPYV; Wisler et al., 1998).

Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.

Cultural Control and Sanitary Methods

The control of CYSDV is dependent on the control of its vector Bemisia tabaci, and elimination of sources of infection. In particular, cucurbit seedlings for planting should come from disease-free stocks. 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. Interplanting with a species that is a good host for the vector, but not the virus may reduce virus incidence. In Lebanon and in 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

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. Many conventional insecticides such as organophosphorus compounds, carbamates and pyrethroids have effectively reduced whitefly populations, but provided only partial virus control even when sprayed as frequently as 2-3 times a week (Nakhla and Maxwell, 1998). Imidacloprid, a systemic insecticide that can be applied to soil and foliage, is used to control whiteflies, but resistance has been reported (Elbert and Nauen, 2000). Insects resistant to buprofezin were also detected (Anon., 1996).

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 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 secondary viral spread within crops so this could apply to other whitefly-transmitted viruses such as CYSDV (Tellez et al., 2017).

Phytosanitary Measures

CYSDV was added to the EPPO A2 action list in 2004, and endangered EPPO member countries are thus recommended to regulate it as a quarantine pest. There are, as yet, no specific measures against CYSDV in Europe, and in particular there are no restrictions on the movement of cucurbit seedlings from areas where the disease occurs. There is a potential danger that infected seedlings could move from countries where CYSDV occurs to other parts of the region, thus spreading the virus. Possible measures would be the same as those proposed for Cucumber vein yellowing virus (CVYV; OEPP/EPPO, 2005a).

Host-Plant Resistance

Several commercial cucumber varieties show intermediate resistance to CYSDV, and can provide efficient virus control especially when combined with the use of insect-proof nets (Janssen et al., 2003). To date there are no commercial resistant melon varieties available, but preliminary attempts have been made to obtain select resistant genotypes (Sese et al., 1999; Marco et al., 2003).

29/08/20 Updated by:

Dirk Janssen, Instituto de Investigación y Formación Agraria y Pesquera (IFAPA), Seville, Spain