Characterization of Local and Systemic Impact of Whitefly (Bemisia tabaci) Feeding and Whitefly-Transmitted Tomato Mottle Virus Infection on Tomato Leaves by Comprehensive Proteomics

Abstract

Tomato mottle virus (ToMoV) is a single-stranded DNA (ssDNA) begomovirus transmitted to solanaceous crops by the whitefly species complex (Bemisia tabaci), causing stunted growth, leaf mottling, and reduced yield. Using a genetic repertoire of seven genes, ToMoV pathogenesis includes the manipulation of multiple plant biological processes to circumvent antiviral defenses. To further understand the effects of whitefly feeding and whitefly-transmitted ToMoV infection on tomato plants (Solanum lycopersicum ‘Florida Lanai’), we generated comprehensive protein profiles of leaves subjected to feeding by either viruliferous whiteflies harboring ToMoV, or non-viruliferous whiteflies, or a no-feeding control. The effects of whitefly feeding and ToMoV infection were measured both locally and systemically by sampling either a mature leaf directly from the site of clip-cage confined whitefly feeding, or from a newly formed leaf 10 days post feeding (dpf). At 3 dpf, tomato’s response to ToMoV included proteins associated with translation initiation and elongation as well as plasmodesmata dynamics. In contrast, systemic impacts of ToMoV on younger leaves 10 dpf were more pronounced and included a virus-specific change in plant proteins associated with mRNA maturation and export, RNA-dependent DNA methylation, and other antiviral plant processes. Our analysis supports previous findings and provides novel insight into tomato’s local and systemic response to whitefly feeding and ToMoV infection.

Vector acquisition and co-inoculation of two plant viruses influences transmission, infection, and replication in new hosts

“…To standardize virus populations in these experiments Rhizobacterium tumenfacious infectious clones of TYLCV and ToMoV 63 were used to initiate infections in Solanum lycopersicum L., variety ‘Florida Lanai 64 , 65 (rhizobacterium-inoculated plants); these plants were used for virus acquisition during the AAPs. There were significant differences in the titers of TYLCV and ToMoV DNA-components in rhizobacterium-inoculated plants, but the titers of each viral component reached similar levels in singly and co-infected plants ( P < 0.0001, Supplemental Fig.…”

Establishing an inexpensive, space efficient colony of Bemisia tabaci MEAM1 utilizing modelling and feedback control principles

“…below 10 k). An inoculation with roughly double the initial whiteflies (~200) illustrates the detrimental impact on the plants (Figure 5, Iteration 13; Supplemental Figure S8‐3) that results from the high amplification ratio of whiteflies and systemic stress gene expression that results from whitefly feeding (Ogden et al, 2020).…”

Vector acquisition and co-inoculation of two plant viruses influences transmission, infection, and replication in new hosts

“…To standardize virus populations in these experiments Rhizobacterium tumenfacious infectious clones of TYLCV and ToMoV 63 were used to initiate infections in Solanum lycopersicum L., variety ‘Florida Lanai 64,65 (rhizobacteriuminoculated plants); these plants were used for virus acquisition during the AAPs. There were significant differences in the titers of TYLCV and ToMoV DNA-components in rhizobacteriuminoculated plants, but the titers of each viral component reached similar levels in singly and coinfected plants ( P <0.0001, Supplemental Figure 1).…”

“…Virus-virus interactions occur in specific plant tissues and at specific time points during the infection cycle, but these interactions have both spatial and temporal dimensions that can be altered by virusplant, vector-plant and vector-virus-plant interactions 42,43,65 . In our experimental treatments, temporal differences in transmission of the two viruses would be influenced by the timing and order in which the viruses were acquired from the source plants, the latent period, and whitefly settling behavior.…”

“…Because there is no consistent relationship between order of acquisition and transmission of TYLCV and ToMoV, these results support the hypothesis that vector-virus interactions during acquisition by and/or circulation through the vector influence transmission outcomes. Virus-virus interactions occur in specific plant tissues and at specific time points during the infection cycle, but these interactions have both spatial and temporal dimensions that can be altered by virusplant, vector-plant and vector-virus-plant interactions 42,43,65 . In our experimental treatments, temporal differences in transmission of the two viruses would be influenced by the timing and order in which the viruses were acquired from the source plants, the latent period, and whitefly settling behavior.…”