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Review
. 2022 Sep;23(9):1262-1277.
doi: 10.1111/mpp.13229. Epub 2022 May 22.

Tomato brown rugose fruit virus: An emerging and rapidly spreading plant RNA virus that threatens tomato production worldwide

Affiliations
Review

Tomato brown rugose fruit virus: An emerging and rapidly spreading plant RNA virus that threatens tomato production worldwide

Shaokang Zhang et al. Mol Plant Pathol. 2022 Sep.

Abstract

Tomato brown rugose fruit virus (ToBRFV) is an emerging and rapidly spreading RNA virus that infects tomato and pepper, with tomato as the primary host. The virus causes severe crop losses and threatens tomato production worldwide. ToBRFV was discovered in greenhouse tomato plants grown in Jordan in spring 2015 and its first outbreak was traced back to 2014 in Israel. To date, the virus has been reported in at least 35 countries across four continents in the world. ToBRFV is transmitted mainly via contaminated seeds and mechanical contact (such as through standard horticultural practices). Given the global nature of the seed production and distribution chain, and ToBRFV's seed transmissibility, the extent of its spread is probably more severe than has been disclosed. ToBRFV can break down genetic resistance to tobamoviruses conferred by R genes Tm-1, Tm-2, and Tm-22 in tomato and L1 and L2 alleles in pepper. Currently, no commercial ToBRFV-resistant tomato cultivars are available. Integrated pest management-based measures such as rotation, eradication of infected plants, disinfection of seeds, and chemical treatment of contaminated greenhouses have achieved very limited success. The generation and application of attenuated variants may be a fast and effective approach to protect greenhouse tomato against ToBRFV. Long-term sustainable control will rely on the development of novel genetic resistance and resistant cultivars, which represents the most effective and environment-friendly strategy for pathogen control.

Taxonomy: Tomato brown rugose fruit virus belongs to the genus Tobamovirus, in the family Virgaviridae. The genus also includes several economically important viruses such as Tobacco mosaic virus and Tomato mosaic virus.

Genome and virion: The ToBRFV genome is a single-stranded, positive-sense RNA of approximately 6.4 kb, encoding four open reading frames. The viral genomic RNA is encapsidated into virions that are rod-shaped and about 300 nm long and 18 nm in diameter. Tobamovirus virions are considered extremely stable and can survive in plant debris or on seed surfaces for long periods of time.

Disease symptoms: Leaves, particularly young leaves, of tomato plants infected by ToBRFV exhibit mild to severe mosaic symptoms with dark green bulges, narrowness, and deformation. The peduncles and calyces often become necrotic and fail to produce fruit. Yellow blotches, brown or black spots, and rugose wrinkles appear on tomato fruits. In pepper plants, ToBRFV infection results in puckering and yellow mottling on leaves with stunted growth of young seedlings and small yellow to brown rugose dots and necrotic blotches on fruits.

Keywords: Tomato brown rugose fruit virus; RNA virus; cross protection; emerging virus; seedborne virus; tobamovirus; tomato.

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Conflict of interest statement

The authors declare that no competing interests exist.

Figures

FIGURE 1
FIGURE 1
Distribution of ToBRFV. (a) The geographic map of ToBRFV. All countries with confirmed incidences are highlighted in red. (b) The graph shows the trend of the accumulated number of reported countries starting from the first outbreak in 2014. Data are adapted from the references in Table 1 and the European and Mediterranean plant protection organization (EPPO) global database (https://gd.eppo.int/taxon/TOBRFV/distribution).
FIGURE 2
FIGURE 2
Typical symptoms induced by ToBRFV. (a–e) Severe mosaic, chlorotic mottling, necrotic, deformed, dark green bulges, and narrowing symptoms on leaves of tomato cultivars Piccolo (a, b), Kivu (c, d), and Moneymaker (e). (f–k) Fruits with brown rugosity (white arrows), yellowing, yellow patches, marbling, and deformation symptoms on tomato cultivars Piccolo (f, g), Kivu (h, i), and Moneymaker (k). (l) ToBRFV‐infected Nicotiana benthamiana showing yellowing and curling leaves along with the stunting phenotype.
FIGURE 3
FIGURE 3
Schematic representation of the ToBRFV genome. The numbers indicate the nucleotide positions where each open reading frame (ORF) begins and ends in the representative ToBRFV isolate (NC_028478.1, 6393 bp). ORF2 is translated via readthrough of ORF1 at nucleotide 3427. The lower panel shows that ORF3 and ORF4 are expressed from subgenomic RNAs.
FIGURE 4
FIGURE 4
Neighbour‐joining phylogenetic tree based upon the complete genome sequences of ToBRFV, TMV, and ToMV. TMV (NC_001367.1), and ToMV (NC_002692.1) are used as outgroups (shown in blue). The representative ToBRFV isolate (NC_028478.1) is highlighted in green. The bootstrap confidence values generated by 1000 replications are shown in purple at the branches.

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