Cucurbit Yellow Stunting Disorder Virus

Taxonomy: Closteroviridae, Crinivirus, Cucurbit yellow stunting disorder virus

The most up-to-date and complete virus taxonomy is available on the International Committee on Taxonomy of Viruses webpage.

Cucurbit yellow stunting disorder virus (CYSDV) causes yellowing of leaves and can lead to substantial reductions in yield for cucurbit production (López-Sesé, A. I. and Gómez-Guillamón, 2000, HortScience 35). The virus was first identified in Saudi Arabia in 1989 (Hassan and Duffus, 1991, Emir. J. Food Agric. 2) and subsequently spread throughout the Middle East and Mediterranean regions (Wintermantel et al., 2017, Virus Res. 241). CYSDV was first identified in the United States (Texas) in 1999 (Kao et al., 2000, Plant Dis. 84) and emerged with widespread infestation of the southwestern desert production regions of California and Arizona in 2006 (Kuo et al., 2007, Plant Dis. 91; Brown et al., 2007, Plant Dis. 91). CYSDV has since spread among many United States cucurbit production regions where its vector, the sweetpotato whitefly (Bemisia tabaci) is present (Wintermantel et al., 2017).

Symptoms

Symptoms of CYSDV infection do not develop until approximately three weeks after infection. On cucurbit leaves, symptoms usually begin as chlorotic (yellow) spots and rapidly develop into a chlorotic mottle (Figures 1 and 2). As symptoms advance, the chlorotic spots coalesce, developing into interveinal chlorosis (yellowing between veins, Figure 3). Symptoms initially appear on older leaves near the crown of the plant (Figure 4) and spread gradually toward younger growth; younger leaves generally remain green until late in disease development. These symptoms are typical on melon, cucumber, squash, and watermelon plants. Early infection of cucumber, melon, and watermelon plants by CYSDV results in reduced yields. Fruit number and weight are reduced in infected plants (López-Sesé, A. I. and Gómez-Guillamón, 2000).

Figure 1. Chlorotic mottle symptoms on a melon leaf caused by cucurbit yellow stunting disorder virus (CYSDV). Leaf spotting and mottle symptoms are the first symptoms observed on cucurbit leaves infected with CYSDV; chlorotic areas eventually coalesce into interveinal yellowing. Credit: W. M. Wintermantel, USDA-ARS.

Figure 2. Early chlorotic mottle symptoms on a watermelon leaf caused by cucurbit yellow stunting disorder virus (CYSDV). Leaf spotting and mottle symptoms are the first symptoms observed on cucurbit leaves infected with CYSDV; chlorotic areas eventually coalesce into interveinal yellowing. Credit: W. M. Wintermantel, USDA-ARS.

Figure 3. Interveinal yellowing on melon leaves infected with cucurbit yellow stunting disorder virus (CYSDV) and cucurbit chlorotic yellows virus (CCYV). Interveinal yellowing is a common symptom of infection by CYSDV as well as the closely related CCYV. Major veins typically remain green until late in symptom development, whereas interveinal areas become chlorotic. Credit: W. M. Wintermantel, USDA-ARS.

Figure 4. Yellowing symptoms caused by cucurbit yellow stunting disorder virus (CYSDV) begin on leaves near the crown and gradually spread outward down vines. New growth typically remains green until late in symptom development at which point all leaves can become yellow. Credit: W. M. Wintermantel, USDA-ARS.

Symptoms of CYSDV infection may be confused with symptoms caused by some other viruses, including the criniviruses, cucurbit chlorotic yellows virus (CCYV) and beet pseudoyellows virus (BPYV), as well as the polerovirus, cucurbit aphid-borne yellows virus (CABYV). Symptoms of CYSDV infection may also be confused with those caused by various nutritional deficiencies or by those associated with other diseases, such as cucurbit yellow vine disease and downy mildew.

Epidemiology & Spread

CYSDV is known to be transmitted by two cryptic species of Bemisia tabaci (sweetpotato whitefly), MEAM1 (Figure 5) and MED (formerly biotypes B and Q, respectively) that are widely prevalent in cucurbit production regions throughout the world. Many other B. tabaci cryptic species exist but have not been evaluated extensively for their ability to transmit CYSDV. Virus transmission occurs in a semipersistent manner (Célix et al., 1996, Phytopathol. 86), which means that viruliferous whiteflies (whiteflies carrying CYSDV) can acquire the virus over short feeding periods (minutes to hours) and transmit it for a limited period of time (hours to days); B. tabaci MEAM1 can acquire CYSDV during feeding periods as short as one hour and can transmit for seven to nine days if removed from an infection source. Longer feeding periods lead to more efficient virus acquisition and transmission by whiteflies (Célix et al., 1996; Wisler and Duffus, 2001, Virus-Insect-Plant Interactions), and transmission efficiency declines the longer the whiteflies are removed from virus source plants.

During the three-week period following infection and before symptom development, CYSDV gradually accumulates in plants. Symptomless, infected plants placed in production settings may then inadvertently serve as a virus source and contribute to virus introduction and spread.

Figure 5. Adult sweetpotato whiteflies (Bemisia tabaci) feeding on the underside of melon leaves. In moderate to heavy infestations, whiteflies can most easily be observed on the underside of leaves in the early morning before temperatures increase. When leaves are disturbed, they often fly away from the leaves and may be visible as “clouds” above the crop canopy. Credit: W. Wintermantel, USDA-ARS.

CYSDV, like other criniviruses, cannot be transmitted through seed or by mechanical means. CYSDV can infect all commonly cultivated cucurbit plants, including cucumber, melon, pumpkin, squash, bottle gourd, and watermelon (Célix et al., 2006). Losses from CYSDV result from reduced plant vigor and an associated loss of fruit number and weight (López-Sesé and Gómez-Guillamón, 2000). In Spain and Lebanon, losses of 30-50% have been observed in melon (Célix et al., 1996; Hourani and Abou-Jawdah, 2003); in the southwestern United States, even greater losses (80%) were observed in fall melons when plants were infected early in the season (Brown et al., 2007).

The virus often occurs in mixed infections with other viruses, particularly those transmitted by the same whitefly vector (Kavalappara et al., 2021, Viruses 13; Mondal et al., 2023, Plant Dis. 107). Mixed infections can be difficult to identify because other viruses, such as CCYV or CABYV, can produce nearly identical symptoms on cucurbit plants. Therefore, appropriate diagnostic methods are required to determine which viruses may be present. In melon production regions of the southwestern and southeastern United States, CYSDV regularly occurs in mixed infections with CCYV as well as other viruses. CYSDV exhibits seasonal differences in prevalence with CCYV in southwestern United States melon production areas; CYSDV is the predominant virus causing yellowing during the fall, whereas CCYV is the primary virus causing yellowing during the spring and early summer (Mondal et al., 2023).

Although several plant species within the Cucurbitaceae family can become infected by CYSDV, many do not develop visible symptoms. Numerous non-cucurbit hosts of CYSDV have been identified, including many common weeds and some agricultural crops; some of these hosts are better sources for whitefly acquisition of the virus than others (Wintermantel et al., 2009; Wintermantel et al., 2016, Plant Dis. 100; Wintermantel et al., 2017). These non-cucurbit host plants provide a reservoir from which whiteflies can acquire CYSDV and then transmit it into cucurbit crops.

Geographic Incidence

Since its initial detection in Saudi Arabia in 1989, CYSDV has been identified in many parts of the world where it occurs in association with B. tabaci MEAM1 or MED.

United States: Texas, (1999), Arizona (2006), California (2006), Florida (2007), Georgia (2016), South Carolina (2019), Alabama (2022).

Africa: Egypt (2004), Morocco (2004), Tunisia (2007), Sudan (2022).

Asia: Israel (2004), Jordan (2004), Lebanon (2004), Saudi Arabia (2004), Turkey (2004), Iran (2005), China (2010), South Korea (2016), India (2021).

Europe: Greece (2004) including Crete (2022), Portugal (2004), Spain (2004) including Canary Islands (2004), Cyprus (2005), Italy (2016) including Sardinia (2022).

Note: Years in parentheses indicate when CYSDV was first identified in that location.

For the most up to date information on geographic incidence, please visit this website (www.eCucurbitviruses.org) or CAB International’s Invasive Species Compendium (www.cabi.org/isc/).

Detection/Diagnosis

Symptoms alone cannot be used to accurately diagnose CYSDV infection. Diagnosis requires molecular or serological protocols that are commonly used in many research and diagnostic laboratories.

Currently, protocols are established for molecular assays including RT-PCR (reverse transcription polymerase chain reaction; Célix et al., 1996; Berdiales et al., 1999, Eur. J. Plant Pathol. 105; Wintermantel and Hladky, 2010, J. Virol. Methods 170; Gil-Salas, et al., 2007, J. Virol. Method. 146), quantitative RT-PCR (Papayiannis et al., 2010, J. Phytopathol. 158; Abrahamian et al., 2013, J. Virol. Methods 193; Jailani et al., 2021, Physiol. Mol. Plant Pathol. 116, Mondal et al., 2023), and dot-blot hybridization (Tian et al, 1996, Phytopathol. 86; Rubio et al., 1999, Phytopathol. 89; Ruiz et al., 2002, J. Virol. Methods 101). Serological protocols, including DAS-ELISA (double antibody sandwich enzyme-linked immunosorbent assay) and tissue blot immunoassays, are also available for use in detecting CYSDV in plant samples (Hourani and Abou-Jawdah, 2003, J. Plant Pathol. 85; Cotillon et al., 2005, EPPO Bulletin 35); however, high-quality, commercially available antiserum is limited for CYSDV. When choosing an assay, keep in mind that sensitivity of serological assays is much lower than that of molecular assays, and cross reactivity with related viruses can occur when using some sources of antisera.

Contact your local plant diagnostic laboratory to determine testing capabilities.

Visit the Diagnostics Page for more information on diagnostic laboratories in your state, protocol publications, and/or the References page for references describing appropriate CYSDV detection methods.

Management

Genes for resistance to CYSDV have been identified in melon (Cucumis melo) (López-Sesé and Gómez-Guillamón, 2000; McCreight and Wintermantel, 2011, HortScience 46; McCreight et al., 2017, Acta Hort. 1151; Pérez-de-Castro et al., 2020, Int. J. Mol Sci. 21; Tamang et al., 2019, HortScience 56), and this resistance is being bred into commercial melon varieties. A source of resistance has also been identified in cucumber (Janssen et al., 2003, IOBC/WPRS Bulletin 26; Eid et al., 2006, Plant Dis. 90).

With limited availability of resistance to CYSDV, management efforts focus on avoidance of virus source plants and vector populations (Carrière et al., 2014, J. Econ. Entomol. 107; Carrière et al., 2017, J. Econ. Entomol. 110). This requires a comprehensive approach that includes establishment of non-infected plants, suppression and avoidance of whitefly vector populations, and management of known and potentially infected hosts (Carrière et al., 2017).

Begin with virus-free transplants.

If transplants are used, it is important that seedling are inspected to be sure that transplants are free of virus symptoms and whitefly eggs, nymphs, and adults. When possible, avoid importing transplants from areas with a known presence of CYSDV or other whitefly-transmitted viruses as this can lead to accidental introduction of the virus to new areas.

Apply insecticides to transplants prior to transplanting.

Insecticide treatment of seedlings one to three days prior to transplanting can reduce infection by whitefly-transmitted viruses when transplanting into areas with elevated virus and whitefly incidence (Okuda and Wintermantel, 2017).

Use reflective mulch.

Planting into reflective silver plastic mulches can be effective in repelling whiteflies, particularly when plants are small (La Tora et al., 2022, Horticulturae 8).

Apply row covers to young plants.

An additional measure for field cucurbits can include the application of row covers—covering young plants with whitefly-proof mesh to exclude whiteflies while plants are young (La Tora et al., 2022).

Apply insecticides to manage whiteflies in production areas.

It is important to limit whitefly populations in fields and greenhouses. Limiting the presence of whiteflies is important as sweetpotato whitefly feeding can kill young plants, as well as cause silvering on leaves of squash or pumpkin plants (Figure 6). If whitefly populations remain low or can be suppressed throughout the season, introduction of CYSDV to crops can be limited or infections may develop late enough that yield impacts are marginal. Consult with guidelines for your production region to determine appropriate materials available for whitefly suppression.

Figure 6. Silvering of zucchini leaves caused by feeding of sweetpotato whiteflies (Bemisia tabaci). Credit: R. A. Melanson, MSU Extension, Bugwood.org.

Survey established fields for whiteflies prior to destruction/removal to determine if treatment is necessary.

Established cucurbit or other agricultural crop fields may serve as hosts to large populations of whiteflies and/or CYSDV. Removal of these fields may cause whiteflies to move to newly established or younger cucurbit plantings. Fields with whiteflies should be treated before destruction/removal or planting of new fields to suppress whitefly populations. This will reduce the potential for whiteflies to move to new fields or host plants in the area and may also reduce virus infections in the new plantings; this is particularly true if the established fields had known infections of CYSDV or other whitefly-transmitted viruses.

Remove virus and vector host plants near cucurbit fields.

In addition to suppression of whitefly populations, it is important to limit the presence of alternate hosts, particularly weeds and other crop plants known to be reservoirs of CYSDV from which whiteflies can acquire the virus and transmit it to cucurbit crops, such as alfalfa (Wintermantel et al., 2009, Plant Dis. 93; Wintermantel et al., 2016; Carrière et al., 2014, 2017). Removal of crops infected with CYSDV and infested with whitefly populations should precede planting of new crops to avoid whiteflies carrying virus from one crop to the next. Additionally, avoid planting near crops, such as cotton, that support large whitefly populations.

Resources

Wintermantel, W.M. 2017. Cucurbit yellow stunting disorder virus. In Keinath, A.P., Wintermantel, W.M., and Zitter, T.A. (eds.), Compendium of Cucurbit Diseases and Pests, 2^nd edition (pp. 123-125). American Phytopathological Society Press.

Visit the References page for a full reference list of cited articles.

Acknowledgement

This work is a publication of the Emerging Viruses in Cucurbits Working Group (EVCWG). It is supported by funding from the USDA NIFA (Agreement 2018-70006-28884) through the Southern IPM Center’s grant program project S22-026. Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the author(s) and the Emerging Viruses in Cucurbits Working Group and do not necessarily reflect the views of the USDA NIFA or the Southern IPM Center.

This publication may be distributed without alteration for nonprofit educational purposes provided that appropriate credit is given to the authors and the Emerging Viruses in Cucurbits Working Group. Permission for any other uses should be requested from the Emerging Viruses in Cucurbits Working Group.

EVCWG Publication 2303 (April 2023)

Author: William M. Wintermantel, USDA-ARS

Senior editor: Rebecca A. Melanson, Mississippi State University

Reviewers: Sudeep Bag, University of Georgia; John Palumbo, University of Arizona