First report of Cucurbit chlorotic yellows virus infecting melon in the New World

Authors: Wintermantel, William - Bill; Hladky, Laura; Fashing, Patricia; Ando, Kaori; McCreight, James - Jim

Submitted to: Plant Disease
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/17/2018
Publication Date: 2/4/2019
Citation: Wintermantel, W.M., Hladky, L.L., Fashing, P.L., Ando, K., McCreight, J.D. 2019. First report of Cucurbit chlorotic yellows virus infecting melon in the New World. Plant Disease. 103(4):778. https://doi.org/10.1094/PDIS-08-18-1390-PDN.
DOI: https://doi.org/10.1094/PDIS-08-18-1390-PDN

Interpretive Summary: During the summer of 2018, melon plants from a germplasm increase in the Imperial Valley of California were found infected with the crinivirus, Cucurbit chlorotic yellows virus (CCYV). Two melon plants were found exhibiting interveinal yellowing and chlorotic spot symptoms similar to those caused by a crinivirus, but varying from symptoms normally observed during infection by the widely prevalent and well-established crinivirus, Cucurbit yellow stunting disorder virus (CYSDV). DNA extracted from leaves of both plants was negative for CYSDV, but positive for CCYV. In an additional test, the two plants were 100% and 99% identical for sequenced regions of RNA 1 and RNA 2 of CCYV isolates from throughout the world. Due to the similarity in symptoms between CCYV and CYSDV, several archived and frozen total nucleic acid and RNA extracts from Imperial Valley melon, collected over the course of 9 years (2010-2018), were re-analyzed for CCYV to determine whether the virus was newly emerged or if it had evaded detection due to similarity in symptoms to CYSDV. Nineteen of 23 samples collected between 2014 and 2018 were positive for CCYV, and many samples contained mixed infections of CCYV with CYSDV and/or the ipomovirus, squash vein yellowing virus (SqVYV). All eighteen archived samples collected from 2010 to 2013 tested negative for CCYV, but extracts were confirmed as viable because parallel amplification of CYSDV from these samples was successful. Therefore, CCYV most likely emerged in the Imperial Valley during in 2014 but remained undetected due to similarity with CYSDV in symptoms on cucurbit host plants and vector transmission. CCYV is prevalent in East Asia, the Middle East, and North Africa, and is transmitted efficiently by the whitefly, Bemisia tabaci. CCYV and CYSDV have long retention times in their whitefly vector, facilitating transmission throughout the region. Further studies will be necessary to evaluate epidemiology of CCYV in the southwestern US desert production region, and to determine its impact on melon production and development of crinivirus-resistant cultivars.

Technical Abstract: During the summer of 2018, melon (Cucumis melo) plants from a germplasm diversity study in the Imperial Valley of California were found infected with Cucurbit chlorotic yellows virus (CCYV; genus Crinivirus, family Closteroviridae). Two melon plants were found exhibiting interveinal yellowing and chlorotic spot symptoms similar to those caused by a crinivirus, but varying from symptoms normally observed during infection by Cucurbit yellow stunting disorder virus (CYSDV; genus Crinivirus). Total nucleic acid was extracted from leaves of both plants and tested negative for CYSDV, but positive for CCYV by RT-PCR using primers specific to portions of RNA2 of each virus encoding the virus coat protein genes. The CCYV amplicon was sequenced and shared 99% sequence identity with most of the CCYV isolates from around the world sequenced to date. A second set of CCYV-specific primers were designed to a region within RNA1 encoding the RNA-dependent RNA polymerase (RdRp) gene and amplification of a 370 nt amplicon was confirmed. This 370 nt RdRp amplicon sequenced was a 100% match to 20 CCYV isolates from around the world. Due to the similarity in symptoms between CCYV and CYSDV, several archived and frozen total nucleic acid and RNA extracts from Imperial Valley melon, collected over the course of 9 years (2010-2018), were re-analyzed for CCYV to determine whether the virus was newly emerged or if it had evaded detection due to similarity in symptoms to CYSDV. Nineteen of 23 samples collected between 2014 and 2018 were positive for CCYV, and many samples contained mixed infections of CCYV with CYSDV and/or the ipomovirus, Squash vein yellowing virus (SqVYV). All eighteen archived samples collected from 2010 to 2013 tested negative for CCYV, but extracts were confirmed as viable because parallel amplification of CYSDV from these samples was successful. Therefore, CCYV most likely emerged in the Imperial Valley during in 2014 but remained undetected due to similarity with CYSDV in symptoms on cucurbit host plants and vector transmission. CCYV is prevalent in East Asia, the Middle East, and North Africa, and is transmitted efficiently by the whitefly, Bemisia tabaci. Both CCYV and CYSDV have long retention times in their whitefly vector, facilitating transmission throughout the region. Further studies will be necessary to evaluate epidemiology of CCYV in the southwestern US desert production region, and to determine its impact on melon production and development of crinivirus-resistant cultivars.