蚜虫唾液蛋白研究进展

蚜虫属于半翅目蚜科,多为重要的农业害虫,通过刺吸式口器吸食植物汁液,传播病毒,其爆发常常造成重大经济损失。在漫长的协同进化历程中,植物建立了高效的防御系统以应对蚜虫威胁。为了克服植物的防御反应,蚜虫也发展了相应的反制手段,其中蚜虫在取食过程中分泌的唾液蛋白能调控植物防御反应,降解植物次生物质,从而在蚜虫与植物互作中发挥着至关重要的作用。本文综述了蚜虫唾液蛋白的组分鉴定方法和相关蛋白的功能,并对唾液蛋白在蚜虫防治的应用和今后的研究方向进行了展望。常见的蚜虫唾液蛋白组分的鉴定和分析方法包括唾液蛋白的酶活性分析、唾液蛋白组学分析、唾液腺转录组学和蛋白组学分析等。但这些方法各有利弊,仅采取一种分析方法不能客观全面地反映蚜虫唾液蛋白分泌谱,多种技术手段联合分析方可提供更为逼真详实的信息。蚜虫唾液蛋白种类繁多,可分为解毒酶、保护酶、水解酶、结合功能蛋白以及分类未知的效应蛋白等。蚜虫唾液蛋白功能多样,能参与唾液鞘的形成,诱导植物防御反应,促进蚜虫取食,提高蚜虫繁殖力等。通过RNAi干扰唾液蛋白编码基因会显著改变蚜虫取食行为,并降低蚜虫存活率、产蚜量和适合度。因此,唾液蛋白是防控蚜虫的理想靶标。目前,采用寄主诱导的基因沉默(host-induced gene silencing, HIGS)技术已培育了数种靶向唾液蛋白基因的高效抗蚜作物品系,展示出了良好的应用前景。从目前研究来看,各种蚜虫唾液蛋白谱急需采用多组学手段联合分析的方法来进行完整解析。各种唾液蛋白的具体功能方面的研究还严重缺乏,需从蚜虫、植物、两者之间的互作等多维度探究唾液蛋白的作用及相关的分子机制,为发展基于蚜虫唾液蛋白调控的蚜虫防治新策略打下基础。     

Insight into watery saliva proteomes of the grain aphid,Sitobion avenae

The grain aphid, Sitobion avenae, is an economically important cereal pest worldwide. Aphid saliva plays an essential role in the interaction between aphids and their host plants. However, limited information is available regarding the proteins found in the saliva of S. avenae. Here, the watery saliva proteins from S. avenae were collected in an artificial diet and identified using a liquid chromatography–mass spectrometry/mass spectrometry analysis. A total of 114 proteins were identified in S. avenae saliva, including several enzymes, binding proteins, and putative effectors, as well as other proteins with unknown functions. In comparison with salivary proteins from nine other aphid species, the most striking feature of the salivary protein from S. avenae was the different patterns of protein functions. Several orthologous proteins secreted by other aphid species such as glucose dehydrogenase, elongation factors, and effector C002 were also detected in S. avenae saliva and speculated to play a significant role in aphid–plant interactions. These results provide further insight into the molecular basis between aphids and cereal plant interactions.     

The impact of Meu1-mediated resistance in tomato on longevity, fecundity and behavior of the potato aphid, Macrosiphum euphorbiae

The effect of the tomato resistance gene, Meu1, on feeding, longevity, fecundity and developmental rate of the pink biotype of the potato aphid, Macrosiphum euphorbiae (Thomas) (Hemiptera, Aphididae), was determined using nearly isogenic tomato (Lycopersicon esculentum Mill, Solanaceae) lines. Aphid mortality was significantly higher on resistant plants, with 60% of the aphids dying by the 4th day of exposure. By the 10th day, all the aphids on the resistant plants were dead whereas 100% of the aphids on susceptible plants were alive. Meu1-mediated resistance resulted in significantly decreased fecundity with a ten-fold decrease in the net fertility rate (4.5 and 45.7 progeny per aphid on resistant and susceptible tomato, respectively). A qualitative analysis showed that honeydew was produced by aphids on resistant and susceptible plants, suggesting that aphids initiate feeding on both plant types. However, significantly lower quantities of honeydew were present when aphids were caged on resistant plants. There were also significant differences in aphid location on resistant and susceptible leaves. Experiments evaluating behavior in less than 24 h showed that aphids left resistant leaves after relatively short exposure (3–6 h). Aphids transferred from resistant to susceptible tomato at intervals between 3 h and 24 h resumed feeding as evidenced by presence of honeydew. Although the mechanism by which Meu1-mediated resistance operates is not yet known, our data suggest that resistance factors act rapidly after initiation of feeding and that lower fecundity and longevity are related to reduction in aphid feeding.     

Loss of function of FATTY ACID DESATURASE7 in tomato enhances basal aphid resistance in a salicylate-dependent manner

We report here that disruption of function of the ω-3 FATTY ACID DESATURASE7 (FAD7) enhances plant defenses against aphids. The suppressor of prosystemin-mediated responses2 (spr2) mutation in tomato (Solanum lycopersicum), which eliminates the function of FAD7, reduces the settling behavior, survival, and fecundity of the potato aphid (Macrosiphum euphorbiae). Likewise, the antisense suppression of LeFAD7 expression in wild-type tomato plants reduces aphid infestations. Aphid resistance in the spr2 mutant is associated with enhanced levels of salicylic acid (SA) and mRNA encoding the pathogenesis-related protein P4. Introduction of the Naphthalene/salicylate hydroxylase transgene, which suppresses SA accumulation, restores wild-type levels of aphid susceptibility to spr2. Resistance in spr2 is also lost when we utilize virus-induced gene silencing to suppress the expression of NONEXPRESSOR OF PATHOGENESIS-RELATED PROTEINS1 (NPR1), a positive regulator of many SA-dependent defenses. These results indicate that FAD7 suppresses defenses against aphids that are mediated through SA and NPR1. Although loss of function of FAD7 also inhibits the synthesis of jasmonate (JA), the effects of this desaturase on aphid resistance are not dependent on JA; other mutants impaired in JA synthesis (acx1) or perception (jai1-1) show wild-type levels of aphid susceptibility, and spr2 retains aphid resistance when treated with methyl jasmonate. Thus, FAD7 may influence JA-dependent defenses against chewing insects and SA-dependent defenses against aphids through independent effects on JA synthesis and SA signaling. The Arabidopsis (Arabidopsis thaliana) mutants Atfad7-2 and Atfad7-1fad8 also show enhanced resistance to the green peach aphid (Myzus persicae) compared with wild-type controls, indicating that FAD7 influences plant-aphid interactions in at least two plant families.     

Impact of chemical elicitor applications on greenhouse tomato plants and population growth of the green peach aphid, Myzus persicae

Recent advances in the understanding of plant signaling pathways have opened the way for using elicitor‐induced plant resistance as a tactic for protecting plants against arthropod pests. Four common elicitors of induced responses in tomato, Lycopersicon esculentum Mill. (Solanaceae), were evaluated with regard to phytotoxicity, induction of plant defensive proteins, and effects on population growth and fecundity of a common pest, the green peach aphid, Myzus persicae (Sulzer) (Homoptera: Aphididae). Ethephon and methyl jasmonate (MJ) treatments caused varying degrees of phytotoxicity. Ethephon caused pronounced changes in plant growth form and severe, dose‐dependent negative impacts on plant growth and flowering. Effects with MJ were milder, but still caused temporary inhibition of development, leading to smaller plants and delayed flowering. The commercial elicitors benzothiadiazole (BTH) and harpin did not cause detectable phytotoxicity. The highest doses of ethephon and MJ significantly increased leaf peroxidase (POD) levels but only MJ treatments significantly increased polyphenol oxidase (PPO) levels. BTH and harpin had no detectable effects on POD and PPO. Populations of green peach aphids grew significantly more slowly on plants treated with BTH or MJ than on control plants or plants treated with harpin or ethephon. Slowed aphid population growth on BTH‐treated plants was due to significant reductions in aphid fecundity, although this was independent of changes in time to onset of reproduction or time to death. Aphid fecundity was also reduced on MJ‐treated plants relative to controls, but this difference was not statistically significant, suggesting that other mechanisms are involved in slowing aphid population growth on MJ‐treated plants. Growth of aphid populations on plants treated with a MJ–BTH mixture was reduced almost as much as with treatments of MJ alone, suggesting that antagonism between JA‐dependant and SA‐dependent plant signaling pathways is only mild with regard to induced defenses against aphids.     

Salicylic acid-mediated reductions in yield in Nicotiana attenuata challenged by aphid herbivory

Aphid herbivory decreases primary production in natural ecosystems and reduces crop yields. The mechanism for how aphids reduce yield is poorly understood as some studies suggest aphid feeding directly impedes photosynthesis, whereas other studies suggest a change in allocation of resources from growth to defense compounds reduces yield. To determine the mechanisms underlying reduced plant growth by aphids, Nicotiana attenuata plants, native tobacco, were infested with Myzus persicae ssp. nicotianae, tobacco-adapted green peach aphids, at low and high densities, and plant performance including fitness was assessed. To test the direct defense capacity of salicylic acid (SA) on aphid performance, we fed aphids an artificial diet with varying levels of SA and measured their survivorship and fecundity. There was no detectable effect of aphid herbivory on net photosynthesis, yet herbivory reduced plant growth, final biomass (43 % at high aphid density), and seed set (18 % at high aphid density) at both low and high aphid infestation levels. High-density aphid attack during the rosette and flowering stage caused an increase in SA levels, but caused only a transient decrease in jasmonic acid concentration at low aphid density. SA concentrations similar to those found in infested flowering plants decreased aphid fecundity, suggesting that SA was an effective chemical defense response against aphids. These results suggest that as aphid densities increased the proximal cause of reduced growth and yield was not reduced photosynthesis, but instead resources may have been mobilized for defense via the SA pathway, decreasing the availability of resources for building plant biomass.     

Shaping the understanding of saliva-derived effectors towards aphid colony proliferation in host plant

‘Effectors’ are proteins and/or small molecules that originated from aphid saliva gland and its secretion is initiated due to interaction between host and insect. The effectors have the ability to manipulate the host cell structure as well as function similar to pathogen’s effectors. Like pathogen’s effectors, aphid effectors suppress the hosts’ defense responses as well as hosts’ defense induction or both. In the susceptible interaction with the host, aphid effectors alter plant processes that contribute to the establishment of compatibility that promotes aphid proliferation. In the susceptible reaction with the host, aphid effectors contribute to the successful salivation and sustainability of the sieve element sap ingestion that have promoting role in more aphid proliferation. In the resistant interaction with the host, aphid effectors are recognized by the typical plant receptors and elicit the induction the effective defense response. As a result, aphid proliferation is reduced due to reduced compatibility establishment in the resistant host. This review focuses on the exciting progress in aphid effector biology that insights new perspective in the molecular basis of plant–aphid interactions.     

Relative suitability of crested wheatgrass and other perennial grass hosts for the Russian wheat aphid (Homoptera: Aphididae)

The Russian wheat aphid, Diuraphis noxia (Mordvilko) (Homoptera: Aphididae), reproduces parthenogenetically in North America and must survive year-round on host plants, including in late summer when small grains are not in cultivation. During this time, cool-season perennial wheatgrasses (Poaceae: Triticeae) contribute substantially to aphid survival, crested wheatgrass (Agropyron spp.) particularly. In greenhouse studies, the number of aphids per plant was measured after four infestation periods on unvernalized and vernalized wheatgrasses. Before placement on these test plant species, aphids were reared either on winter wheat or on the grass host species on which aphid progeny were counted. On vernalized plants, aphids reared on wheat resulted in more aphids per test plant than when the aphids were reared on wheatgrasses, but on unvernalized plants the number of aphids per test plant did not differ significantly regardless of rearing host. Aphids on crested wheatgrass were similar in number to the other grasses when plants were unvernalized. However, when plants were vernalized, crested wheatgrass supported significantly more aphids than some of the other hosts. Aphid numbers increased on all test species as infestation period lengthened, and plant growth was largely unaffected by aphid feeding. These results suggest if sufficient moisture is available during summer when small grains are not in cultivation, all host species observed are capable of sustaining aphids. Crested wheatgrass is an abundant and important host of the Russian wheat aphid in its northern range of the western United States, but other less prevalent wheatgrasses also may contribute to aphid survival during late summer when small grains are not in cultivation.     

Proteins Identified from Saliva and Salivary Glands of the Chinese Gall Aphid Schlechtendalia chinensis

Aphid saliva plays an essential role in the interaction between aphids and their host plants. Several aphid salivary proteins have been identified but none from galling aphids. Here the salivary proteins from the Chinese gall aphid are analyzed, Schlechtendalia chinensis, via an LC‐MS/MS analysis. A total of 31 proteins are identified directly from saliva collected via an artificial diet, and 141 proteins are identified from extracts derived from dissected salivary glands. Among these identified proteins, 17 are found in both collected saliva and dissected salivary glands. In comparison with salivary proteins from ten other free‐living Hemipterans, the most striking feature of the salivary protein from S. chinensis is the existence of high proportion of proteins with binding activity, including DNA‐, protein‐, ATP‐, and iron‐binding proteins. These proteins maybe involved in gall formation. These results provide a framework for future research to elucidate the molecular basis for gall induction by galling aphids.     

Comparisons of salivary proteins from five aphid (Hemiptera: Aphididae) species

Aphid (Hemiptera: Aphididae) saliva, when injected into host plants during feeding, causes physiological changes in hosts that facilitate aphid feeding and cause injury to plants. Comparing salivary constituents among aphid species could help identify which salivary products are universally important for general aphid feeding processes, which products are involved with specific host associations, or which products elicit visible injury to hosts. We compared the salivary proteins from five aphid species, namely, Diuraphis noxia (Kurdjumov), D. tritici (Gillette), D. mexicana (Baker), Schizaphis graminum (Rondani), and Acyrthosiphon pisum (Harris). A 132-kDa protein band was detected from the saliva of all five species using sodium dodecyl sulfate polyacrylamide gel electrophoresis. Alkaline phosphatase activity was detected from the saliva of all five species and may have a universal role in the feeding process of aphids. The Diuraphis species cause similar visible injury to grass hosts, and nine electrophoretic bands were unique to the saliva of these three species. S. graminum shares mutual hosts with the Diuraphis species, but visible injury to hosts caused by S. graminum feeding differs from that of Diuraphis feeding. Only two mutual electrophoretic bands were visualized in the saliva of Diuraphis and S. graminum. Ten unique products were detected from the saliva of A. pisum, which feeds on dicotyledonous hosts. Our comparisons of aphid salivary proteins revealed similarities among species which cause similar injury on mutual hosts, fewer similarities among species that cause different injury on mutual hosts, and little similarity among species which feed on unrelated hosts.     

Infection with an insect virus affects olfactory behaviour and interactions with host plant and natural enemies in an aphid

Aphid ecology and population dynamics are affected by a series of factors including behavioural responses to ecologically relevant chemical cues, capacity for population growth, and interactions with host plants and natural enemies. Using the aphid Rhopalosiphum padi (L.) (Homoptera: Aphididae), we showed that these factors were affected by infection with Rhopalosiphum padi virus (RhPV). Uninfected aphids were attracted to odour of uninfected aphids on the host plant, an aggregation mechanism. However, infected aphids were not attracted, and neither infected nor uninfected aphids were attracted to infected aphids on the plant. Infected aphids did not respond to methyl salicylate, a cue denoting host suitability. Infected aphids were more behaviourally sensitive to aphid alarm pheromone, and left the host plant more readily in response to it. RhPV reduced the lifespan and population growth rate of the aphid. The predacious ladybird, Coccinella septempunctata (L.) (Coleoptera: Coccinellidae), consumed more infected aphids than uninfected aphids in a 24‐h period, and the aphid parasitoid Aphidius ervi Haliday (Hymenoptera: Aphidiidae) attacked more infected than uninfected aphids. However, the proportion of mummies formed was lower with infected aphids. The results represent further evidence that associated organisms can affect the behaviour and ecology of their aphid hosts.     

The NIa‐Pro protein of Turnip mosaic virus improves growth and reproduction of the aphid vector,Myzus persicae (green peach aphid)

Many plant viruses depend on aphids and other phloem‐feeding insects for transmission within and among host plants. Thus, viruses may promote their own transmission by manipulating plant physiology to attract aphids and increase aphid reproduction. Consistent with this hypothesis, Myzus persicae (green peach aphids) prefer to settle on Nicotiana benthamiana infected with Turnip mosaic virus (TuMV) and fecundity on virus‐infected N. benthamiana and Arabidopsis thaliana (Arabidopsis) is higher than on uninfected controls. TuMV infection suppresses callose deposition, an important plant defense, and increases the amount of free amino acids, the major source of nitrogen for aphids. To investigate the underlying molecular mechanisms of this phenomenon, 10 TuMV genes were over‐expressed in plants to determine their effects on aphid reproduction. Production of a single TuMV protein, nuclear inclusion a‐protease domain (NIa‐Pro), increased M. persicae reproduction on both N. benthamiana and Arabidopsis. Similar to the effects that are observed during TuMV infection, NIa‐Pro expression alone increased aphid arrestment, suppressed callose deposition and increased the abundance of free amino acids. Together, these results suggest a function for the TuMV NIa‐Pro protein in manipulating the physiology of host plants. By attracting aphid vectors and promoting their reproduction, TuMV may influence plant–aphid interactions to promote its own transmission.     

Effect of plant nutrition on aphid size,prey consumption,and life history characteristics of green lacewing

Plant quality can directly and indirectly affect the third trophic level. The predation by all the instars of green lacewing, Chrysoperla carnea （S.） （Neuroptera： Chrysopidae） on the cereal aphids, Rhopalosiphum padi （L.）, and Sitobion avenae （F.） at varying nitrogen fertilizer levels was calculated under laboratory conditions. Wheat plants were grown on four nitrogen fertilizer levels and aphids were fed on these plants and subsequently offered as food to the C. carnea. Aphid densities of 10, 30, and 90 were offered to first, second, and third instar larvae of green lacewing. Increased nitrogen application improved nitrogen contents of the plants and also the body weight of cereal aphids feeding on them. Aphid consumption by green lacewings was reduced with the increase in nitrogen content in the host plants of aphids. Predation of both aphid species by first, second, and third instars larvae of C. carnea was highest on aphids reared on plants with the lowest rate of fertilization, suggesting a compensatory consumption to overcome reduced biomass （lower aphid size）. Total biomass devoured by C. carnea on all nitrogen fertilizer treatments was not statistically different. Additionally, the heavier host prey influenced by the plant nutrition had an effect on the life history characteristics of green lacewings. The larval duration, pupal weight, pupal duration, fecundity, and male and female longevity were significantly affected by the level of nitrogen fertilization to the aphid＇s host plants, except for pupal duration when fed on S. avenae. This study showed that quantity of prey supplied to the larvae affects the prey consumption and thereafter the life history characteristics of green lacewings.     

Proteomic profiling of aphid Macrosiphum euphorbiae responses to host-plant-mediated stress induced by defoliation and water deficit

Abiotic and biotic host-plant stress, such as desiccation and herbivory, may strongly affect sap-sucking insects such as aphids via changes in plant chemicals of insect nutritional or plant defensive value. Here, we examined (i) water deprivation and (ii) defoliation by the beetle Leptinotarsa decemlineata as stresses indirectly affecting the aphid Macrosiphum euphorbiae via its host plant Solanum tuberosum. For plant-induced stress, aphids were reared on healthy vs. continuously stressed potato for 14 days (no watering; defoliation maintained at approximately 40%). Aphid performance under stress was correlated with metabolic responses monitored by profiling of the aphid proteome. M. euphorbiae was strongly affected by water stress, as adult survival, total aphid number and biomass were reduced by 67%, 64%, and 79%, respectively. Aphids performed normally on defoliated potato, indicating that they were unaffected or able to compensate any stress induced by plant defoliation. Stressed aphid proteomes revealed 419-453 protein spots, including 27 that were modulated specifically or jointly under each kind of host-plant stress. Reduced aphid fitness on water-stressed plants mostly correlated with modulation of proteins involved in energy metabolism, apparently to conserve energy in order to prioritize survival. Despite normal performance, several aphid proteins that are known to be implicated in cell communication were modulated on defoliated plants, possibly suggesting modified aphid behaviour. The GroEL protein (or symbionin) of the endosymbiont Buchnera aphidicola was predominant under all conditions in M. euphorbiae. Its expression level was not significantly affected by aphid host-plant stresses, which is consistent with the high priority of symbiosis in stressed aphids.     

Genetics coupled to quantitative intact proteomics links heritable aphid and endosymbiont protein expression to circulative polerovirus transmission

Yellow dwarf viruses in the family Luteoviridae, which are the causal agents of yellow dwarf disease in cereal crops, are each transmitted most efficiently by different species of aphids in a circulative manner that requires the virus to interact with a multitude of aphid proteins. Aphid proteins differentially expressed in F2 Schizaphis graminum genotypes segregating for the ability to transmit Cereal yellow dwarf virus-RPV (CYDV-RPV) were identified using two-dimensional difference gel electrophoresis (DIGE) coupled to either matrix-assisted laser desorption ionization-tandem mass spectrometry or online nanoscale liquid chromatography coupled to electrospray tandem mass spectrometry. A total of 50 protein spots, containing aphid proteins and proteins from the aphid's obligate and maternally inherited bacterial endosymbiont, Buchnera, were identified as differentially expressed between transmission-competent and refractive aphids. Surprisingly, in virus transmission-competent F2 genotypes, the isoelectric points of the Buchnera proteins did not match those in the maternal Buchnera proteome as expected, but instead they aligned with the Buchnera proteome of the transmission-competent paternal parent. Among the aphid proteins identified, many were involved in energy metabolism, membrane trafficking, lipid signaling, and the cytoskeleton. At least eight aphid proteins were expressed as heritable, isoelectric point isoform pairs, one derived from each parental lineage. In the F2 genotypes, the expression of aphid protein isoforms derived from the competent parental lineage aligned with the virus transmission phenotype with high precision. Thus, these isoforms are candidate biomarkers for CYDV-RPV transmission in S. graminum. Our combined genetic and DIGE approach also made it possible to predict where several of the proteins may be expressed in refractive aphids with different barriers to transmission. Twelve proteins were predicted to act in the hindgut of the aphid, while six proteins were predicted to be associated with the accessory salivary glands or hemolymph. Knowledge of the proteins that regulate virus transmission and their predicted locations will aid in understanding the biochemical mechanisms regulating circulative virus transmission in aphids, as well as in identifying new targets to block transmission.     

Cauliflower mosaic virus protein P6-TAV plays a major role in alteration of aphid vector feeding behaviour but not performance on infected Arabidopsis

Emerging evidence suggests that viral infection modifies host plant traits that in turn alter behaviour and performance of vectors colonizing the plants in a way conducive for transmission of both nonpersistent and persistent viruses. Similar evidence for semipersistent viruses like cauliflower mosaic virus (CaMV) is scarce. Here we compared the effects of Arabidopsis infection with mild (CM) and severe (JI) CaMV isolates on the feeding behaviour (recorded by the electrical penetration graph technique) and fecundity of the aphid vector Myzus persicae. Compared to mock-inoculated plants, feeding behaviour was altered similarly on CM- and JI-infected plants, but only aphids on JI-infected plants had reduced fecundity. To evaluate the role of the multifunctional CaMV protein P6-TAV, aphid feeding behaviour and fecundity were tested on transgenic Arabidopsis plants expressing wild-type (wt) and mutant versions of P6-TAV. In contrast to viral infection, aphid fecundity was unchanged on all transgenic lines, suggesting that other viral factors compromise fecundity. Aphid feeding behaviour was modified on wt P6-CM-, but not on wt P6-JI-expressing plants. Analysis of plants expressing P6 mutants identified N-terminal P6 domains contributing to modification of feeding behaviour. Taken together, we show that CaMV infection can modify both aphid fecundity and feeding behaviour and that P6 is only involved in the latter.     

The effect of rearing history and aphid density on volatile‐mediated foraging behaviour of Diaeretiella rapae

1. Parasitoid females foraging for hosts rely on cues derived from the insect host, the host plant and/or their interaction, and all of these can be learned during the immature and adult stages. 2. The present study investigated the importance of rearing history on foraging behaviour of Diaeretiella rapae, an endoparasitoid often associated with aphids feeding on brassicaceous plant species. 3. Parasitoids were reared on one of the four possible combinations, comprising two brassicaceous host plant species, Brassica nigra or Raphanus sativus, and two aphid species Brevicoryne brassicae or Myzus persicae. These parasitoids were tested in a Y‐tube olfactometer and given the choice between volatiles emitted by an aphid‐infested plant (25 or 100 aphids per plant) and an uninfested control plant. The parasitoid's responses were compared when offered: (i) the same plant–aphid combination as the one on which it had been reared; (ii) the same host plant infested with the alternative aphid species; or (iii) an alternative plant with the alternative aphid species. 4. Aphid density did affect the behavioural responses to the various odour sources, but rearing history did not. Diaeretiella rapae only preferred aphid‐induced to non‐induced plant volatiles at low aphid infestation level, whereas they did not discriminate between volatiles at high aphid infestation level. 5. It is concluded that aphid‐induced volatiles of brassicaceous plants play an important role during host habitat location, but seem less important for parasitoids to locate the aphid host itself. The data are discussed in the light of manipulation of host plant defences by aphids.