Glandular trichome-derived sesquiterpenes of wild tomato accessions (Solanum habrochaites) affect aphid performance and feeding behavior Author Wang, Fumin Author Park, Yong-Lak Author Gutensohn, Michael text Phytochemistry 2020 112532 2020-12-31 180 1 11 http://dx.doi.org/10.1016/j.phytochem.2020.112532 journal article 10.1016/j.phytochem.2020.112532 1873-3700 8292694 2.4. Some sesquiterpenes emitted by S. habrochaites have repellent activity against aphids In addition to the observed effects on performance and feeding of M. euphorbiae , sesquiterpenes produced in glandular trichomes of different S. habrochaites accessions upon emission into the surrounding atmosphere could also influence the pre-landing orientation and host plant choice of M. euphorbiae . In order to test the behavioral response of M. euphorbiae alatae towards emitted tomato terpenes we performed choice assays using an open Y-track olfactometer. When the aphids were given the choice between pure air and the odors of tomato leaves ( Fig. 3A ) a significant effect on their behavior was observed only with the S. habrochaites accessions of chemotype 5, but not with any of the other chemotypes. Only 28.3% (χ 2 =8.70, P =0.003) and 32.6% (χ 2 = 5.23, P = 0.022) of M. euphorbiae alatae oriented towards the odors of accession LA1624 and LA2860, respectively, suggesting that the emitted β- caryophyllene and α- humulene (Table S2) have repellent activity. Remarkably, in the same assays ( Fig. 3A ) we observed that 71.8% (χ 2 = 7.41, P = 0.007) and 68.2% (χ 2 = 5.82, P = 0.016) of M. euphorbiae alatae orientated towards the odors from leaves of S. lycopersicum cultivars M82 and Moneymaker, respectively, suggesting that the terpenes emitted from cultivated tomato attracted M. euphorbiae . Fig. 1. Longevity (A) and fecundity (B) of M. euphorbiae apterae arrested on the leaf surface of two S. lycopersicum cultivars and different S. habrochaites accessions. Solanum habrochaites accessions represent five chemotypes characterized by the production of different sesquiterpenes in their glandular trichomes. Values for longevity and fecundity are presented as mean ± SE. Different letters indicate that logarithmic values were significantly different (Tukey’ s HSD test, α = 0.05). Fig. 2. Feeding performance of M. euphorbiae apterae on artificial diets containing leaf dip extracts of S. lycopersicum c.v. M82 and different S. habrochaites accessions (MTBE solvent control). (A) Kaplan-Meier estimates of survivorship and analysis of log-rank test (α =0.05). (B) Box and violin plots represent mean ±SE of gel saliva density (cm 2 ) and the probability density, respectively. (C) Number of honeydew drops accumulated in the feeding chambers. Asterisks in (B) and (C) represent significant differences between diets with leaf dip extracts and control based on Dunnett’ s test (⋅, P < 0.08; *, P < 0.05; **, P < 0.01; ***, P < 0.001). Due to the observed attraction towards S. lycopersicum , in a second set of assays aphid alatae were given the choice between the odor of S. lycopersicum c.v. M82 and different S. habrochaites accessions ( Fig. 3B ). In all but one of the pairs > 50% of the M. euphorbiae alatae were found to orient towards c.v. M82 thus further confirming their attraction by S. lycopersicum odors. When LA1779, LA1624, and LA2860 were paired with c.v. M82 only 32.4% (χ 2 =4.24, P =0.040), 30.2% (χ 2 = 6.72, P = 0.010), and 30.0% (χ 2 = 6.40, P = 0.011) of the M. euphorbiae alatae, respectively, oriented towards the S. habrochaites odors, indicating a significant repellent activity of the sesquiterpenes emitted by the accessions of the chemotypes 4 and 5 (Table S2). An additional set of assays was performed to test if these sesquiterpenes produced by S. habrochaites could be transferred to cultivated tomato and would show a similar repellent activity towards M. euphorbiae in the presence of the monoterpene blend emitted by S. lycopersicum . Macrosiphum euphorbiae alatae were given the choice between the odors of S. lycopersicum c.v. M82 leaves alone, and c.v. M82 leaves to which aliquots of S. habrochaites leaf dip extracts on filter papers had been added ( Fig. 3C ). The addition of the S. habrochaites leaf dip extracts in general affected the orientation of M. euphorbiae alatae towards c.v. M82 leaves. However, only the addition of the β- caryophyllene and α- humulene containing extracts from accessions LA1624 and LA2860 significantly reduced the attraction of M. euphorbiae with only 33.3% (χ2 = 4.67, P =0.031) and 34.8% (χ2 = 4.26, P = 0.039), respectively, of the aphids orienting towards the mixed odors of c.v. M82 leaves and added leaf dip extracts. A similar trend was observed upon the addition of extracts from accession LA1779 (chemotype 4) to c.v. M82 leaves which resulted in only 35.0% (χ2 = 3.60, P = 0.058) of M. euphorbiae orienting towards the mixed odors. In summary, the results of the olfactometer choice assays suggested that the sesquiterpenes produced in glandular trichomes of S. habrochaites chemotypes 4 and 5 not only affect performance and feeding of M. euphorbiae but clearly also their choice behavior prior to landing on potential host plants.