Tomato bushy stunt virus

N. benthamiana, a common experimental host for TBSV.

TBSV has a broad host range under experimental conditions and has been reported to infect over 120 plant species spanning 20 families. However, under natural conditions its range is much narrower and generally comprises crop vegetables and ornamental plants. It was first identified in tomato plants and also has been documented to affect apple, artichoke, cherry, grapevine, hops, and pepper. Although it causes significant loss of yield in tomato plants, it is not considered an economically significant pathogen.[4][5] It is, however, a very well-established model system for the study of plant viruses, usually through experimental infection of Nicotiana benthamiana or Nicotiana clevelandii, relatives of tobacco plants in which TBSV can cause systemic infection. Notably, the common model plant Arabidopsis thaliana is not a host.[3][4] TBSV can also replicate in yeast in laboratory conditions.[6]

The signs of TBSV are host-dependent. Local infections can cause necrotic or chlorotic lesions. Systemic infections can cause stunted growth, deformed or absent fruit, and damaged leaves; in agricultural settings yield can be significantly reduced. The stunted, "bushy" appearance of the tomato plants in which the virus was first discovered gave the pathogen its name. In some hosts, most notably N. benthamiana, TBSV can cause lethal systemic necrosis.[4][5]

TBSV is thought to be passively transmitted in the wild, primarily through soil or water. There are no known vector organisms; transmission by aphids, mites, and the fungus Olpidium brassicae has specifically been ruled out.[5] However, the closely related tombusvirus Cucumber necrosis virus (CNV) has been observed to be transmitted by Olpidium bornovanus zoospores, so transmission of TBSV by as-yet unknown vector remains a possibility.[4] TBSV can also be transmitted through seed or by mechanical inoculation.[4][5] In experimental tests, the virus can survive passage through the human digestive system if consumed in food and will remain infectious; it has been hypothesized that spread through sewage could occur.[7]

TBSV is distributed fairly widely across central and western Europe, north Africa, and North and South America.[4][5] No specific control measures are recommended for the virus, though pest management guidelines distributed by the University of California recommend avoiding fields with a history of TBSV or using long crop rotations.[8]

TBSV is assigned to the Tombusvirus genus in the family Tombusviridae.[9] Both the genus and the family derive their names from an abbreviation of "tomato bushy stunt virus".[10]

Schematic drawings of a Tombusviridae virion (cross-section and side view)

TBSV is an unenveloped icosahedral virus with a T=3 viral capsid composed of 180 subunits of a single capsid protein. Its structure was studied extensively by X-ray crystallography from the late 1950s; its icosahedral symmetry was first identified by structural biologist Donald Caspar, who also pioneered the study of the tobacco mosaic virus.[11] A near-atomic-resolution map was obtained in 1978 by a research team including Stephen C. Harrison.[12][13]

Tombusvirus genome map

TBSV is a positive-sense single-stranded RNA virus with a linear genome of ~4800 nucleotides.[14][15] The genome contains five genes that encode a replicase composed of two proteins (p33 and p92), a capsid protein (called CP or p41), and two additional proteins, the RNA silencing suppressor p19 and movement protein p22.[4] These two proteins are expressed from overlapping genes arranged so that the open reading frame of p19 is completely within the ORF of p22.[16] The genome contains one additional possible gene, called pX, of unknown function.[4]

p19

The p19 protein in complex with double-stranded RNA.

The p19 protein is a pathogenicity factor and functions by suppressing the RNA silencing pathway, a common form of antiviral defense. The p19 protein binds short interfering RNAs and prevents their incorporation into the RNA-induced silencing complex (RISC), thereby allowing viral propagation in the host plant.[3][17][18] The presence of p19 is necessary for systemic infection or for lethal infection in some hosts; in the experimental host N. benthamiana, p19 largely mediates the lethal systemic necrosis that is the outcome of TBSV infection.[4][17]

A TBSV virion contains one copy of its positive-sense single-stranded RNA genome, which is linear and lacks a 3' polyadenine tail or 5' cap. Nevertheless, the p33 and p92 proteins are translated directly from genomic RNA. When the genome is replicated, two subgenomic RNA molecules are produced that act as messenger RNA; one from which the p41 (CP) gene is expressed, and one from the p19 and p22 genes are expressed. The overlapping p19 and p22 genes are both translated through the effects of leaky scanning.[4] Several long-distance interactions between linearly well-separated areas of the genome have been identified with functional importance in ensuring efficient replication.[16]

Defective interfering RNA (DI) molecules are RNAs that are produced from the viral genome but are not competent to infect cells on their own; instead they require coinfection with an intact "helper" virus. TBSV infections often produce significant numbers of DIs from consistent parts of the genome under experimental conditions, but this behavior has not been observed in the wild. Their production is likely to be host specific. Infections that give rise to DIs usually have milder signs.[4][19]