Aphid Macrosiphum Euphorbiae Research Articles

Wastewater irrigation and Trichoderma colonization in tomato plants: effects on plant traits, antioxidant activity, and performance of the insect pest Macrosiphum euphorbiae

The scarcity of freshwater for agriculture in many regions has led to the application of sewage and saline water for irrigation. Irrigation with non-conventional water sources could become a non-harmful process for plant cultivation, and the effects of their use on crops should be monitored in order to develop optimal management strategies. One possibility to overcome potential barriers is to use biostimulants such as Trichoderma spp. fungi. Tomato is a crop of great economic importance in the world. This study investigated the joint effects of Trichoderma afroharzianum T-22 on tomato plants irrigated with simulated unconventional waters. The experiment consisted of a control and three water treatments. In the control, the plants were watered with distilled water. The three water treatments were obtained by using an irrigation water added with nitrogen, a wastewater effluent, and a mixed groundwater-wastewater effluents. Potted tomato plants (variety Bobcat) were grown in a controlled growth chamber. Antioxidant activity, susceptibility to the aphids Macrosiphum euphorbiae, and tomato plant growth parameters were estimated. Trichoderma afroharzianum T-22 had a positive effect on plant growth and antioxidant defenses when plants were irrigated with distilled water. Instead, no significant morphological effects induced by T. afroharzianum T-22 on plants were observed when unconventional water was used for irrigation. However, inoculation with T. afroharzianum T-22 activated a stress response that made the colonized plants more susceptible to aphid development and increased their fecundity and longevity. Thanks to this study, it may be possible for the first time to open a new discussion on the practical possibility of using reclaimed wastewater for crop irrigation with the addition of a growth-promoting fungal symbiont.

Untangling an insect’s virome from its endogenous viral elements

BackgroundInsects are an important reservoir of viral biodiversity, but the vast majority of viruses associated with insects have not been discovered. Recent studies have employed high-throughput RNA sequencing, which has led to rapid advances in our understanding of insect viral diversity. However, insect genomes frequently contain transcribed endogenous viral elements (EVEs) with significant homology to exogenous viruses, complicating the use of RNAseq for viral discovery.MethodsIn this study, we used a multi-pronged sequencing approach to study the virome of an important agricultural pest and prolific vector of plant pathogens, the potato aphid Macrosiphum euphorbiae. We first used rRNA-depleted RNAseq to characterize the microbes found in individual insects. We then used PCR screening to measure the frequency of two heritable viruses in a local aphid population. Lastly, we generated a quality draft genome assembly for M. euphorbiae using Illumina-corrected Nanopore sequencing to identify transcriptionally active EVEs in the host genome.ResultsWe found reads from two insect-specific viruses (a Flavivirus and an Ambidensovirus) in our RNAseq data, as well as a parasitoid virus (Bracovirus), a plant pathogenic virus (Tombusvirus), and two phages (Acinetobacter and APSE). However, our genome assembly showed that part of the ‘virome’ of this insect can be attributed to EVEs in the host genome.ConclusionOur work shows that EVEs have led to the misidentification of aphid viruses from RNAseq data, and we argue that this is a widespread challenge for the study of viral diversity in insects.

Sugar and pollen supply enhances aphid control by hoverflies in strawberry

Larvae of many hoverfly species (Diptera: Syrphidae) are efficient aphid predators, while the adults feed on pollen and nectar. Strawberry crops can be infested by several aphid species, such as the strawberry aphid Chaetosiphon fragaefolii (Cockerell) and the potato aphid Macrosiphum euphorbiae (Thomas), both of which can cause economic damage. Protected cultivation of strawberry seems to be ideal for introducing biological control agents that depend on flower resources, but the nectar and pollen provided by the crop may not be the most suitable for all flower-dependent insects. In this study, we evaluated the biocontrol potential of hoverflies released preventively or curatively against the potato aphid in strawberry in two separate greenhouse experiments and the effect of adding sugars and pollen on their control efficacy.In the curative experiment, Eupeodes corollae (Fabricius) and Sphaerophoria rueppellii (Wiedemann) were released and supported with flowering plants of Fagopyrum esculentum Moench (buckwheat). Both species reduced the aphid numbers significantly compared to the control treatment.In the preventive experiment, we tested three syrphid species, Episyrphus balteatus (De Geer), S. rueppellii, and E. corollae, in the presence and absence of additional food sources (sugar solution and pollen). All three syrphid species reduced the aphid population to a similar extent, but only in the presence of additional food sources. This study shows that hoverflies perform better in strawberry crops when adults have access to different supplementary food sources.

More than trichomes and acylsugars: the role of jasmonic acid as mediator of aphid resistance in tomato

ABSTRACT This study investigates the impact of priming on the resistance of tomato plants to the potato aphid Macrosiphum euphorbiae, focusing on the role of glandular trichomes. Glandular trichomes are specific hairs that provide protection to tomato plants against herbivorous insects. The experimental priming conducted in this study revealed that prior infestation by Spodoptera littoralis caterpillars increased the plant's resistance against M. euphorbiae, pointing at the jasmonic acid (JA) signaling pathway in regulating this plant-aphid interaction. Glandular trichomes type IV were effective against aphids regardless of the previous infestation. Using JA-deficient tomato (spr2), we observed that M. euphorbiae multiplication increased, while the number of aphids on salicylic -deficient NahG plants was lower than in the wildtype Moneymaker. These findings emphasize the crucial role of the JA signaling pathway in tomato plant resistance to aphids and the importance of glandular trichomes to enhance plant defences against pests.

Wheat as a new host for potato aphid Macrosiphum euphorbiae Thomas (Hemiptera: Aphididae) and construction of its age-stage two-sex life tables.

Wheat (Triticum aestivum L.) is the major global staple food crop that meets the food security demands of various nations across the continents. The recent reduction in wheat production is attributed to several biotic and abiotic factors especially, temperature and rainfall patterns, and pest occurrence. Among insect pests, aphid species are emerging as new pests of economic importance in India and elsewhere. The present investigation identified a new association of Macrosiphum euphorbiae Thomas with the wheat crop. Life table parameters were studied for M. euphorbiae and Rhopalosiphum padi fed on wheat foliage. The total nymphal duration and life cycle duration, respectively, of R. padi (4.76 ± 0.54 and 9.71 ± 1.38days) and M. euphorbiae (5.84 ± 0.69 and 9.96 ± 1.31days) were significantly different for these species. The fecundity of the two aphid species was 23.95 ± 8.67 and 11.6 ± 4.10 progeny/female, respectively. Age-specific survival rate (lx), age-specific fecundity (fx), and population age-specific fecundity (mx) were higher in R. Padi compared to M. euphorbiae. Reproductive value (Vxj) was high in R. padi and the duration of reproduction was less, while these parameters showed an opposite trend in M. euphorbiae. The gross reproduction rate (GRR) was found higher in R. Padi (29.17 offspring/adult lifetime) compared to M. euphorbiae (19.58 offspring/adult lifetime). The M. euphorbiae being a pest of solanaceous crops seems to have shifted to a new host, i.e., wheat. This new adaptation strategy to survive for long periods on a wheat crop might pose a serious threat to wheat crop cultivation in near future.

Sublethal effects of Brevibacillus laterosporus an emerging novel entomopathogenic bacterium with potential role to trigger defense response in chili pepper Capsicum annuum L. against potato aphid Macrosiphum euphorbiae

The emerging elicitor protein PeBL1, extracted from Brevibacillus laterosporus A60, was tested against the potato aphid (Macrosiphum euphorbiae) for its biocontrol potential. Its effects on M. euphorbiae survival, lifespan, immature development, adult reproductive performance, and pest–pathogen interaction were assessed using electrical penetration graphs (EPGs), The levels of jasmonic acid (JA), salicylic acid (SA), and ethylene (ET) were significantly increased in the B. laterosporus-treated C. annuum seedlings, indicating substantial accumulation. Brevibacillus laterosporus improved the height of the C. annuum L. plant and the surface structure of the leaves, by reducing M. euphorbiae reproduction and preventing colonization, according to the findings of this study. The activation of pathways was also part of the defensive response (JA, SA, and ET). The use of B. laterosporus for integrated pest management in the agroecosystem appears to be suitable based on these findings against M. euphorbiae.

Otanical insecticides for pest management in tomato grown in cultivation facilities

Abstract. An alternative to synthetic insecticides is the use of naturally occurring products, such as botanical products with insecticidal properties. Biological testing of the botanical products Krisant EC 750 ml/ha and Neem Azal T/S 0.3% was performed at the Maritza Vegetable Crops Research Institute – Plovdiv to determine their effectiveness against potato aphid (Macrosiphum euphorbiae Thomas, 1878), thrips (Thrips tabaci Lindemanla, 1889; Frankliniella occidentalis Pergande, 1895), greenhouse whitefly (Trialeurodes vaporariorum Westwood, 1856), cotton bollworm (Helicoverpa armigera Hübner, 1808), tomato leaf miner (Tuta absoluta Meyrick, 1917) and two-spotted spider mite (Tetranychus urticae Koch, 1836). These species are some of the most common economically important pests in growing tomatoes in greenhouses. The phytopesticides Neem Azal T/S and Krisant EC were applied alone and in combination. The tested plant protection products showed very good biological activity against these pests and relatively higher effectiveness over 78% shows the combined treatment.

Local adaptation to hosts and parasitoids shape Hamiltonella defensa genotypes across aphid species.

Facultative symbionts are common in insects and can provide their hosts with significant adaptations. Yet we still have a limited understanding of what shapes their distributions, such as why particular symbiont strains are common in some host species yet absent in others. To address this question, we genotyped the defensive symbiont Hamiltonella defensa in 26 aphid species that commonly carry this microbe. We found that Hamiltonella strains were strongly associated with specific aphid species and that strains found in one host species rarely occurred in others. To explain these associations, we reciprocally transferred the Hamiltonella strains of three aphid species, Acyrthosiphon pisum, Macrosiphoniella artemisiae and Macrosiphum euphorbiae, and assessed the impact of Hamiltonella strain on: the stability of the symbiosis, aphid fecundity and parasitoid resistance. We demonstrate that the Hamiltonella strains found in nature are locally adapted to specific aphid hosts, and their ecology: aphids tend to carry Hamiltonella strains that are efficiently transmitted to their offspring, non-lethal, and that provide strong protection against their dominant parasitoid species. Our results suggest that facultative symbiont distributions are shaped by selection from natural enemies, and the host itself, resulting in locally adapted symbioses that provide significant benefits against prevailing natural enemies.

The Effects of Cucumber Mosaic Virus and Its 2a and 2b Proteins on Interactions of Tomato Plants with the Aphid Vectors Myzus persicae and Macrosiphum euphorbiae.

Cucumber mosaic virus (CMV), a major tomato pathogen, is aphid-vectored in the non-persistent manner. We investigated if CMV-induced volatile organic compounds (VOCs) or other virus-induced cues alter aphid–tomato interactions. Y-tube olfactometry showed that VOCs emitted by plants infected with CMV (strain Fny) attracted generalist (Myzus persicae) and Solanaceae specialist (Macrosiphum euphorbiae) aphids. Myzus persicae preferred settling on infected plants (3 days post-inoculation: dpi) at 1h post-release, but at 9 and 21 dpi, aphids preferentially settled on mock-inoculated plants. Macrosiphum euphorbiae showed no strong preference for mock-inoculated versus infected plants at 3 dpi but settled preferentially on mock-inoculated plants at 9 and 21 dpi. In darkness aphids showed no settling or migration bias towards either mock-inoculated or infected plants. However, tomato VOC blends differed in light and darkness, suggesting aphids respond to a complex mix of olfactory, visual, and other cues influenced by infection. The LS-CMV strain induced no changes in aphid–plant interactions. Experiments using inter-strain recombinant and pseudorecombinant viruses showed that the Fny-CMV 2a and 2b proteins modified tomato interactions with Macrosiphum euphorbiae and Myzus persicae, respectively. The defence signal salicylic acid prevents excessive CMV-induced damage to tomato plants but is not involved in CMV-induced changes in aphid–plant interactions.

Genome Size Estimation of Potato Aphid <i>Macrosiphum Euphorbiae</i> using Flow Cytometry

Potato aphid Macrosiphum euphorbiae(Thomas) (Hemiptera: Aphididae) is colonizing species and vector for many economically important potato viruses. There is dearth of genomic information about this economically important aphid species. Hence, to get insight into the genomic architecture, genome size was determined using flow cytometry. The estimated size of M. euphorbiae was 0.53 pg or 519.4 Mbp. The genome size of M. euphorbiae is approximately 2.9, 2.2 and 1.9x larger than that of Drosophila melanogaster, honey bee (Apis mellifera) and mosquito Anopheles gambiae, respectively. The generated genome size information will provide the foundation for futuristic genomic research on M. euphorbiae.

Compositional Analysis and Potent Insecticidal Activity of Supercritical CO2 Fluid Extracts of Alcea nudiflora L. Leaves.

To mitigate potentially severe food shortages due to the exponential growth of the global population, it is of paramount importance to improve the yield and quality of globally harvested food crops. As pest control contributes to both these aspects, the development of safe and effective pesticides is one of the main strategies pursued in this direction in the context of agricultural chemistry. During our investigation of natural pesticides, a supercritical CO2 fluid extract of Alcea nudiflora L. was found to exert extremely potent insecticidal activity against aphids (Macrosiphum euphorbiae) and cowpea seed beetles (Callosobruchus maculatus) with LC50 values of 0.03 mg/mL (24 h exposure, contact method). The facts that their insecticidal activity is in the most potent class among the essential oils known to date, and that the extract did not show any toxicity toward beneficial insects such as ladybugs (Coccinella magnifica) and European honeybees (Apis mellifera Linnaeus), indicate that this extract could be a good, natural, and safe new pesticide candidate. A compositional analysis of this extract was carried out using GC/MS.

Epidermis-Specific Metabolic Engineering of Sesquiterpene Formation in Tomato Affects the Performance of Potato Aphid Macrosiphum euphorbiae

Tomato produces a number of terpenes in their glandular trichomes that contribute to host plant resistance against pests. While glandular trichomes of cultivated tomato Solanum lycopersicum primarily accumulate a blend of monoterpenes, those of the wild tomato species Solanum habrochaites produce various sesquiterpenes. Recently, we have identified two groups of sesquiterpenes in S. habrochaites accessions that negatively affect the performance and choice behavior of the potato aphid (Macrosiphum euphorbiae). Aphids are piercing-sucking herbivores that use their mouthpart to penetrate and probe plant tissues in order to ultimately access vascular tissue and ingest phloem sap. Because secondary metabolites produced in glandular trichomes can affect the initial steps of the aphid feeding behavior, introducing the formation of defensive terpenes into additional plant tissues via metabolic engineering has the potential to reduce tissue penetration by aphids and in consequence virus transmission. Here, we have developed two multicistronic expression constructs based on the two sesquiterpene traits with activity toward M. euphorbiae previously identified in S. habrochaites. Both constructs are composed of sequences encoding a prenyl transferase and a respective S. habrochaites terpene synthase, as well as enhanced green fluorescent protein as a visible marker. All three coding sequences were linked by short nucleotide sequences encoding the foot-and-mouth disease virus 2A self-processing oligopeptide which allows their co-expression under the control of one promoter. Transient expression of both constructs under the epidermis-specific Arabidopsis CER5-promoter in tomato leaves demonstrated that formation of the two sets of defensive sesquiterpenes, β-caryophyllene/α-humulene and (−)-endo-α-bergamotene/(+)-α-santalene/(+)-endo-β-bergamotene, can be introduced into new tissues in tomato. The epidermis-specific transgene expression and terpene formation were verified by fluorescence microscopy and tissue fractionation with subsequent analysis of terpene profiles, respectively. In addition, the longevity and fecundity of M. euphorbiae feeding on these engineered tomato leaves were significantly reduced, demonstrating the efficacy of this novel aphid control strategy.

Biopesticide Evaluation from Lab to Greenhouse Scale of Essential Oils Used against Macrosiphum euphorbiae

Aphids are recognized as a major threat to economically important crops. Their control is predominantly based on synthetic insecticides that are detrimental to human health and the environment. Botanical pesticides based on essential oils (EOs) are a promising alternative. In this study, the entomotoxicity of green anise and fennel EO fumigation was tested on the potato aphid Macrosiphum euphorbiae. Three different settings of increasing scale were considered (leaflet, whole plant and greenhouse) to appraise the consistency of EO impact from controlled laboratory to greenhouse production conditions. LC50 values for green anise and fennel were 6.6 μl L−1air and 12.2 μl L−1air, respectively, based on dose-response curves in leaflet experiments but fennel EO induced phytotoxicity. EO efficiency was confirmed at the whole-plant scale. In the greenhouse experiment, fennel EO exhibited greater efficiency than at the laboratory scale equaling green anise EO efficiency but both EOs showed delayed phytotoxicity, illustrating the importance of long-term monitoring. The present study revealed the ability of both EOs to control M. euphorbiae populations under greenhouse conditions and hinted at the importance of assessing EO efficiency in realistic agronomic conditions (e.g., under the fluctuating environmental conditions usually occurring in greenhouses).

Post-Dropping Behavior of Potato Aphids (Macrosiphum euphorbiae)

Dropping behavior is an effective antipredator defense utilized by many insects including aphids, which drop from plants to lower plant parts or underlying substrates to avoid attack from predatory invertebrates. While research commonly focusses on triggers of dropping, less attention is given to what happens to prey individuals following escape drops. In this study, the duration of tonic immobility, recovery rates, and cases of “instant recovery” (re-clinging to lower plant parts) exhibited by potato aphids (Macrosiphum euphorbiae) that dropped from potted seedlings in response to introduced ladybird (Adalia bipunctata) adults, lacewing (Chrysoperla carnea) larvae, and a standardized tactile stimulus were investigated in relation to a range of environmental factors. Air temperature had a negative correlation with the duration of post-dropping tonic immobility; as temperature increased, time spent motionless decreased. Aphids also showed a pattern of increased recovery rate at higher temperatures. Aphids may be selected to move off the substrate quicker to avoid risks of overheating/desiccation at higher temperatures; and/or higher body temperature facilitates locomotion. Stimulus type also influenced recovery rate back to the original seedling, with aphids generally recovering after the standardized stimulus quicker than after dropping triggered by a real predator. Considering cases of instant recovery onto lower-reaches of the host seedling, seedling height influenced the likelihood of re-clinging, with aphids that managed to instantly recover dropping from, on average, taller seedlings than aphids that dropped to the substrate. Plant architecture could mitigate the costs of dropping for aphids, but further studies quantifying understory foliage cover are needed.

Assessment of potential invasion for six phytophagous quarantine pests in Taiwan

Pest risk assessment is typically performed by expert taxonomists using a pest’s biological data. However, the biological data or expert taxonomists may be difficult to find. Here, we used species distribution modelling to predict potential invasion in which phytophagous quarantine pests survive in Taiwan; the pests (unrecorded yet in Taiwan) included were three notorious quarantine whiteflies (Crenidorsum aroidephagus, Aleurothrixus trachoides, and Paraleyrodes minei) and three aphids (Nasonovia ribisnigri, Macrosiphum euphorbiae, and Viteus vitifoliae). In brief, maximum entropy modelling (MaxEnt) was used to predict the suitability of the pests’ habitats under certain climatic conditions, and then receiver operating characteristic curve analysis was performed (to verify the prediction result). We then analysed environmental variables affecting the habitat suitability and matched them with Taiwan’s crop cultivation areas for the assessment of potential invasion. We observed that the habitat suitability of the cultivation areas of host plants was low for C. aroidephagus, A. trachoides, and N. ribisnigri but was high for the remaining three species. Moreover, precipitation of coldest quarter negatively affected habitat suitability for C. aroidephagus, P. minei, N. ribisnigri, and M. euphorbiae. Seasonal temperature changes also negatively affected the habitat suitability for A. trachoides. This is the first study to demonstrate the use of species distribution modelling as the preliminary step for the pest risk assessment of these emerging pests with limited biological data before their invasion.

Characterization of the detrimental effects of type IV glandular trichomes on the aphid Macrosiphum euphorbiae in tomato

Glandular trichomes are essential in plants' defence against pests however, the mechanisms of action are not completely understood. While there is considerable evidence of feeding and movement impairment by trichomes, the effect on other traits is less clear. We combined laboratory and greenhouse experiments with molecular analysis to understand how glandular trichomes affect the behavior, population growth, and the expression of biomarkers involved in detoxification, primary metabolism, and developmental pathways of the aphid Macrosiphum euphorbiae. We used two isogenic tomato lines that differ in the presence of type IV glandular trichomes and production of acylsucroses; i.e.,Solanum lycopersicum cv. 'Moneymaker' and an introgressed line from Solanum pimpinellifolium (with trichomes type IV). Type IV glandular trichomes affected host selection and aphid proliferation with aphids avoiding, and showing impaired multiplication on the genotype with trichomes. The exposure to type IV glandular trichomes resulted in the overexpression of detoxication markers (i.e., Hsp70, Hsp17, Hsp10); the repression of the energetic metabolism (GAPDH), and the activation of the ecdysone pathway; all these, underlying the key adaptations and metabolic trade-offs in aphids exposed to glandular trichomes. Our results demonstrate the detrimental effect of glandular trichomes (type IV) on the aphid and put forward their mode of action. Given the prevalence of glandular trichomes in wild and cultivated Solanaceae; and of the investigated molecular biomarkers in insects in general, our results provide relevant mechanisms to understand the effect of trichomes not only on herbivorous insects but also on other trophic levels.

Induced Local and Systemic Defense Responses in Tomato Underlying Interactions Between the Root-Knot Nematode Meloidogyne incognita and the Potato Aphid Macrosiphum euphorbiae.

Plants mediate interactions between different herbivores that attack simultaneously or sequentially aboveground (AG) and belowground (BG) organs. The local and systemic activation of hormonal signaling pathways and the concomitant accumulation of defense metabolites underlie such AG-BG interactions. The main plant-mediated mechanisms regulating these reciprocal interactions via local and systemic induced responses remain poorly understood. We investigated the impact of root infection by the root-knot nematode (RKN) Meloidogyne incognita at different stages of its infection cycle, on tomato leaf defense responses triggered by the potato aphid Macrosiphum euphorbiae. In addition, we analyzed the reverse impact of aphid leaf feeding on the root responses triggered by the RKN. We focused specifically on the signaling pathways regulated by the phytohormones jasmonic acid (JA), salicylic acid (SA), abscisic acid (ABA), and indole-3-acetic acid (IAA) as well as steroidal glycoalkaloids as induced defense compounds. We found that aphid feeding did not induce AG hormonal signaling, but it repressed steroidal glycoalkaloids related responses in leaves, specifically when feeding on plants in the vegetative stage. Root infection by the RKN impeded the aphid-triggered repression of the steroidal glycoalkaloids-related response AG. In roots, the RKN triggered the SA pathway during the entire infection cycle and the ABA pathway specifically during its reproduction stage. RKN infection also elicited the steroidal glycoalkaloids related gene expression, specifically when it was in the galling stage. Aphid feeding did not systemically alter the RKN-induced defense responses in roots. Our results point to an asymmetrical interaction between M. incognita and Ma. euphorbiae when co-occurring in tomato plants. Moreover, the RKN seems to determine the root defense response regardless of a later occurring attack by the potato aphid AG.

Drop when the stakes are high: adaptive, flexible use of dropping behaviour by aphids

Abstract For herbivorous insects, dropping from the host plant is a commonly-observed antipredator defence. The use of dropping compared to other behaviours and its timing in relation to contact with a predator was explored in both pea aphids (Acyrthosiphon pisum) and potato aphids (Macrosiphum euphorbiae). Pea aphids dropped more frequently in response to ladybird adults (Adalia bipunctata) than lacewing larvae (Chrysoperla carnea). Potato aphids mainly walked away or backed-up in response to both predator types; but they dropped more frequently relative to other non-walking defences when faced with ladybird adults. Contact with a predator was an important influencer of dropping for both species, and most drops occurred from adjacent to the predator. Dropping appears to be a defence adaptively deployed only when the risk of imminent predation is high; factors that increase dropping likelihood include presence of faster-foraging predators such as adult ladybirds, predator proximity, and contact between aphid and predator.

Glandular Trichome-Derived Mono- and Sesquiterpenes of Tomato Have Contrasting Roles in the Interaction with the Potato Aphid Macrosiphum euphorbiae.

Secondary metabolites produced in glandular trichomes of tomato are involved in interactions with herbivores. In cultivated tomato (Solanum lycopersicum) glandular trichomes accumulate a blend of abundant monoterpenes and smaller amounts of a few sesquiterpenes. These mono- and sesquiterpenes are synthesized by three terpene synthases, TPS20 as well as TPS9 and TPS12, respectively. To study effects of these terpenes on performance and choice behavior of potato aphid (Macrosiphum euphorbiae), we utilized two tomato trichome mutants, hairless and odorless-2, that are differently affected in mono- and sesquiterpene production. Non-choice assays demonstrated that longevity and fecundity of M. euphorbiae were increased when kept on the trichome mutants. A principal component analysis of these aphid performance parameters and terpene production in the trichome mutants indicated that longevity and fecundity of M. euphorbiae were negatively correlated with production of the TPS12-derived sesquiterpenes β-caryophyllene and α-humulene. While we had previously shown that addition of pure β-caryophyllene/α-humulene to an artificial feeding diet affected M. euphorbiae apterae survivorship and feeding behavior, no such effects were observed here upon addition of a mixture of pure TPS20-derived monoterpenes. In olfactometer assays M. euphorbiae alates displayed differential choice behaviors towards the hairless and odorless-2 mutants suggesting a role of TPS20-derived monoterpenes in aphid attraction, which was further confirmed using a mixture of pure monoterpenes. Our analyses revealed contrasting roles of glandular trichome-derived terpenes in S. lycopersicum. While TPS12-derived sesquiterpenes contribute to host plant resistance against M. euphorbiae, TPS20-derived monoterpenes appear to be exploited as cue for host plant orientation by aphids.

Glandular trichome-derived sesquiterpenes of wild tomato accessions (Solanum habrochaites) affect aphid performance and feeding behavior

Glandular trichomes of tomato produce a number of secondary metabolites including terpenes that contribute to host plant resistance against pests. While glandular trichomes of cultivated tomato Solanum lycopersicum primarily accumulate a monoterpene blend, those of wild tomato species like Solanum habrochaites produce various sesquiterpenes. Previous studies have shown that glandular trichome derived terpenes in cultivated and wild tomato species have repellent and toxic activity against multiple biting-chewing herbivores. In contrast, considerably less is known about the effect of these glandular trichome derived terpenes on piercing-sucking herbivores such as aphids. Here, we have screened a collection of S. habrochaites accessions representing five chemotypes that produce distinct sets of sesquiterpenes to identify those affecting the potato aphid (Macrosiphum euphorbiae). Non-choice assays demonstrated that the longevity and fecundity of M. euphorbiae was significantly reduced when kept on the leaf surface of S. habrochaites accessions producing β-caryophyllene and α-humulene, or α-santalene, α-bergamotene, and β-bergamotene, respectively. When M. euphorbiae apterae were feeding on artificial diets with added terpene containing leaf dip extracts, the same β-caryophyllene/α-humulene and α-santalene/α-bergamotene/β-bergamotene producing S. habrochaites accessions were found to affect aphid survivorship and feeding behavior as indicated by gel saliva investment and honeydew production. Olfactometer assays revealed that the sesquiterpenes emitted from these S. habrochaites accessions also have repellent activity against M. euphorbiae alatae affecting their choice behavior prior to landing on host plants. Assays performed with pure sesquiterpene compounds and an introgression line carrying respective S. habrochaites terpene biosynthetic genes in the S. lycopersicum background confirmed that β-caryophyllene/α-humulene and α-santalene/α-bergamotene/β-bergamotene were responsible for the observed effects on performance, feeding and choice behavior of M. euphorbiae.