EPPO Alert List – Tomato mottle mosaic virus

 

 

Why

Tomato mottle mosaic virus (Tobamovirus, ToMMV) was first described in 2013 infecting tomato crops in Mexico. It was subsequently found in the Americas, Asia and Europe causing infections on tomato and capsicum crops. As ToMMV is an emerging virus which present similarities with another emerging tobamovirus, tomato brown rugose fruit virus (ToBRFV - EPPO A2 List), and as capsicum and tomato are important crops in the EPPO region, the EPPO Panel on Phytosanitary Measures recommended that ToMMV should be added to the EPPO Alert List.

 

Where

Although being a distinct species, ToMMV is closely related to tomato mosaic virus (ToMV) and cross-reactions have been observed when using serological tests. It is noted that before ToMMV was characterized in 2013 in Mexico, several isolates deposited in GenBank as ToMV corresponded in fact to ToMMV (e.g. isolates from Brazil (2003), China and Iran previously attributed to ToMV have now been re-attributed to ToMMV). The distribution below shows the countries where ToMMV has been detected using molecular tests, but it cannot be excluded that some past records of ToMV should be attributed to ToMMV and that its distribution might be wider than shown below.

EPPO region: Czech Republic (detected in 2020 in 3 asymptomatic seed crops), Israel (detected in 2014 in a tomato glasshouse), Spain (detected in 2015 in a research glasshouse).

Asia: China (Gansu, Hainan, Henan, Hunan, Liaoning, Neimenggu, Shaanxi, Shandong, Xizhang, Yunnan), Iran, Israel.

North America: Mexico, USA (California, Florida, New York, South Carolina).

South America: Brazil (Minas Gerais, Sao Paulo).

 

On which plants

Natural infections have mainly been reported on tomato and capsicum (C. annum, C. frutescens) grown in the field and under glasshouses, and there is one record of ToMMV in symptomatic peas (Pisum sativum) in Yunnan province (China). However, laboratory experiments have shown that the host range of ToMMV might be wider, as the virus could be mechanically transmitted to other Solanaceae (Nicotiana spp., Petunia hybrida, Physalis spp.) and Brassicaceae (Brassica spp., Raphanus sativus). The presence of ToMMV has also been detected by metagenomics in Cicer arietinum (Fabaceae) in Italy but this has not been confirmed by further studies. In China, mixed infections of ToMMV with tobacco mild green mosaic virus have been observed on aubergine (Solanum melongena) causing symptoms and yield losses, but the host status of S. melongena for ToMMV remains to be clarified.

 

Damage

Affected tomato plants show leaf distortion, mosaic, mottle and necrosis. During inoculation experiments, susceptible tomato cultivars were seriously stunted, flowers aborted and no fruit was produced. Outbreaks on capsicum crops have been reported from China (Tibet and Yunnan) where affected plants showed foliar mottle, shrinking, and necrosis. As is the case for other Tobamovirus, it has been observed that disease symptoms rapidly spread within infected crops. During experiments carried out on several tomato cultivars in China, it has been shown that ToMMV could overcome the resistance to ToMV in some cultivars.

 

Transmission

Further studies are needed on the transmission of ToMMV, but observations suggest that as other tobamoviruses, it is a highly contagious virus which is mechanically transmitted from plant to plant through common cultural practices. Like tomato brown rugose fruit virus, ToMMV might also be spread by bumblebees. Most tobamoviruses contaminate the seed coat (but not necessarily the embryo) of their host plants. So far, seed transmission has not been clearly demonstrated, but observations suggest that seeds could play a role in the rapid spread of the virus at global level. For example, ToMMV was detected in 2019 by the Australian NPPO in an imported seed lot of C. annuum and emergency measures are currently taken to prevent any further entry of the virus in Australia.

 

Pathways

Plants for planting, fruit? seeds? of S. lycopersicum and Capsicum spp. from countries where ToMMV occurs.

 

Possible risks

Tomato and capsicum are important crops for the EPPO region, either grown under glasshouses (across the EPPO region) or in the field (Southern part of the region). For many years, tobacco mosaic virus (TMV) and tomato mosaic virus (ToMV) have been the main tobamoviruses infecting tomatoes, but they were managed by the use of resistant cultivars and virus-tested seed lots. However, the recent emergence of new tobamoviruses such as ToMMV and Tomato brown rugose fruit virus (EPPO A2 List) which are able to overcome cultivar resistance could represent a serious threat to the tomato industry. An Express PRA conducted in Germany concluded that ToMMV could present a high risk to tomato and pepper production in Germany and in other EU member states. In a Dutch express PRA (quick scan), the absence of symptoms observed so far on the EU territory and the lack of data on resistance of cultivars used in Europe against ToMMV raised uncertainties about the potential impact of this virus. Further studies on ToMMV are necessary to better determine its geographical distribution, host range, epidemiology and economic impact, but in the meantime, it seems desirable to avoid its further spread within the EPPO region.

 

Sources

Ambros S, Martinez F, Ivars, P, Hernandez C, de la Iglesia F, Elena SF (2017) Molecular and biological characterization of an isolate of Tomato mottle mosaic virus (ToMMV) infecting tomato and other experimental hosts in Eastern Spain. European Journal of Plant Pathology 149(2), 261-268.

Australian Government. Department of Agriculture, Water and the Environment (2019-11) Emergency measures for tomato and capsicum seed: Tomato mottle mosaic virus (ToMMV) Questions and Answers. https://www.agriculture.gov.au/import/goods/plant-products/seeds-for-sowing/emergency-measures-tommv-qa#what-evidence-exists-for-tommv-spread-through-the-movement-of-tomato-and-capsicum-seed

Chai AL, Chen LD, Li B J, Xie XW, Shi YX (2018) First report of a mixed infection of tomato mottle mosaic virus and tobacco mild green mosaic virus on eggplants in China. Plant Disease 102(12), 2668. https://doi.org/10.1094/PDIS-04-18-0686-PDN

Chai A, Chen L Cao J Kang H, Shi Y Xie X, Li B (2019) [Identification of viruses causing eggplant purple mottle flower disease by siRNA High-Throughput Sequencing and RT-PCR detection]. Acta Horticulturae Sinica 46(3), 508-518 (in Chinese).

Che HY, Cao XR (2018) First report of Tomato mottle mosaic virus in tomato crops in China. Plant Disease 102(10), p 2051. https://doi.org/10.1094/PDIS-03-18-0538-PDN

Dutch NPPO (2020-11-09) Tomato mottle mosaic virus quick scan. https://english.nvwa.nl/topics/pest-risk-analysis/documents/plant/plant-health/pest-risk-analysis/documents/quick-scan-tomato-mottle-mosaic-virus

JKI (2020-04-01) Express PRA on Tomato mottle mosaic virus (in German). https://pflanzengesundheit.julius-kuehn.de/dokumente/upload/ToMMV_expr-pra.pdf

Fillmer K, Adkins S, Pongam P, D'Elia T (2015) Complete genome sequence of a Tomato mottle mosaic virus isolate from the United States. Genome Announcements 3(2), e00167-15. https://doi.org/10.1128/genomeA.00167-15

Li R, Gao S, Fei Z, Ling KS (2013) Complete genome sequence of a new tobamovirus naturally infecting tomatoes in Mexico. Genome Announcements 1(5), e00794-13.

Li Y, Wang Y, Hu J, Xiao L, Tan G, Lan P, Liu Y, Li F (2017) The complete genome sequence, occurrence and host range of Tomato mottle mosaic virus Chinese isolate. Virology Journal 14, 15. doi: 10.1186/s12985-016-0676-2

Li Y, Tan G, Xiao L, Zhou W, Lan P, Chen X, Liu Y, Li R, Li F (2021) a multiyear survey and identification of pepper- and tomato-infecting viruses in Yunnan Province, China. Fronters in Microbiology 12, 623875. https://doi.org/10.3389/fmicb.2021.623875

Li YY, Wang CL, Xiang D, Li RH, Liu Y, Li F (2014) First report of Tomato mottle mosaic virus infection of pepper in China. Plant Disease 98(10), p 1447. https://doi.org/10.1094/PDIS-03-14-0317-PDN

Li YY, Zhou WP, Lu SQ, Chen DR, Dai JH, Guo QY, Liu Y, Ta, GL (2020) Occurrence and biological characteristics of tomato mottle mosaic virus on solanaceae crops in China. Scientia Agricultura Sinica 53(3), 539-550 (abst.).

Lovelock DA, Kinoti WM, Bottcher C, Wildman O, Dall D, Rodoni BC, Constable FE (2020) Tomato mottle mosaic virus intercepted by Australian biosecurity in Capsicum annuum seed. Australasian Plant Disease Notes 15, 8. https://doi.org/10.1007/s13314-020-0378-x

Marubayashi JM, Bello VH, Yuki VA, Ortiz MRA, Banja WH, Neto SD, Krause-Sakate R, Pavan MA (2017) Ocorrência do tomato mottle mosaic virus - ToMMV em tomateiros no municipio de Uberlândia - MG. Abstract of a paper presented at the XL Congresso Paulista de Fitopatologia (Campinas, BR, 2017-02-07/09). Summa Phytopathologica 43(suppl.), unpaginated.

Nagai A, Duarte LML, Chaves ALR, Alexandre MAV, Ramos-González PL, Chabi-Jesus C, Harakava R, Santos DYAC dos (2018) First complete genome sequence of an isolate of tomato mottle mosaic virus infecting plants of Solanum lycopersicum in South America. Genome Announcements 6(19), e00427-18. https://doi.org/10.1128/genomea.00427-18

Padmanabhan C, Zheng Y, Martin GB, Fei Z, Ling KS (2015) Complete genome sequence of a tomato-infecting Tomato mottle mosaic virus in New York. Genome Announcements 3(6) e01523-15. https://doi.org/10.1128/genomeA.01523-15

Pirovano W, Miozzi L, Boetzer M, Pantaleo V (2014) Bioinformatics approaches for viral metagenomics in plants using short RNAs: model case of study and application to a Cicer arietinum population. Frontiers in Microbiology 5, 790.

Sui X, Zheng Y, Li R, Padmanabhan C, Tian T, Groth-Helms D, Keinath AP, Fei Z, Wu Z, Lin KS (2017) Molecular and biological characterization of Tomato mottle mosaic virus and development of RT-PCR detection. Plant Disease 101(5), 704-711. https://doi.org/10.1094/PDIS-10-16-1504-RE

Turina M, Geraats BPJ, Ciuffo M (2016) First report of Tomato mottle mosaic virus in tomato crops in Israel. New Disease Reports 33, 1. http://dx.doi.org/10.5197/j.2044-0588.2016.033.001

Webster CG, Rosskopf EN, Lucas L, Mellinger HC, Adkins S (2014) First report of Tomato mottle mosaic virus infecting tomato in the United States. Plant Health Progress. https://doi.org/10.1094/PHP-BR-14-0023

Zhan BH, Cao N, Wang KN, Zhou XP (2018) Detection and characterization of an isolate of Tomato mottle mosaic virus infecting tomato in China. Journal of Integrative Agriculture 17(5), 1207-1212.

Zhang S, Tan G, Li F (2021) First report of pea as a natural host of tomato mottle mosaic virus in China. Plant Disease. Early view. https://doi.org/10.1094/PDIS-02-21-0280-PDN

 

EPPO RS 2020/252, 2020/253, 2021/049, 2021/185