Using genomic analysis to identify tomato Tm-2 resistance-breaking mutations and their underlying evolutionary path in a new and emerging tobamovirus

Abstract

In September 2014, a new tobamovirus was discovered in Israel that was able to break Tm-2-mediated resistance in tomato that had lasted 55 years. The virus was isolated, and sequencing of its genome showed it to be tomato brown rugose fruit virus (ToBRFV), a new tobamovirus recently identified in Jordan. Previous studies on mutant viruses that cause resistance breaking, including Tm-2-mediated resistance, demonstrated that this phenotype had resulted from only a few mutations. Identification of important residues in resistance breakers is hindered by significant background variation, with 9-15% variability in the genomic sequences of known isolates. To understand the evolutionary path leading to the emergence of this resistance breaker, we performed a comprehensive phylogenetic analysis and genomic comparison of different tobamoviruses, followed by molecular modeling of the viral helicase. The phylogenetic location of the resistance-breaking genes was found to be among host-shifting clades, and this, together with the observation of a relatively low mutation rate, suggests that a host shift contributed to the emergence of this new virus. Our comparative genomic analysis identified twelve potential resistance-breaking mutations in the viral movement protein (MP), the primary target of the related Tm-2 resistance, and nine in its replicase. Finally, molecular modeling of the helicase enabled the identification of three additional potential resistance-breaking mutations.

Role of the Genetic Background in Resistance to Plant Viruses

“…Jaag and Nagy [ 108 ] showed that environmental and host factors could play an important role in viral RNA recombination, one of the major driving forces in RNA virus evolution [ 103 ]. A recent example of the emergence of a resistance-breaking virus that may have resulted from host-switching, is the description of a new resistance-breaking tobamovirus, an Israeli isolate of Tomato brown rugose fruit virus ( ToBRFV), that is able to overcome Tm-2 -mediated resistance in tomato [ 109 ].…”

Effectiveness of disinfectants against the spread of tobamoviruses: Tomato brown rugose fruit virus and Cucumber green mottle mosaic virus

“…A new tobamovirus infecting tomatoes and peppers is Tomato brown rugose fruit virus (ToBRFV), which was recently discovered in 2014-2015 in Jordan [5] and Israel [6]. ToBRFV is considered more virulent than other known tomato-infecting tobamoviruses, as it breaks the popular Tm-2 2 resistance gene which is present in many commercial tomato cultivars [6,7]. ToBRFV outbreaks in greenhouse tomatoes have been reported in countries around the world, including China [8] and Palestine [9] in Asia, Egypt in Africa [10], Germany [11], Greece [12], Italy [13]), Turkey [14] and the United Kingdom [15] in Europe, and Mexico [16,17], the United States [18,19] and Canada [20] in North America.…”

Tomato brown rugose fruit disease: current distribution, knowledge and future prospects

“…There has been some discussion about the possible pathways leading to the emergence of this new virus. A comprehensive phylogenetic analysis and genomic comparison of different tobamoviruses by Maayan et al () concluded that a host‐shifting event (jumping) of the ToBRFV variant occurred with a relatively low mutation rate within a very short time. It is also thought that ToBRFV may have emerged as a result of recombination.…”

“…Most importantly, genomic sequencing of emerging resistance breakers has demonstrated that they can differ by 9-15% from known viruses, for instance, when making comparisons between ToMMV and TMV or ToMV, which may have resulted from the innate mutability of the tobamovirus RNA genome (Domingo & Holland, 1997). In contrast, phylogenetic analysis has shown that the genomic sequence of ToBRFV differs from either ToMV or TMV by 18% and suggests that it could have originated from a common ancestor of ToMV and TMV (Maayan et al, 2018). Salem et al (2016) confirmed the viral causal agent as ToBRFV when a single local lesion taken from an inoculated Nicotiana tabacum 'White Burley' reproduced mosaic symptoms on tomato plants cv.…”