Impact of Host Resistance to Tomato Spotted Wilt Orthotospovirus in Peanut Cultivars on Virus Population Genetics and Thrips Fitness

Abstract

Thrips-transmitted tomato spotted wilt orthotospovirus (TSWV) is a major constraint to peanut production in the southeastern United States. Peanut cultivars with resistance to TSWV have been widely used for over twenty years. Intensive usage of resistant cultivars has raised concerns about possible selection pressure against TSWV and a likelihood of resistance breakdown. Population genetics of TSWV isolates collected from cultivars with varying levels of TSWV resistance was investigated using five TSWV genes. Phylogenetic trees of genes did not indicate host resistance-based clustering of TSWV isolates. Genetic variation in TSWV isolates and neutrality tests suggested recent population expansion. Mutation and purifying selection seem to be the major forces driving TSWV evolution. Positive selection was found in N and RdRp genes but was not influenced by TSWV resistance. Population differentiation occurred between isolates collected from 1998 and 2010 and from 2016 to 2019 but not between isolates from susceptible and resistant cultivars. Evaluated TSWV-resistant cultivars differed, albeit not substantially, in their susceptibility to thrips. Thrips oviposition was reduced, and development was delayed in some cultivars. Overall, no evidence was found to support exertion of selection pressure on TSWV by host resistance in peanut cultivars, and some cultivars differentially affected thrips fitness than others.

Evaluation of Wild Peanut Species and Their Allotetraploids for Resistance against Thrips and Thrips-Transmitted Tomato Spotted Wilt Orthotospovirus (TSWV)

“…TSWV-induced phenotypes in this study could potentially be influenced by the different isolates (from field-collected foliage). Partial sequencing of TSWV isolates from the last 10 years, including the isolates used in this study, indicated a tremendous amount of variation in sequences in a given spatial scale [ 18 , 48 ]. However, purifying selection seems to be the major factor influencing the population genetics and evolution.…”

“…However, purifying selection seems to be the major factor influencing the population genetics and evolution. Also, isolate effects on the host phenotype were not influenced by host resistance to TSWV [ 18 , 48 ]. Despite using multiple isolates in this study, the phenotype induced by TSWV does not seem to be affected by host resistance in diploids.…”

“…With such a narrow genetic base, there is room for evolution of resistance-breaking variants, as noticed in other crops [ 14 , 52 , 61 ]. Recent research provided no evidence for high levels of host resistance-induced virus selection pressure against TSWV in peanut in Georgia, USA [ 48 ]. However, intense cultivation of peanut in over a million acres in the southeastern United States annually might facilitate the development of resistance-breaking strains in the future.…”

Viral Diseases of Tomato – Origins, Impact, and Future Prospects with a Focus on Tomato Spotted Wilt Virus and Tomato Yellow Leaf Curl Virus

“…There are several examples of multigenic resistance and tolerance that provide long-term stable reductions in pathogen losses. One current example is a multigenic field resistance that appears to be providing long-term durable control of TSWV in peanuts [80]. Sequence-level population analysis of multiple TSWV genes did not detect any resistance-related selection in TSWV populations, indicating that this multigenic resistance is likely to be durable.…”

Characterization of gene expression patterns in response to an orthotospovirus infection between two diploid peanut species and their hybrid

“…The QTLs on A01 alone were responsible for 36% phenotypic variation associated with TSWV resistance, and A09 QTL contribution to TSWV resistance also was significant but not estimated ( Tseng et al., 2016 ; Agarwal et al., 2019 ). Unlike tomato and pepper wherein the selection pressure induced by TSWV has led to resistance-breaking variants, no such resistance-breaking variants have been documented in peanut thus far ( Sundaraj et al., 2014 ; Lai et al., 2021a ). Therefore, it is likely that TSWV resistance in peanut is governed by multiple genes.…”