Resistance-Breaking Tomato Spotted Wilt Virus Variant that Recently Occurred in Pepper in South Korea is a Genetic Reassortant

Abstract

Tomato spotted wilt virus (TSWV) is a destructive viral pathogen in various crops, including pepper. While the single dominant gene Tsw has been utilized in pepper breeding to confer resistance to TSWV, the occurrence of TSWV variants that overcome Tsw-mediated resistance has been reported in various countries after several years of growing resistant cultivars. In this study, we determined the complete genome sequence of a resistance-breaking TSWV variant (TSWV-YI) that recently emerged in pepper in South Korea. TSWV-YI infected all the resistant pepper cultivars tested. The phylogenetic and recombination analyses of the complete TSWV-YI genome sequence showed that it is a reassortant that acquired its L and M RNA segments from the existing South Korean TSWV population and its S RNA in an isolate from another country. Given that TSWV-YI is a resistance-breaking variant, it appears that reassortment of the S RNA led to the emergence of this variant that breaks the Tsw gene in pepper grown in South Korea. Our results suggest that resistance-breaking TSWV variants are a potential threat to pepper production in South Korea and that strategies to manage these variants should be developed to ensure sustainable pepper production.

Determinants of Virus Variation, Evolution, and Host Adaptation

“…Based on their fitness or through founder events, variants are selected out of or fixed into viral genomes and virus population structure (Figure 3) [19,41]. Through this process, resistance-breaking virus strains or species with new host ranges or presenting novel symptoms can emerge and lead to epidemics threatening global food security [127,187]. Tomato brown rugose fruit virus (ToBRFV) emerged in 2015 after a recombination event between the major parent, tobacco mosaic virus strain Ohio, and the minor parent, tomato mild mottle virus [86].…”

“…Measuring reassortment and recombination in wild populations remains difficult. However, occasional variants in wild populations emerge with significant economic and evolutionary effects (Tables 1 and 3) [127]. Additionally, reassortment and recombination are commonly seen in phylogenetic and evolutionary studies of virus species over time [85,184] that show that these processes are occurring and shaping the genetic structures of wild virus populations.…”

“…Reassortment has led to the emergence of new viral strains with novel characteristics and biological properties and to the formation of specific clades in the population [85,[145][146][147][148]. Reassortant viruses might be genetically diverse enough to break resistance [85,127], cause novel symptoms [149][150][151], alter host range [152,153], and evolve into new species.…”

Quasispecies Nature of RNA Viruses: Lessons from the Past

“…The fact that segmented viruses consistently evolve within and across families suggests that reassortment benefits viral fitness and evolution. Reassortment results in viruses that might be genetically diverse enough to break resistance [ 29 , 30 ], cause novel symptoms [ 31 , 32 , 33 ], alter host range [ 34 , 35 ], and evolve into new species.…”

Reassortments in single-stranded DNA multipartite viruses: Confronting expectations based on molecular constraints with field observations

“…2003 ) and can be associated with substantial alterations in viral traits, such as hypervirulence ( Chakraborty et al. 2008 ), resistance-breaking ( Kwon et al. 2021 ), or host range expansion ( Idris et al.…”