Research Article: Identification and Expression Profiling of Odorant Binding Proteins and Chemosensory Proteins between Two Wingless Morphs and a Winged Morph of the Cotton Aphid Aphis gossypii Glover

Date Published: September 20, 2013

Publisher: Public Library of Science

Author(s): Shao-Hua Gu, Kong-Ming Wu, Yu-Yuan Guo, Linda M. Field, John A. Pickett, Yong-Jun Zhang, Jing-Jiang Zhou, Thomas L. Wilkinson.


Insects interact with their environment and respond to the changes in host plant conditions using semiochemicals. Such ecological interactions are facilitated by the olfactory sensilla and the use of olfactory recognition proteins. The cotton aphid Aphis gossypii can change its phenotype in response to ecological conditions. They reproduce mainly as wingless asexual morphs but develop wings to find mates or new plant hosts under the influence of environmental factors such as temperature, plant nutrition and population density. Two groups of small soluble proteins, odorant binding proteins (OBPs) and chemosensory proteins (CSPs) are believed to be involved in the initial biochemical recognition steps in semiochemical perception. However, the exact molecular roles that these proteins play in insect olfaction remain to be discovered. In this study, we compared the transcriptomes of three asexual developmental stages (wingless spring and summer morphs and winged adults) and characterised 9 OBP and 9 CSP genes. The gene structure analysis showed that the number and length of introns in these genes are much higher and this appears to be unique feature of aphid OBP and CSP genes in general. Another unique feature in aphids is a higher abundance of CSP transcripts than OBP transcripts, suggesting an important role of CSPs in aphid physiology and ecology. We showed that some of the transcripts are overexpressed in the antennae in comparison to the bodies and highly expressed in the winged aphids compared to wingless morphs, suggesting a role in host location. We examined the differential expression of these olfactory genes in ten aphid species and compared the expression profile with the RNA-seq analyses of 25 pea aphid transcriptome libraries hosted on AphidBase.

Partial Text

Insects use sensitive olfactory systems to detect airborne chemicals from the environment and to find preferred hosts, mates and oviposition sites [1-4]. The sap-sucking aphids are destructive pests of many economically important crops throughout the world. Like other insects, aphids use chemical molecules such as species-specific pheromones and plant volatiles to interact with each other, host plants and to react to changes in their environment. Mature sexual females of many aphid species release a mixture of two iridoids (4aS, 7S, 7aR)-nepetalactone and (1R, 4aS, 7S, 7aR)-nepetalactol which act as sex pheromones to attract conspecific males [5,6]. Another semiochemical which is widely used by most aphid species is the alarm pheromone (E)-β-farnesene which warns neighbouring aphids of attacks and overcrowding [7,8]. (E) -β-farnesene is also used as a foraging cue for many of the aphids’ natural enemies [6,8]. Many plants release (E)-β-farnesene as a component of their essential oils. To avoid responding to this compound when not released by aphids, there are specific olfactory neurons co-located with (E)-β-farnesene neurons, for other sesquiterpenes such as (1R,4E,9S)-caryophyllene in aphids [9,10] and also in the typical aphid predators Coccinellaseptempunctata [11]. The combinatory actions of these neurons in aphids allow them to discriminate (E)-β-farnesene released by plants and aphids. Plants release aphid-induced defence volatiles to attract aphid predators and parasitoids [12,13]. Aphids use plant volatiles to locate suitable hosts and to avoid unfavourable plants by detecting chemical signals emitted by plants in response to aphid feeding and nutrient condition. Aphids are specifically sensitive to the homoterpenes such as (E)-4,8-dimethyl-1,3,7-nonatriene and (E, E)- 4,8,12-trimethyltrideca-1,3,7,11-tetraene which are produced by plants attacked by aphids and which reduce colonisation or attraction of predators or parasitoids in cotton aphids [14] and other aphids [15]. Thus, studying how aphid’s respond to pheromones and plant volatiles at the molecular level offers promising ways to explain the ecological context of aphid-aphid and aphid-plant interactions. In turn, this will facilitate the design and implementation of novel sustainable aphid management strategies for pest control and benefit environmental and ecological systems.

This study has identified OBPs and CSPs in the cotton aphid A. gossypii and shown that these proteins are clustered in highly conserved groups comprising OBP genes from different aphid species. The genes have more and longer introns than in non-aphid species suggesting different evolution mechanisms from those of other insects. The overexpression of some OBP and CSP genes in the antennae and winged adults produced when the cotton aphids are ready to migrate in search of new hosts suggests that they play a role in host location and may offer a target for intervention to prevent completion of the life-cycle. This study provides, for the first time, the antennal expression profile of aphid OBP and CSP transcripts and three morph stages with ecological significance from a population composed of genetically identical individuals derived parthenogenetically from a single founding aphid. Some transcripts (AgosOBP2, AgosOBP8, AgosCSP4, and AgosCSP6) that are highly expressed in the cotton aphid antennae have homologues that are indicated to be expressed highly in the male library and the sexuparae head libraries of the pea aphid. Further studies are needed to see which olfactory cues (plant volatiles and/or sex pheromones) may be perceived by these proteins. However, the homologues of all up-regulated transcripts in the winged morphs of the cotton aphid (AgosOBP6, AgosOBP9, AgosOBP10, AgosCSP1, AgosCSP2, AgosCSP4, AgosCSP6 and AgosCSP8) have very low abundance in the winged female transcript library (SRR073136) of the pea aphid reported in AphidBase. Since the experimental size is relative small (3 technical replicates and 2 biological replicates) and all individuals are expected to be genetically homogeneous, the expression profiling between tissue types may be regarded from “one individual” and the results might not be representative of the entire species/population. Further statistical analyses on the pea aphid RNA-seq data in AphidBase are needed to confirm such comparative results. Nevertheless this expression difference between the cotton and pea aphids and the differential expression among different aphid species of 15 OBP and 13 CSP transcripts annotated in the pea aphid genome demonstrate a significant regulation of these olfactory genes in aphid species, thus indicating the important role they may play in aphid physiology.