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

Simple Summary The sweetpotato whitefly, Bemisia tabaci, besides causing feeding-related injuries, also transmits the economically devastating tomato yellow leaf curl virus (TYLCV) to tomato plants. The main management options include host resistance and insecticides. Host resistance is imparted against TYLCV and not against the vector. Incorporating host resistance against whiteflies could broaden management options. Acylsugars are secondary metabolites exuded from trichomes of wild solanums that can negatively impact numerous herbivores, including whiteflies. This study examined the effects of acylsugar-producing tomato lines with fatty acid quantitative trait loci introgressions from Solanum pennellii LA716 into cultivated tomato on whitefly preference and fitness, and whitefly-mediated TYLCV inoculation and subsequent TYLCV acquisition. Overall, the acylsugar-producing lines negatively affected whitefly preference and fitness in comparison with the non-acylsugar hybrid. Acylsugars’ mediated antixenosis and antibiosis effects against whiteflies were documented. Acylsugar-producing lines also reduced whitefly-mediated TYLCV inoculation and subsequent TYLCV acquisition by whiteflies in comparison with the non-acylsugar hybrid. These results suggest that acylsugar-mediated resistance against whiteflies could complement already existing TYLCV resistance in tomato cultivars/hybrids and could reduce the heavy reliance on chemical control of whiteflies. Abstract 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.