Symptoms of Tomato Brown Rugose Fruit Virus (ToBRFV) have been reported for the first time in the UK on a tomato crop.
The outbreak was promptly reported to the Plant Health and Seeds Inspectorate (PHSI) and necessary steps have been taken towards virus eradication, including crop destruction. No further outbreaks have been reported.
Now that the disease has been reported in the UK, propagators and growers are advised to review their production protocols, particularly regarding imports of seed and plants, and crop hygiene.
The virus is a tobamovirus, and is a related to Tobacco mosaic virus (TMV) and Tomato mosaic virus (ToMV). However, the new virus can overcome the Tm-22 resistance gene which means that TMV and ToMV resistant varieties will be susceptible to this new virus (ToBRFV). At present there is no reported tomato resistance to ToBRFV.
ToBRFV was first described from tomato crops in Israel in 2014, where the virus spread in tomato greenhouses almost nationwide within the period of one year after the first outbreak reports. The virus has since been reported from Jordan, Mexico, and Italy, including the island of Sicily, and is present but under eradication in Germany following outbreaks in several glasshouses.
Symptoms of ToBRFV
The virus is named after the characteristic brown wrinkled (rugose) patches which can develop on fruit of infected plants. However, symptoms of infection can vary with variety and in tomato can include mild to severe mosaic, discolouring on the leaves, with some leaves becoming narrower. Tomato fruits can be discoloured, misshapen, turning yellow or brown with crinkling of the skin. The virus can readily spread to all plants in a crop. Due to the symptoms, the fruits of infected plants lose market value or are unmarketable.
- Mosaics (chlorotic or pale patches) develop on younger leaves in the head and side shoots.
- Leaves may be crumpled (puckered) and deformed, in some cases leaves may be narrowed
- Brown (necrotic) streaks may develop on stems.
- Fruit can develop chlorotic marbling which can appear similar to infection with Pepino mosaic virus.
- Fruit may develop brown wrinkled (rugose) patches
Symptoms of tomato brown rugose fruit virus - pictures
Symptoms in Sweet pepper
Images showing symptoms in Sweet pepper crops can also be found on this presentation sourced from the Ministry of Agriculture, Mexico. Please note the presentation is in Spanish, but the images should be useful for symptom recognition. We do not necessarily endorse the hygiene recommendations in the document, please instead refer to the hygiene document and recommendations below.
Hosts and spread
Tomato is a major host of ToBRFV, but inoculation trials have demonstrated that Sweet pepper (Capsicum annuum) as well as the experimental host plants Nicotiana species, Solanum nigrum, Chenopodium quinoa, Petunia hybrida and Chenopodium murale can act as minor hosts showing slight symptoms. To date, the only confirmed outbreak of the virus on peppers was from Mexico.
Tobamoviruses are stable outside of their host, and the main routes for transmission of ToBRFV are through propagation material (cuttings and grafts) or mechanical means and contact. For example, the movement of virus on contaminated tools, hands and clothing, or plant-to-plant contact. As with other tobamoviruses, it is also thought that ToBRFV is seed transmitted. Even a low efficiency of seed transmission could cause a number of infected plants to be present in a glasshouse.
Once an outbreak of ToBRFV occurs, normal glasshouse working practices can quickly spread the virus via movements of contaminated tools and equipment (such as during plant cutting, on workers hands and clothing, via picking carts and crates, stringing to trellis ropes, and on glasshouse structures). It has also recently been reported that the virus can be transmitted by bumblebees during pollination.
Following an outbreak the virus could remain viable in leaf debris, seeds or contaminated soil for several months. Once the virus is introduced in an area, potential control measures are very limited and rely mainly on elimination of infected plants and strict hygiene measures. However, many of these hygiene measures can also be used prophylactically to minimise the risk of entry, spread and impact of this virus.
Hygiene best practice
Hygiene best practice procedures should be followed as a precautionary measure to minimise the impact of an outbreak should one occur.
As the virus is primarily transmitted via contact, a suite of prophylactic measures termed ‘hygiene best practice’ should be followed to minimise the chances of the virus entering and spreading within a crop. These precautions should be applied routinely. This list is not exhaustive but gives measures recommended to minimise the risk of spread of contact transmitted pathogens including other viruses and viroids.
Access should be limited to people working in the specific crop/glasshouse. This will minimise the risk of inadvertent introduction and spread around the glasshouse production facility via human activity. Additionally, as a standard, there should be no direct travel between packhouses and glasshouses on the same day. Clothing must be changed/washed between the two locations if entering on different days.
If infected produce goes through a packing facility, both machinery, equipment, and workers can be contaminated. If these workers or equipment are then moved into a production facility this can spread the virus into a previously healthy crop.
Staff should be trained in basic symptom recognition and hygiene measures to contain outbreaks of pathogens when they occur, including best practice for plant handling etc.
Ideally staff should not be moving between production facilities and should never move between packing and production facilities
Growers and employees eating fruit of tomato and pepper which may be contaminated could inadvertently pass on the virus.
Washing your hands for 30 seconds does not kill the virus. However, nurseries should continue to implement their standard hand washing procedures to prevent the spread of other diseases.
Disposable gloves should be used and changed regularly. The virus will remain active on hands and gloves for at least two hours.
Workers should use disposable clothing, such as a disposable over-suit and shoe covers, to minimise introduction and spread of the pathogen. These should be put on when entering a glasshouse and should be disposed off on leaving the glasshouse and not reused. If this is not feasible for full-time staff, then they should be issued clothing to wear only in the glasshouse which is then regularly laundered at high temperature. Growers could use clothing in different colours to denote workers from different parts of the site to prevent cross contamination.
Equipment and tools which come into contact with an infected plant can act as a source of virus for onward transmission. Equipment such as picking carts, sprayers, and hand tools (e.g. pruning knives) should all be cleaned and disinfected routinely. Tools should ideally be disinfected during pruning activities between individual plants. Equipment should be cleaned and disinfected at least between crops. The virus on plastic trays can be destroyed by heat treatment (e.g. steam sterilisation) for five minutes at 90°C. Treatment at 70°C for five minutes appears to be ineffective.
It is important to assess your business and the protocols in place at each stage of production. This document has been produced to help you identify the risk points in your business and production cycle:
Presentations from the Tomato Growers' Association Conference 2019 afternoon session on ToBFRV:
Testing for ToBRFV in tomato seed and young plants
Fera Science Ltd is the only UK organisation to offer seed testing for ToBRFV at present. Contact: Adrian.email@example.com. Seed numbers required and costs are outlined in the table below:
£450 + VAT
10 working days
£226 + VAT
10 working days
A similar service is provided by Naktuinbouw in the Netherlands. Contact: Harrie Koenraadt (Head of seed testing) firstname.lastname@example.org
Hard and fast guidance on approaches for testing for ToBRFV in propagation plants is not yet available.
As part of AHDB's response to this threat we hosted a webinar with Adrian Fox (Senior Plant Virologist, Fera), Heiko Ziebell (Senior Scientist, Julius Kühn-Institut for Epidemiology and Pathogen Diagnostics), and Sharon Matthews-Berry (Plant Health Consultant, Defra) to update the industry with the latest information on this virus and recommendations for growers. Click here for FAQs.
In the event of an outbreak
The main advice is to implement good hygiene measures as a matter of course, be vigilant for any unusual symptoms in the crop, and report any symptoms to manager if suspected.
Suspected outbreaks of a viroid or virus in a tomato crop or any other non-native plant pest should be reported to the relevant authority:
For England and Wales, contact your local APHA Plant Health and Seeds Inspector or the PHSI Headquarters, Sand Hutton, York. Tel: 01904 405138
For Scotland, contact the Scottish Government’s Horticulture and Marketing Unit:
For Northern Ireland, contact the DAERA Plant Health Inspection Branch:
Tel: 0300 200 7847 Email: email@example.com
For additional information on UK Plant Health please see:
Author: Adrian Fox, Fera
Pictures reproduced by kind permission of EPPO; Dr Aviv Dombrovsky and Elisheva Smith, (source Dombrovsky and Smith, 2017, Seed Transmission of Tobamoviruses: Aspects of Global Disease Distribution, from Seed Biology Ed. Jose C. Jimenez-Lopez); and Dr Wulf Menzel (as published in Menzel et al. (2019). New Disease Reports 39, 1)