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PM 7/146 (1) Tomato Brown Rugose Fruit Virus Bulletin OEPP/EPPO Bulletin (2021) 51 (1), 178–197 ISSN 0250-8052. DOI: 10.1111/epp.12723 European and Mediterranean Plant Protection Organization Organisation Europe´enne et Me´diterrane´enne pour la Protection des Plantes PM 7/146 (1) Diagnostics PM 7/146 (1) Tomato brown rugose fruit virus Diagnostic Specific approval and amendment Approved in 2020-10. Specific scope This Standard describes a diagnostic protocol for detection and identification of tomato brown rugose fruit virus.1 This Standard should be used in conjunction with PM 7/ 76 Use of EPPO diagnostic protocols. 1. Introduction 2. Identity Tomato brown rugose fruit virus (ToBRFV genus Name: Tomato brown rugose fruit virus. Tobamovirus) was first observed in 2014 and 2015 on Synonyms: None. tomatoes in Israel and Jordan, and outbreaks have recently Acronym: ToBRFV. occurred in China, Mexico, the USA and several EPPO Taxonomic position: Virus, Riboviria, Virgaviridae, countries (EPPO, 2020). The virus is a major concern for Tobamovirus. growers of tomato and pepper as it reduces the vigour of EPPO Code: TOBRFV. the plant, causes yield losses and virus symptoms make the Phytosanitary categorization: EPPO Alert List, EU emer- fruits unmarketable. However, the virus may also be present gency measures. in asymptomatic foliage and fruit. Note Virus nomenclature in Diagnostic Protocols is based Tomato (Solanum lycopersicum) and pepper (Capsicum on the latest release of the official classification by the annuum) are the only confirmed natural cultivated hosts of International Committee on Taxonomy of Viruses (ICTV, ToBRFV (Salem et al., 2016, 2019; Luria et al., 2017; Release 2018b, https://talk.ictvonline.org/taxonomy/). NAPPO, 2018; Panno et al., 2020). ToBRFV was also Accepted species names are italicized when used in their detected in natural weed hosts (Chenopodium murale and taxonomic context, whereas virus names are not, corre- Solanum nigrum) in Israel (Dombrovsky, pers. comm., 2019). sponding to ICTV instructions. The integration of the genus The host status of Solanum melongena (aubergine) is not name within the name of the species is currently not consis- confirmed. tently adopted by ICTV working groups and therefore spe- Because ToBRFV is a relatively new described virus spe- cies names in diagnostic protocols do not include the genus cies, limited published scientific information is available name. Names of viruses not included in the official ICTV and evaluation of tests is underway. This Standard includes classification are based on first reports. tests which have been evaluated in laboratories from the EPPO region. 3. Detection Flow diagrams describing the diagnostic procedure for tomato brown rugose fruit virus in plant material and in 3.1. Disease symptoms seeds are presented in Figs 1 and 2. ToBRFV causes a wide range of symptoms. Symptoms 1Use of brand names of chemicals or equipment in these EPPO Stan- may range from very severe to mild, or plants can be dards implies no approval of them to the exclusion of others that may infected asymptomatically. Leaf symptoms often first also be suitable. appear in the young shoots at the top of the plant. 178 ª 2021 OEPP/EPPO, Bulletin OEPP/EPPO Bulletin 51, 178–197 PM 7/146 (1) Tomato brown rugose fruit virus 179 Plant material except seeds ELISA Symptomatic plant material only PM 7/125 Sample preparation Appendix 1 + - Detection Sample preparation ToBRFV not detected One of the following tests Appendix 1 RT-PCR (Appendix 2 & 3) Real-time RT-PCR (Appendix 4 & 5) - + Confirmation of detection and identification : One of the following tests (use a different test than for detection) RT-PCR (Appendix 2 & 3) OR Real-time RT-PCR (Appendix 4 & 5) - + Retesting or resampling ToBRFV identified ToBRFV not detected Fig. 1 Flow diagram describing the diagnostic procedure for tomato brown rugose fruit virus in plant material except seeds. Seeds Sample preparation Appendix 1 Detection One of the following tests Real-time RT-PCR (Appendix 4 & 5) - + Confirmation of detection and identification: One of the following tests (use a different test than for detection) Real-time RT-PCR (Appendix 4 & 5) - + ToBRFV not detected Retesting or resampling ToBRFV identified Fig. 2 Flow diagram describing the diagnostic procedure for tomato brown rugose fruit virus in seeds. ª 2021 OEPP/EPPO, Bulletin OEPP/EPPO Bulletin 51, 178–197 180 Diagnostic 3.1.1. Symptoms on tomato - Blistering of the leaf surface (Fig. 4). The following virus symptoms may be observed on tomato - Wilting of leaves, followed by yellowing (Fig. 5) (Solanum lycopersicum) infected with ToBRFV (Salem and plant death. et al., 2016; Dombrovsky & Smith, 2017; Cambron-Crisan- tos et al., 2018; AHDB Horticulture, 2019): • Leaves or plants - Chlorosis, mosaic patterns (chlorotic/pale patches) (Fig. 3) and mottling often observed on young leaves at the top of the plant and on side-shoots. Fig. 3 Mosaic symptoms caused by ToBRFV on tomato leaves. Courtesy: C. Picard (EPPO). - Crumpling, puckering or deformation of young Fig. 5 Wilting of leaves, followed by yellowing and plant death caused leaves. by ToBRFV observed in Germany. Courtesy: H. Scholz-Dobelin€ (LWK - Narrowing of leaves (needle-like symptoms), occa- NRW). sionally observed (Fig. 4). • Pedicles (stems), calyx (sepals), and petioles - Brown necrotic lesions (Figs 6 and 7C illustrating symptoms caused by ToBRFV on fruits (see below) also show symptoms on stems and calices. • Fruits - Yellow (chlorotic) spots and marbling of fruits (Fig. 7A, B and C). - Dark-coloured (necrotic) spots on green fruits (Fig. 7B and D). Fig. 6 Necrotic lesions caused by ToBRFV on the sepals of a young Fig. 4 Narrowing (needle-like symptoms) and blistering of the surface tomato fruit. Courtesy: Prof. S. Davino. of tomato leave caused by ToBRFV. Courtesy: C. Picard (EPPO). ª 2021 OEPP/EPPO, Bulletin OEPP/EPPO Bulletin 51, 178–197 PM 7/146 (1) Tomato brown rugose fruit virus 181 ab c (B) Yellow and necrotic spots (a.b) and brown (A) Typical fruit symptoms with yellow (chlorotic) rugose (c) on tomato fruits spots. Courtesy: Dr. P. Keles Ozturk Courtesy: Dr A. Dombrovsky (C) Yellow spots on tomato fruits and necrotic spots on stems and calix (D) Dark coloured (necrotic) spots on green Courtesy: Dr. P. Keles Ozturk fruits. Courtesy: D. Godínez (E) Marbling of fruits and delay in ripening. Courtesy: Dr A. Dombrovsky Fig. 7 Symptoms caused by ToBRFV in tomato fruits. (A) Typical fruit symptoms with yellow (chlorotic) spots. Courtesy: Dr A. Dombrovsky. (B) Yellow and necrotic spots (a, b) and brown rugose (c) on tomato fruits. Courtesy: Dr. P. Keles Ozturk. (C) Yellow spots on tomato fruits and necrotic spots on stems and calix. Courtesy: Dr. P. Keles Ozturk. (D) Dark-coloured (necrotic) spots on green fruits. Courtesy: D. Godınez. (E) Marbling of fruits and delay in ripening. Courtesy: Dr A. Dombrovsky. - Deformation and uneven ripening of young fruits If any of the above symptoms are observed in a tomato (e.g. individual fruits can be red in some parts and variety harbouring tobamovirus resistance genes (e.g. Tm- showing green stripes, blotches or patches in other 22), there is a strong suspicion that ToBRFV is present as parts) (Fig. 7E). these tomato varieties are susceptible to ToBRFV (Luria - Orange fruits not turning red (variety Juanita in et al., 2017). However, similar symptoms might be caused Germany; Scholz-Dobelin,€ pers. comm., 2020). by other viruses and symptoms might be different in the - Brown rugose (wrinkled) patches (rarely observed). case of mixed infections. - Reduced number of fruits per branch. ª 2021 OEPP/EPPO, Bulletin OEPP/EPPO Bulletin 51, 178–197 182 Diagnostic Confusion with other diseases of tomato 3.1.2. Symptoms on pepper Other viruses such as pepino mosaic virus (PepMV), Only pepper plants that do not harbour the L3 and L4 resistance physostegia chlorotic mottle virus (PhCMoV), tomato gene/alleles2 can be infected and therefore show symptoms mosaic virus (ToMV) and tobacco mosaic virus (TMV) may (Turina, pers. comm., 2019); plants harbouring those gene/alle- cause similar (nonspecific) leaf and fruit symptoms that may les react with a local hypersensitive response and are therefore be confused with ToBRFV symptoms (Alkowni et al., not systemically infected (Dombrowski, pers. comm., 2019). 2019). In some EPPO countries, tomato plants are inoculated Symptoms of a hypersensitive response are shown in Fig. 8. with mild strain(s) of PepMV in an early growth stage at the Based on pictures of symptoms on pepper from Mexico fruit production site to prevent infection by more severe available from Sader & Senasica (2019), pepper shows rela- strains (this technique is called cross-protection) (Aguero€ tively similar symptoms to those described for tomato, but et al., 2018; Pechinger et al., 2019). This can lead to mild more severe necrosis is seen on fruit. However, in pepper vari- virus symptoms early in the growing cycle, masking the eties that do not harbour the L resistance gene/alleles L3 and early ToBRFV symptoms and therefore delaying the detec- L4, ToBRFV often occurs in mixed infections with other tion of ToBRFV. The uneven ripening seen on fruit infected viruses (SADER & SENASICA, 2019). Therefore, the by ToBRFV is in general more severe than for PepMV observed symptoms are potentially due to a combination of (EPPO, 2020). Double infection of ToBRFV and another viruses. Symptoms on pepper from an outbreak in Sicily (IT) tobamovirus may result in accelerated virus accumulation in are described in Panno et al. (2020). The infected variety did the plants. This phenomenon has been observed in suscepti- not harbour the L resistance gene (Davino, pers. comm., 2020). ble wild-type tomato plants and in tomato plants harbouring Symptoms of pepper plants that do not harbour the gene/ the Tm-22 resistance gene infected by paprika mild mottle alleles L3 and L4 obtained after mechanical inoculation are virus (PaMMV) and ToBRFV (Luria et al., 2018).
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