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Schwartz, M.; Boichot, V.; Fraichard, S.; Muradova, M.; Senet, P.; Nicolaï, A.; Lirussi, F.; Bas, M.; Canon, F.; Heydel, J.; et al. The Involvement of GSTs in Insect Chemoperception. Encyclopedia. Available online: https://encyclopedia.pub/entry/41620 (accessed on 13 June 2024).
Schwartz M, Boichot V, Fraichard S, Muradova M, Senet P, Nicolaï A, et al. The Involvement of GSTs in Insect Chemoperception. Encyclopedia. Available at: https://encyclopedia.pub/entry/41620. Accessed June 13, 2024.
Schwartz, Mathieu, Valentin Boichot, Stéphane Fraichard, Mariam Muradova, Patrick Senet, Adrien Nicolaï, Frédéric Lirussi, Mathilde Bas, Francis Canon, Jean-Marie Heydel, et al. "The Involvement of GSTs in Insect Chemoperception" Encyclopedia, https://encyclopedia.pub/entry/41620 (accessed June 13, 2024).
Schwartz, M., Boichot, V., Fraichard, S., Muradova, M., Senet, P., Nicolaï, A., Lirussi, F., Bas, M., Canon, F., Heydel, J., & Neiers, F. (2023, February 24). The Involvement of GSTs in Insect Chemoperception. In Encyclopedia. https://encyclopedia.pub/entry/41620
Schwartz, Mathieu, et al. "The Involvement of GSTs in Insect Chemoperception." Encyclopedia. Web. 24 February, 2023.
The Involvement of GSTs in Insect Chemoperception
Edit

Glutathione transferases (GSTs) are ubiquitous key enzymes with different activities as transferases or isomerases. As key detoxifying enzymes, GSTs are expressed in the chemosensory organs. They fulfill an essential protective role because the chemosensory organs are located in the main entry paths of exogenous compounds within the body. 

insects glutathione transferase olfaction taste chemosensory organs

1. Chemoperception in Insects

Insects constitute the largest class of living animal species. Due to their small size, they have developed multiple mechanisms to limit toxic xenobiotic effects, including the enhancement of metabolic detoxification [1][2], which reduces penetration through the cuticle, or behavioral avoidance [3]. Insects can taste through many parts of their body. The proboscis organs used for feeding and sucking allow insects to taste food during ingestion before it reaches the digestive system. In addition to the proboscis, insects are able to detect tastants with their legs, wings, and ovipositor organs. Consequently, due to their small size compared with food, they are generally already in contact with it before ingesting it, making it advantageous to taste it with their legs before eating or with the ovipositor organ before laying eggs. Although the taste systems of mammals and insects evolved independently, they enable the detection of similar qualities, including sweet, salty, and bitter stimuli. Insects are able to detect carbonation as a taste modality through gustatory neurons [4], similar to mammals, through carbonic anhydrase IV, which produces protons that activate a proton-gated channel [5]. Interestingly, carbonation detection is also possible in both mammals and insects through the olfactory system [5]. Insects have gustatory sensory neurons that mediate the recognition of water [6]; to date, it has not been established whether other animals can taste the water. In mammals, taste receptors are not hosted by neurons. Neurons are in contact with the taste cells that carry gustatory receptors and are located in taste buds. In insects, gustatory receptors are directly carried by gustatory neurons, in contrast to vertebrate gustatory neurons, which are housed in cells that are indirectly in contact with neurons. Gustatory neurons are housed within the hundreds of gustatory sensilla distributed on the surface of the different sensory organs except the proboscis, which also includes internal sensilla [7].
In insects, the equivalent of the mammalian nose is the antenna and the maxillary palps. Although they do not exhibit any evolutionary relationship with mammals, olfaction is also supported by olfactory neurons in insects. Indeed, the olfactory sensilla cover the distal segment of the antenna, and the maxillary palps host the olfactory neurons. Dendrites of olfactory neurons that express olfactory neurons are located in the sensilla lymph within the sensilla. Odor molecules pass through pores or slits in the sensillum cuticle and enter the sensillum lymph [8]. Insect olfactory receptors are not homologs of vertebrate olfactory receptors [9], suggesting different evolutionary origins compared with those found in vertebrates. Consequently, although the organizational features of the olfactory systems of vertebrates and insects appear very similar, these structures may not share a common evolutionary heritage [10].
Insect GRs and ORs, which are membrane proteins, do not show any homology to those of vertebrates [11][12] and consequently do not belong to the GPCR family. However, both GRs and ORs evolved from an ancestral protein, and in addition to sharing the same sequence identity, they share the same inverted transmembrane topology as vertebrate olfactory GPCRs. The expansion of genes coding for the insect GR and OR has occurred only in insects [13]. In contrast to the monomeric ORs of vertebrates, insect ORs form heteromers with a conserved OR receptor also called Orco (i.e., the OR coreceptor). One specific OR is expressed in each insect olfactory neuron in addition to Orco, as in vertebrate olfactory neurons, where one specific OR is expressed in each olfactory neuron. It is unclear whether insect GRs can function alone as multimers or with other insect GRs due to the observation that multiple GR genes are expressed in a single GR neuron [14].
Even if the chemosensory systems in insects and mammals present similar biological organizations, they do not share any evolutionary links. However, in both chemosensory systems, glutathione transferases from the same common ancestor are expressed, most likely sharing similar physiological roles.

2. Roles of GSTs in Insect Chemoperception

In addition to the Omega, Sigma, Theta, and Zeta GST classes found in insects and shared with mammals, two other classes are observed: Delta and Epsilon GSTs. Delta GSTs are found in insects and are observed in a more general manner in arthropods, such as crustaceans [15]. Epsilon GSTs appear more specific to insects and were hypothesized to be insect-specific [16]. The numbers of Delta and Epsilon GSTs are variable from one insect species to another, mostly due to duplication events that occur in each insect species (Table 1). This gene-coding GST duplication might be associated with functional differentiation during insect evolution and is related to environmental adaptation. Gene duplication followed by sequence divergence is a key process during evolution, allowing the creation of novel gene functions [17]. Interactions of insects with plants, and especially plant chemicals and their adaptations to them, appear to be the most likely major driving force in herbivorous insect evolution [18]. Plant molecules can be toxic to insects, and consequently, GSTs and detoxifying enzymes are essential for insect survival. GSTs detoxify a broad range of plant molecules, generally with an overlap of GSTs for the same substrate [19][20][21]. Signatures of a positive selection of Delta GSTs suggest that they may have evolved under positive selection in the herbivorous [22] lineage after the transition of insects to herbivory > 350 Ma [23]. This adaptation phenomenon can be rapid; indeed, anthropological pressure toward insects for insecticide resistance has been suggested to promote Musca domestica gst gene amplification [24][25]. The main classes of GST diversification appear to be the Epsilon and Delta classes in various insects, such as Anopheles gambiae, Drosophilia melanogaster, or Tribolium castaneum [16][26]. In this context, it is not surprising to observe numerous insect adaptations toward insecticides [27][28] due to the Delta and Epsilon GSTs in the role of A. gambiae GSTE1 and GSTE2 in the DDT resistance [29]. The chemical resistance promoted by GSTs involves various chemicals, such as pyrethroids or neonicotinoids and 2,2-dichlorovinyl dimethylphosphate for Diaphorina citri [30] and Rynochophorus phoenicis, respectively [31]. In contrast, Apis mellifera, known to be highly sensitive to insecticides, presents only one Delta GST (including two isoforms) and no Epsilon GST. It is not excluded that some GSTs resulting from functional differentiation appear with different functions not related at all to xenobiotic metabolism, such as GSTE14 in D. melanogaster, which is involved in ecdysone biosynthesis [32][33][34]. Additionally, GSTs formed during the diversification process can also be specific in metabolizing some molecules without a functional overlap from other GSTs within the same insect species. For example, the deletion of epsilon and omega GSTs in the Asian gypsy moth, Lymantria dispar, affected its adaptability to salicin and rutin produced by its host, the poplar tree [35].
Table 1. Number of identified canonical GSTs in different insect species.
Order Insect Species Cytosolic   Total Ref.
    Delta Epsilon Omega Sigma Theta Zeta Unclassified    
Coleoptera Lasioderma serricorne 1 0 0 1 1 0 0 3 [36]
Agrilus planipennis 5 9 0 2 0 0 0 16 [36]
Anoplophora glabripennis 10 10 2 4 2 0 0 28 [37]
Rhaphuma horsfieldi 5 8 3 2 1 1 0 20 [36]
Xylotrechus quadripes 5 7 2 2 1 1 0 18 [36]
Diabrotica virgifera 3 11 1 0 2 0 0 17 [36]
Leptinotarsa Decemlineata 6 11 7 6 2 1 0 33 [38]
Phyllotreta striolata 5 6 2 6 1 1 2 23 [39]
Dendroctonus armandi 0 4 1 2 1 0 0 8 [40]
Dendroctonus ponderosae 6 12 2 5 2 1 0 28 [41]
Lissorhoptrus oryzophilus 3 7 2 8 1 1 2 24 [36]
Sitophilus oryzae 2 12 3 6 2 1 0 26 [42]
Aethina tumida 3 19 1 7 1 5 7 43 [43]
Oryctes borbonicus 4 5 3 15 3 1 0 31 [44]
Onthophagus taurus 4 7 3 1 4 0 0 19 [36]
Nicrophorus vespilloides 8 6 0 1 3 0 0 18 [36]
Asbolus verrucosus 3 14 2 2 1 0 0 22 [36]
Tribolium castaneum 3 19 3 7 1 1 2 36 [16]
Tenebrio molitor 2 13 1 5 1 1 2 25 [45]
Diptera Chironomus riparius 3 1 1 4 1 1 2 13 [46]
Aedes aegypti 8 8 1 1 4 1 3 26 [47]
Anopheles gambiae 17 8 1 1 2 1 2 32 [16]
Culex quinquefasciatus 14 10 1 1 6 0 3 35 [48][49]
Drosophila melanogaster 11 14 4 1 4 2 1 37 [16]
Bactrocera dorsalis 9 5 3 1 3 3 1 25 [50]
Ceratitis capitata 7 14 1 1 3 2 1 29 [51]
Hemiptera Bemisia tabaci 14 0 1 6 0 2 0 23 [52]
Orius laevigatus 1 0 2 16 1 1 0 21 [53]
Acyrthosiphon pisum 16 1 2 6 2 0 3 30 [16]
Myzus persicae 8 0 0 8 2 0 0 18 [54]
Laodelphax striatellus 1 1 1 3 1 1 0 8 [55]
Nilaparvata lugens 2 1 1 3 1 1 0 9 [56][57]
Supraphorura furcifera 2 1 1 1 1 1 0 7 [57]
Rhodnius prolixus 1 0 1 7 4 1 0 14 [58]
Diaphorina citri 2 2 0 3 0 0 1 8 [52]
Hymeno-ptera Apis mellifera 2 0 2 4 1 1 1 11 [16]
Bombus impatiens 5 0 2 4 1 1 0 13 [59]
Bombus terrestris 5 0 2 4 1 1 0 13 [59]
Meteorus pulchricornis 4 0 3 7 0 1 0 15 [60]
Nasonia vitripennis 5 0 2 8 3 1 0 19 [61]
Pteromalus puparum 5 0 2 8 3 1 0 19 [62]
Lepidoptera Bombyx mori 4 8 4 2 1 2 2 23 [63]
Cnaphalocrocis medinalis 4 9 3 5 0 2 2 25 [45]
Heortia vitessoides 3 2 3 3 1 2 2 16 [64]
Spodoptera litura 5 21 3 7 1 2 3 42 [65]
Danaus plexippus 3 6 3 5 1 3 2 23 [36]
Pieris rapae 3 3 4 4 1 2 0 17 [66]
Plutella xylostella 5 5 5 2 1 2 2 22 [67]
Manduca sexta 6 9 4 2 1 2 1 25 [36]
Cydia pomonella 4 3 2 1 1 1 1 13 [68]
Orthoptera Locusta migratoria 10 0 3 12 2 1 0 28 [69]
Phthir-aptera Pediculus humanus 4 0 1 4 1 1 0 11 [70]
Psocoptera Liposcelis entomophila 17 0 1 13 3 1 0 35 [71]
As shown in vertebrate chemosensory organs, GSTs are also expressed in insect chemosensory organs (Table 2). This expression is advantageous to protect these sensitive organs where neurons are directly exposed to xenobiotics. GSTs were shown to be expressed in the antennae of various orders of insect species, such as the dipteran D. melanogaster [72][73], various lepidopteran species [45][68][74][75][76][77][78] such as Manduca sexta [79] or Spodoptera littoralis [80], and in the Coleoptera antennae of Agrilus planipennis [81] or Dendroctonus valens [82]. Table 2 shows the diversity of insect species expressing GSTs within their sensory organs. Although a limited number of studies have analyzed GST expression, GSTs appear to be ubiquitously expressed in antennae. To support this hypothesis, GST expression in two particular insect species can be highlighted. The only Delta GST found in A. melifera is expressed in its antennae [83]. Ticks have a unique chemosensory organ presumed to function similarly to insect antennae, the fore-tarsal Haller’s organ. GSTs were found to be expressed in this organ of the dog tick, Dermacentor variabilis [84]. As in mammals, GSTs were proposed to protect the chemosensory organs so they could participate in odorant clearance and consequently signal termination. Antennal GSTs were shown to be active toward the model substrate CDNB (1-chloro-2,4-dinitrobenzene); for example, most antennal Drosophila GSTs [85][86]. The ability to conjugate CDNB was also observed for the antennal-specific GST identified in Bombyx mori [76]. The selective pressure to conserve efficient odorant clearance is crucial for flying insects, which need to reinitiate odorant perception as quickly as possible to follow the odorant volute. The detection of odorant food sources can be diversified, probably involving different GSTs. However, pheromone detection can also involve more specialized GSTs, as shown for an antenna-specific Delta GST found in Manducta sexta. This GST was shown to metabolize trans-2-hexenal, a plant-derived green leaf aldehyde known to stimulate the olfactory system of M. sexta. This GST was proposed to be involved in the signal termination of a complex mixture of aldehyde molecules forming the sex pheromone bouquet [79]. A delta GST found in the antennae of Grapholita molesta shows high activity toward a sex pheromone component, (Z)-8-dodecenyl alcohol [87]. The role of GST in sex pheromone detection is also supported by the differential expression of GST depending on the insect sex. For example, antennal-specific genes of a GST belonging to the Delta class were significantly more highly expressed in male Helicoverpa armigera antennae compared with females [78]. Despite all the different studies, to the best of the authors’ knowledge, the cellular localization of GSTs within the olfactory sensilla is not known to date. Moreover, expression within the sensory lymph, where the olfactory neurons are located, has not been validated experimentally. The same question about localization exists for insect gustatory sensilla. GSTs have been identified in diverse taste organs, such as the labellum, in insects belonging to the dipteran and ledidopteran orders (Table 2); however, the cell types and localization within the lymph of gustatory sensilla are not shown. Food containing bitter molecules such as glucosinolates and isothiocyanates led to GST overexpression in aphids in a general manner [88]. Additionally, other results have shown the same regulation in chemosensory organs. Isothiocyanates were shown to increase the expression of GST Delta in Drosophila labellum [89]. This modulation can be hypothesized to affect food habits. The results showed that the loss of bitter taste receptors observed in D. suzukii in comparison to D. melanogaster was proposed to contribute to the evolutionary shift in oviposition preference between the two species [90], knowing that ovipositor organs are taste-sensitive. In the same study, the taste difference between these two Drosophila species showed an associated differential expression of xenobiotic metabolism enzymes, including delta and epsilon GSTs. Again, this observation supports a direct link between these enzymes and the taste biochemistry in insects.
Table 2. Identification of GSTs in the chemosensory organs of various insect species.
Order Insect Species Location GST Classes Ref.
Coleoptera Agrilus planipennis Antennae Delta [81]
Dendroctonus valens Antennae Not indicated [82]
Phyllotreta striolata Antennae Delta and Epsilon [39]
Diptera Aedes albopictus Antennae/maxillary palps Not indicated [91]
Drosophila melanogaster Antennae/maxillary palps/labellum Delta, Epsilon, Omega, Sigma, Theta, and Zeta [72][73][89]
Hymenoptera Apis melifera Antennae Delta [83]
Ixodida Dermacentor variabilis Haller’s organ Epsilon and Mu [84]
Lepidoptera Bombyx Mori Antennae Delta [76]
Chilo suppressalis Antennae Delta, Epsilon, Omega, Sigma, Theta, and Zeta [75]
Cydia pomonella Antennae Delta, Epsilon, Omega, Sigma, Theta, and Zeta [68]
Epiphyas postvittana Antennae Delta, Epsilon, Omega, Sigma, and Theta [92]
Grapholita molesta Antennae Delta [87]
Helicoverpa armigera Antenna Delta [78]
Heortia vitessoides Antennae Delta and Epsilon [64]
Manduca sexta Antennae Delta [79]
Papilio xuthus Antennae, labella, and tarsi Delta [93]
Plodia interpunctella Antennae Delta, Epsilon, Omega, Sigma, Theta, and Zeta [94]
Spodoptera littoralis Antennae Delta, Epsilon, Omega, Sigma, Theta, and Zeta [80][95]

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