Taxonomy: Closteroviridae, Crinivirus, Cucurbit chlorotic yellows virus
The most up-to-date and complete virus taxonomy is available on the International Committee on Taxonomy of Viruses webpage.
Cucurbit chlorotic yellows virus (CCYV) is an important emerging virus of cucurbit crops, such as melon and watermelon, in the United States. It was first identified as a threat to cucurbit production in Japan during the early 2000s (Gyoutoku et al., 2009, Jpn. J. Phytopath. 75), and subsequently spread within eastern Asia, the Middle East, and parts of Africa over the next several years. CCYV was introduced into the southwestern U.S. in 2014 (Wintermantel et al., 2019, Plant Dis. 103) and has since spread among many U.S. production regions where the vector, the sweetpotato whitefly (Bemisia tabaci), is present. The virus has been shown to affect yield through reduced plant vigor and Brix (Peng and Huang, 2011, Phytopathol. 101(6S)).
Symptoms of CCYV infection do not develop until approximately three weeks after infection. On cucurbit plants, symptoms usually begin as chlorotic (yellow) spots and rapidly develop into a chlorotic mottle (Figure 1). As symptoms advance, the chlorotic spots coalesce, developing into interveinal chlorosis (chlorosis between veins) (Figure 2). Symptoms initially appear on older leaves near the crown of the plant (Figure 3) and spread gradually toward younger growth; younger leaves generally remain green until late in disease development. These symptoms are typical on cucumber, melon, squash, and watermelon plants. Early infection of cucumber, melon, and watermelon plants by CCYV results in reduced yields. Infection may also affect the quality of melons. Brix, a measure of the sugar content, has been shown to be reduced in fruits of infected melon and watermelon plants.
Symptoms of CCYV infection may be confused with symptoms caused by some other viruses, including the criniviruses cucurbit yellow stunting disorder virus (CYSDV) and beet pseudoyellows virus (BPYV) as well as the polerovirus cucurbit aphid-borne yellows virus (CABYV). Symptoms of CCYV 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, downy mildew, and Fusarium wilt.
CCYV is known to be transmitted by two cryptic species of Bemisia tabaci (sweetpotato whitefly), MEAM1 (Figures 4 and 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 CCYV.
CCYV transmission occurs in a semipersistent manner (Gyoutoku et al., 2009; Li et al., 2016, Sci Rep 6), which means that viruliferous whiteflies (whiteflies carrying CCYV) 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 MED can acquire CCYV during feeding periods as short as one hour and can transmit for 11 to 14 days if removed from an infection source. Longer feeding periods lead to more efficient virus acquisition by whiteflies (Li et al., 2016), and transmission efficiency declines the longer the whiteflies are removed from the source. CCYV, like other criniviruses, cannot be transmitted through seed or by mechanical means.
During the three-week period following infection and before symptom development, CCYV 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.
CCYV is known to infect a wide range of cucurbit plants, including cucumber, melon, pumpkin, squash, bottle gourd, and watermelon (Okuda et al., 2010, Phytopathol. 6; Orfanidou et al., 2017, Plant Dis. 101). Although several plant species within the Cucurbitaceae family can become infected by CCYV, not all develop visible symptoms. Numerous non-cucurbit hosts, including many common weeds and some agricultural crops, have been identified (Okuda et al. 2010; Orfanidou et al. 2017); some are better sources for whitefly acquisition of CCYV than others. Additional host plant species may exist. The role these non-cucurbit hosts play in virus epidemics is not well established and may vary by region and whitefly feeding preference. Additionally, some plant species that are not hosts of CCYV may contribute to epidemics by serving as important hosts for whitefly reproduction as increases in whitefly populations can lead to increases in virus transmission.
CCYV may be present in plants as a single-virus infection, but it is often found in mixed infections with other viruses, especially those transmitted by the sweetpotato whitefly, including CYSDV and squash vein yellowing virus (SqVYV) Abrahamian et al., 2013, J. Virol. Methods 193; Jailani et al., 2021, Physiol. Mol. Plant Pathol. 116; Mondal et al., 2023, Plant Dis. accepted; Mondal et al. 2022, Plant Dis. 106). It has also commonly been found in mixed infections with CABYV (Mondal et al., 2021, Plant Dis. 105; Mondal et al., 2023, Plant Dis. accepted). It is not possible to determine from symptoms if one or more viruses are present in a plant; molecular diagnostics are needed to determine if a mixed infection is present and which viruses are present in the infection.
Since its initial detection in Japan in 2004, CCYV has been identified in many parts of the world where it occurs in association with the sweetpotato whitefly (B. tabaci MEAM1 or MED):
United States: California (2014), Alabama (2020), Florida (2020), Georgia (2020), Texas (2020).
Africa: Sudan (2009), Egypt (2015), Algeria (2018).
Asia: Japan (2004), China (2007), Taiwan (2009), Iran (2011), Lebanon (2011), Saudi Arabia (2014), Jordan (2017), Turkey (2017), South Korea (2018), Sri Lanka (2018), Israel (2019), India (2021), the Philippines (2021).
Europe: Greece (2011), Spain (2018), Cyprus (2019).
Note: Years in parentheses indicate when CCYV was first identified in that location.
For the most up to date information on geographic incidence, please visit CAB International’s Invasive Species Compendium (www.cabi.org/isc/).
Symptoms alone cannot be used to accurately diagnose CCYV infection. Diagnosis requires molecular or serological protocols that are commonly used in many research and diagnostic laboratories.
Molecular assays have been developed for detection of CCYV and include RT-PCR (reverse transcriptase polymerase chain reaction; Okuda et al., 2010), quantitative RT-PCR (Abrahamian et al., 2013; Jailani et al., 2021; Mondal et al., 2023, Plant Dis. accepted), RT-RPA (reverse transcription recombinase polymerase amplification; Zang et al., 2022, J. Virol. Methods 300), and RT-LAMP (reverse transcription loop-mediated isothermal amplification; Wang et al., 2014, J. Virol. Methods 195, and Okuda et al., 2015, J. Virol. Methods 221). DAS-ELISA (double antibody sandwich enzyme-linked immunosorbent assay; Kubota et al., 2011, J. Gen. Plant Pathol. 77), a serological detection methods, is also available for detecting CCYV in plant samples. When choosing an assay, keep in mind that sensitivity for 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 CCYV detection methods.
Although some sources of CCYV resistance have been identified in melon (Okuda et al., 2013, Eur. J. Plant Pathol. 135; Tamang et al., 2019, Cucurbit Gen. Coop. Report 42), resistance does not currently exist for any commercially produced cucurbit species. Management efforts for CCYV, therefore, focus on establishment of non-infected plants, suppression of whitefly vector populations, and management of weed and non-cucurbit hosts. Of these methods, the most important aspect of CCYV management is suppression of whitefly vector populations.
Transplants should be visibly free of virus symptoms and whiteflies (nymphs and adults). Do not import transplants from areas with a known presence of CCYV or other whitefly-transmitted viruses as this can lead to introduction of the virus to new areas.
Insecticide treatment of transplants one to three days before planting can reduce virus infection when transplanting into areas with elevated CCYV and whitefly incidence (Okuda and Wintermantel, 2017).
An additional measure for field crops can include the application of row covers—covering young plants with whitefly-proof mesh to exclude whiteflies while plants are young (LaTora, et al. 2022, Horticulturae 8).
Suppression of whiteflies in fields and greenhouses can be important because sweetpotato whitefly not only can spread CCYV and other viruses to cucurbit crop plants, but whitefly feeding can also kill young plants as well as cause silvering on leaves of squash or pumpkin plants (Figure 6). Yellow sticky traps can be used to monitor the emergence of whiteflies in production areas. Consult local or regional guidelines to determine appropriate materials for suppression of whiteflies and treatment thresholds.
If whitefly populations remain low or can be suppressed throughout the season, introduction of CCYV to crops can be limited or may occur late enough that yield impacts are marginal; however, if plants become infected early, plants will develop more extensive symptoms and will likely have reduce fruit sugars.
Established cucurbit or agricultural crop fields may serve as hosts to large populations of whiteflies and/or CCYV. Removal of these fields may cause whiteflies to move to newly established or younger cucurbit plantings. Fields with whiteflies should be treated prior to 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 CCYV infections.
In addition to suppression of sweetpotato whitefly populations in cucurbit fields, it is important to limit the presence of weed and non-cucurbit host plants, particularly those known to be reservoirs of CCYV, as whiteflies can acquire the virus from these hosts and transmit it to cucurbit crops (Okuda and Wintermantel, 2017).
Okuda, M. and Wintermantel, W. M. 2017. Cucurbit chlorotic yellows. In Keinath, A. P., Wintermantel, W. M., and Zitter, T. A. (eds.), Compendium of Cucurbit Diseases and Pests, 2nd edition (pp. 122-123). American Phytopathological Society Press.
Visit the References page for a full reference list of cited articles.
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.
Author: William M. Wintermantel, USDA-ARS
Senior editor: Rebecca A. Melanson, Mississippi State University
Reviewers: Rajagopalbab (Babu) Srinivasan, University of Georgia, and Shaker Kousik, USDA-ARS
The Emerging Viruses in Cucurbits Working Group and its outreach activities are supported by funding from the Southern IPM Center’s Southern IPM Grants 2022. 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 view of the Southern IPM Center.
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