The amount and chemistry of acylsugars affects sweetpotato whitefly (Bemisia tabaci) oviposition and development, and tomato yellow leaf curl virus incidence, in field grown tomato plants.

The objectives of this study were to ascertain the impact of endogenous production of trichome-exuded acylsugars on insects and insect transmitted virus by evaluating tomato lines and their hybrids bred for acylsugar production under field settings on whiteflies and the whitefly-transmitted tomato yellow leaf curl virus. Specifically, we utilized a diverse array of tomato lines and hybrids bred for changes in acylsugar amount or type, grown in three field trials under natural whitefly and virus pressure, to investigate whether the amount of accumulated acylsugars and or the chemical profile of the acylsugars were associated with greater resistance to whiteflies and reduced incidence of tomato yellow leaf curl virus. There was considerable variation in the abundance of whitefly eggs and nymphs and incidence of tomato yellow leaf curl virus across experiments and between entries. Increasing amount of acylsugars accumulated by the tomato entries was associated with a reduction in the abundance of whitefly eggs and nymphs and a reduction in the incidence of tomato yellow leaf curl virus. Additionally, we identified lines with changes in several acylsugar fatty acids that were associated with decreased abundance of whitefly eggs and nymphs and reduced incidence of tomato yellow leaf curl virus. These results inform the utility of acylsugars as a host plant defense system for improving resistance to whiteflies and their transmitted viruses, with potential for reducing insecticides as a control method for whiteflies and provide breeding targets for optimization of existing acylsugar tomato lines to create lines with the most efficacious amount and chemistry of acylsugars.

Evaluating Acylsugars-Mediated Resistance in Tomato against Bemisia tabaci and Transmission of Tomato Yellow Leaf Curl Virus.

The sweetpotato whitefly, Bemisia tabaci, is a major pest of cultivated tomato. Whitefly feeding-related injuries and transmission of viruses including tomato yellow leaf curl virus (TYLCV) cause serious losses. Management strategy includes planting resistant cultivars/hybrids. However, TYLCV resistance is incomplete and whiteflies on TYLCV-resistant cultivars/hybrids are managed by insecticides. Acylsugars'-mediated resistance against whiteflies has been introgressed from wild solanums into cultivated tomato. This study evaluated acylsugar-producing tomato lines with quantitative trait loci (QTL) containing introgressions from Solanum pennellii LA716, known to alter acylsugars' levels or chemistry. Evaluated acylsugar-producing lines were the benchmark line CU071026, QTL6/CU071026-a CU071026 sister line with QTL6, and three other CU071026 sister lines with varying QTLs-FA2/CU71026, FA7/CU071026, and FA2/FA7/CU071026. Non-acylsugar tomato hybrid Florida 47 (FL47) was also evaluated. Acylsugars' amounts in FA7/CU071026 and FA2/FA7/CU071026 were 1.4 to 2.2 times greater than in other acylsugar-producing lines. Short chain fatty acid, i-C5, was dominant in all acylsugar-producing lines. Long chain fatty acids, n-C10 and n-C12, were more abundant in FA7/CU071026 and FA2/FA7/CU071026 than in other acylsugar-producing lines. Whiteflies preferentially settled on non-acylsugar hybrid FL47 leaves over three out of five acylsugar-producing lines, and whiteflies settled 5 to 85 times more on abaxial than adaxial leaf surface of FL47 than on acylsugar-producing lines. Whiteflies' survival was 1.5 to 1.9 times lower on acylsugar-producing lines than in FL47. Nevertheless, whiteflies' developmental time was up to 12.5% shorter on acylsugar-producing lines than on FL47. TYLCV infection following whitefly-mediated transmission to acylsugar-producing lines was 1.4 to 2.8 times lower than FL47, and TYLCV acquisition by whiteflies from acylsugar-producing lines was up to 77% lower than from FL47. However, TYLCV accumulation in acylsugar-producing lines following infection and TYLCV loads in whiteflies upon acquisition from acylsugar-producing lines were not different from FL47. Combining TYLCV resistance with acylsugars'-mediated whitefly resistance in cultivated tomato could substantially benefit whiteflies and TYLCV management.

A thrips vector of tomato spotted wilt virus responds to tomato acylsugar chemical diversity with reduced oviposition and virus inoculation.

There is increasing evidence that acylsugars deter insect pests and plant virus vectors, including the western flower thrips (WFT), Frankliniella occidentalis (Pergande), vector of tomato spotted wilt virus (TSWV). Acylsugars are sugar-polyesters composed of saturated, un-saturated, and variously branched short and long chain fatty acids (FAs) esterified to a glucose (acylglucose) or sucrose (acylsucrose) moiety. We sought to understand how acylsucrose amount and composition of associated FA profiles interacted to mediate resistance to WFT oviposition and TSWV inoculation on tomato leaves. Towards this goal, we examined WFT oviposition and TSWV inoculation behavior on tomato lines bred to exude varying amounts of acylsucrose in association with diverse FA profiles. Our data show that as acylsucrose amounts increased, WFT egg-laying (oviposition) decreased and TSWV inoculation was suppressed. Western flower thrips also responded to FA profiles that included iC4, iC11, nC12 and nC10 FA. These findings support improving acylsugar-mediated resistance against WFT by breeding tomatoes exuding greater amounts of acylsucrose associated with specific FA profiles. We show that increasing acylsucrose amount output by type IV trichomes and selecting for particular FA profiles through advanced breeding profoundly affects WFT behavior in ways that benefit management of WFT as direct pests and as TSWV vectors.

Acylsugar amount and fatty acid profile differentially suppress oviposition by western flower thrips, Frankliniella occidentalis, on tomato and interspecific hybrid flowers.

Tomatoes (Solanum lycopersicum L.) have been bred to exude higher amounts or different types of the specialized plant metabolites, acylsugars, from type IV trichomes. Acylsugars are known to deter several herbivorous insect pests, including the western flower thrips (WFT), Frankliniella occidentalis (Pergande); however, all previous studies investigated the effect of acylsugars on leaves, or acylsugar extracts obtained from leaves. In spite of the WFT predilection for flowers, there is a gap in knowledge about flower defenses against thrips damage. This is especially important in light of their capacity to acquire and inoculate viruses in the genus Orthotospovirus, such as Tomato spotted wilt orthotospovirus (TSWV), in flowers. Therefore, we turned our attention to assessing thrips oviposition differences on flowers of 14 entries, including 8 interspecific hybrids, 5 tomato lines bred for specific acylsugar-related characteristics (type IV trichome densities, acylsugar amount, sugar moiety and fatty acid profile), and a fresh market tomato hybrid, Mt. Spring, which only produces trace amounts of acylsugars. Our results show that the density of the acylsugar droplet bearing type IV trichomes is greatest on sepals, relative to other flower structures, and accordingly, WFT avoids oviposition on sepals in favor of trichome-sparse petals. In concordance with past studies, acylsugar amount was the most important acylsugar-related characteristic suppressing WFT oviposition. Certain acylsugar fatty acids, specifically i-C5, i-C9 and i-C11, were also significantly associated with changes in WFT oviposition. These results support continued breeding efforts to increase acylsugar amounts and explore modifications of fatty acid profile and their roles in deterring thrips oviposition. The finding that acylsugar production occurs and reduces thrips oviposition in tomato flowers will be important in efforts to use acylsugar-mediated resistance to reduce incidence of orthotospoviruses such as TSWV in tomato by deterring virus transmission and development of thrips vector populations in the crop.

Genetic mapping identifies loci that influence tomato resistance against Colorado potato beetles.

The Colorado potato beetle (CPB; Leptinotarsa decemlineata Say), the most economically important insect pest on potato (Solanum tuberosum L.), also feeds on other Solanaceae, including cultivated tomato (Solanum lycopersicum L.). We used tomato genetic mapping populations to investigate natural variation in CPB resistance. CPB bioassays with 74 tomato lines carrying introgressions of Solanum pennellii in S. lycopersicum cv. M82 identified introgressions from S. pennellii on chromosomes 1 and 6 conferring CPB susceptibility, whereas introgressions on chromosomes 1, 8 and 10 conferred higher resistance. Mapping of CPB resistance using 113 recombinant inbred lines derived from a cross between S. lycopersicum cv UC-204B and Solanum galapagense identified significant quantitative trait loci on chromosomes 6 and 8. In each case, the S. galapagense alleles were associated with lower leaf damage and reduced larval growth. Results of both genetic mapping approaches converged on the same region of chromosome 6, which may have important functions in tomato defense against CPB herbivory. Although genetic mapping identified quantitative trait loci encompassing known genes for tomato acyl sugar and glycoalkaloid biosynthesis, experiments with acyl sugar near-isogenic lines and transgenic GAME9 glycoalkaloid-deficient and overproducing lines showed no significant effect of these otherwise insect-defensive metabolites on CPB performance.