EPPO Alert List – Citrus yellow vein clearing virus (Potexvirus citriflavivenae)

 

Why

The yellow vein clearing disease is an emerging disease of citrus that was first observed in Pakistan in 1988 in lemon (Citrus limon) and sour orange trees (C. aurantium). In 1997, the disease was observed in several citrus-growing areas of India on different citrus species (Etrog citron (C. medica var ‘Etrog’), Rangpur lime (C. x limonia), sour orange, and lemon). In 2000, the disease was reported from Türkiye in lemon and sour orange trees in the region of Adana. In 2009, CYVCV was also found in lemon trees in Yunnan, China. Following the detection in Türkiye, eradication measures were taken, and surveys were carried out. As of 2023, the virus was no longer detected in the Turkish citrus-producting regions.  In 2024, CYVCV was detected in a small number of citrus trees (6 symptomatic lemon trees and 1 asymptomatic sweet orange tree) in a private garden in Campania, Italy. 

Initially the presence of a filamentous virus was consistently observed in citrus symptomatic plants, but its identity remained unknown until 2012, when serological, molecular and biological studies showed that a new virus species called citrus yellow vein clearing virus (Potexvirus citriflavivenae, CYVCV) was the causal agent of the disease (EPPO RS 2013/196). Since then, CYVCV has continued to spread in China and other Asian countries and has recently been reported in California (US), a first record for the Americas. Considering the potential impact of this emerging disease on citrus production, the EPPO Secretariat considered that CYVCV should be added to the EPPO Alert List.

 

Courtesy: Melike Yurtmen

Where

EPPO region: Italy (transient).

Asia: China (Chongqing, Fujian, Guangdong, Guangxi, Guizhou, Hunan, Jiangxi, Sichuan, Yunnan), India (Andhra Pradesh, Maharashtra, Punjab), Iran, Korea (Republic of), Pakistan.

North America: USA (California).

 

On which plants

CYVCV can infect most citrus species, cultivars and hybrids, particularly lemon (C. limon) and sour orange (C. aurantium). In Türkiye, in addition to the findings on citrus, CYVCV has been reported once on grapevine (Vitis vinifera) plants showing leaf necrosis, small leaves and shortened internodes. In addition to citrus and grapevine, CYVCV has also been detected in asymptomatic wild plants (Malva sylvestris, Ranunculus arvensis, Sinapis arvensis and Solanum nigrum).

 

Damage

On citrus, symptoms include strong yellow vein clearing, leaf distortion, and occasionally, ringspots and veinal necrosis, as well as fruit malformation. Severe infections can lead to tree decline and decreased fruit marketability (fruit quantity and quality is reduced). Disease symptoms may vary according to citrus varieties, viral strains, and environmental conditions.

 

Transmission

CYVCV can be transmitted by grafting and contaminated tools. In addition to mechanical transmission, CYVCV is transmitted by insect vectors. Two aphid species, Aphis spiraecola, and A. craccivora have been shown to transmit CYVCV from infected lemons to legumes. In addition, A. A. aurantii, A. spiraecola, A. gossypii and Dialeurodes citri (citrus whitefly) could successfully transmit CYVCV between citrus species. It is thought that disease spread in the field is mainly ensured by insect vectors. So far, seed transmission of CYVCV has not been demonstrated.

 

Pathways

Plants for planting (scions, rootstocks, seedlings), viruliferous vectors, contaminated tools and equipment.

 

Possible risks

Citrus spp. are economically important trees for the Mediterranean Basin, cultivated for fruit production and ornamental purposes. CYVCV is causing an emerging disease which can potentially have negative impacts on citrus production by affecting tree growth and fruit marketability. The fact that CYVCV has been detected once in grapevine in Türkiye may also add to the risk. The past detection of CYVCV in Türkiye and the recent one in Italy show that this virus has the potential to enter citrus production in the EPPO region, in addition its known insect vectors are present to ensure its further spread. As CYVCV can be spread by the movements of infected propagation material, as well as by grafting and contaminated tool, it is important that NPPOs of the citrus-growing countries of the EPPO region are alerted about this new citrus disease.

 

Sources

Afloukou FM, Çalişkan F, Önelge N (2021) Aphis gossypii Glover is a vector of citrus yellow vein clearing virus. Journal of General Plant Pathology 87(2), 83-86.

Afloukou FM, Önelge N (2020) First report of natural infection of grapevine (Vitis vinifera) by citrus yellow vein clearing virus. New Disease Reports 42, 5. http://dx.doi.org/10.5197/j.2044-0588.2020.042.005

Bani Hashmian SM, Aghajanzadeh S (2017) Occurrence of citrus yellow vein clearing virus in citrus species in Iran. Journal of Plant Pathology 99(1), p 290.

Chen HM, Li ZA, Wang XF, Zhou Y, Tang KZ, Zhou CY, Zhao XY, Yue JQ (2014) First report of citrus yellow vein clearing virus on lemon in Yunnan, China. Plant Disease 98(12), p 1747.

Citrus Insider. Citrus Pest & Disease Prevention Program (2023-12-22) Citrus yellow vein clearing virus found in Los Angeles County. https://citrusinsider.org/2023/12/22/citrus-yellow-vein-clearing-virus-found-in-los-angeles-county/

Jin T, Kim JK, Byun HS, Choi HS, Cha B, Kwak HR, Kim M (2024) Occurrence and multiplex PCR detection of citrus yellow vein clearing virus in Korea. The Plant Pathology Journal 40(2), 125. https://doi.org/10.5423/PPJ.OA.09.2023.0136

Li XT, Su HN, Tan KG, Tong XN, Zhong BL (2017) Fruit malformation of Satsuma mandarin (Citrus unshiu Marc.) infected by citrus yellow vein clearing virus. Journal of Phytopathology 165(5), 283-288.

Liu C, Liu H, Hurst J, Timko MP, Zhou C (2020) Recent advances on citrus yellow vein clearing virus in Citrus. Horticultural Plant Journal 6(4), 216-222. https://www.sciencedirect.com/science/article/pii/S2468014120300431

Loconsole G, Önelge N, Portere O, Giampetruzzi A, Bozan O, Satar S, De Stradis A, Savino V, Yokomi RK, Saponari M (2012) Identification and characterization of citrus yellow vein clearing virus, a putative new member of the genus Mandarivirus. Phytopathology 102(12), 1168-1175.

Maghsoudi R, Nassrollahnejad S, Aghajanzadeh S, Hashemian SM (2023) Transmissibility of Citrus yellow vein clearing virus by three dominant citrus aphids. Iranian Journal of Plant Protection Science 54(1), 101-113. https://doi.org/10.22059/IJPPS.2023.353042.1007016

NPPO of Italy (2024-07).

NPPO of Türkiye (2023-08).

Önelge N, Bozan O, Gök-Güler P (2016) First report of ctrus yellow vein clearing virus infecting new natural host plants in Turkey. Journal of Plant Pathology 98(2), p 373.

Satar S, Önelge N (2009) First report of the transmission of Citrus yellow vein clearing by Aphis craccivora Koch. Journal of Phytopathology 91(4 suppl.), S4. 99.

Zhang Y, Liu Y, Wang Y, Wang Q, He S, Li X, Zhou Y (2019) Transmissibility of citrus yellow vein clearing virus by contaminated tools. Journal of Plant Pathology 101(1), 169-171.

Zhang Y, Wang Y, Wang Q, Cao M, Zhou C, Zhou Y (2018) Identification of Aphis spiraecola as a vector of citrus yellowing vein clearing virus. European Journal of Plant Pathology 152(3), 841-844.

Zhang YH, Liu Ch, Wang Q, Wang YL, Zhou CY, Zhou Y (2019) Identification of Dialeurodes citri as a vector of citrus yellow vein clearing virus in China. Plant Disease 103(1), 65-68.

Zhou Y, Chen HM, Cao MJ, Wang XF, Jin X, Liu KH, Zhou CY (2017) Occurrence, distribution, and molecular characterization of citrus yellow vein clearing virus in China. Plant Disease 101(1), 137-143.

Zhou Y, Chen HM, Wang XF, Li ZA, Tang M, Zhou CY (2015) Lack of evidence for seed transmission of citrus yellow vein clearing virus despite its frequent detection in seed tissues. Journal of Plant Pathology 97(3), 519-521.

 

EPPO RS 2013/196, 2022/221, 2023/194, 2023/210, 2024/001, 2024/136, 2024/151