Identification of Candidate Chemosensory Gene Families by Head Transcriptomes Analysis in the Mexican Fruit Fly, Anastrepha ludens Loew (Diptera: Tephritidae)

Abstract

Insect chemosensory systems, such as smell and taste, are mediated by chemosensory receptor and non-receptor protein families. In the last decade, many studies have focused on discovering these families in Tephritidae species of agricultural importance. However, to date, there is no information on the Mexican fruit fly Anastrepha ludens Loew, a priority pest of quarantine importance in Mexico and other countries. This work represents the first effort to identify, classify and characterize the six chemosensory gene families by analyzing two head transcriptomes of sexually immature and mature adults of A. ludens from laboratory-reared and wild populations, respectively. We identified 120 chemosensory genes encoding 31 Odorant-Binding Proteins (OBPs), 5 Chemosensory Proteins (CSPs), 2 Sensory Neuron Membrane Proteins (SNMPs), 42 Odorant Receptors (ORs), 17 Ionotropic Receptors (IRs), and 23 Gustatory Receptors (GRs). The 120 described chemosensory proteins of the Mexican fruit fly significantly contribute to the genetic databases of insects, particularly dipterans. Except for some OBPs, this work reports for the first time the repertoire of olfactory proteins for one species of the genus Anastrepha, which provides a further basis for studying the olfactory system in the family Tephritidae, one of the most important for its economic and social impact worldwide.

Keywords: multigene families; olfactory proteins; pest insect; sensorial perception.

Figure 1

Functional annotation in GO, InterPro, and UniprotKB databases (accessed on October 2021) of unigenes obtained from A. ludens head transcriptomes constructed with Illumina HiSeq2000 (a) and BGISEQ-500 (b) platforms; also showing species distribution, similarity percentages, and E-value from BLASTx analysis against the Insecta-UniprotKB database.

Figure 2

Bayesian phylogenetic analysis of candidate OBPs from Anastrepha ludens with homologs from seven Tephritidae species and the model organism Drosophila melanogaster. The clusters of subfamily OBPs identified in AludOBPs have distinct color bar marks. Gray bars delimit the branch expansions of the AludOBPs and their orthologues. Circles showed posterior probability values higher than 70%.

Figure 3

Bayesian phylogenetic analysis of candidate CSPs of Anastrepha ludens with homologs from twelve dipteran species and the model organism Drosophila melanogaster. Blue and gray bars delimit the branch expansions of the AludCSPs and their orthologues. Circles showed posterior probability values over 70%. Letters “U-” and “P-” refer to sequences in the databases that are uncharacterized or were automatically annotated by the genomic sequence prediction method.

Figure 4

Bayesian phylogenetic analysis of candidate SNMPs from Anastrepha ludens with homologs from seven dipteran species and the model organism Drosophila melanogaster. Bars delimit clusters of AludSNMPs and their orthologues. Circles showed posterior probability values higher than 70%.

Figure 5

Bayesian phylogenetic analysis of candidate ORs of Anastrepha ludens with homologs from eight dipteran species and the model organism Drosophila melanogaster. Circles showed posterior probability values higher than 70%. Pink bars delimit clusters of AludORs and their orthologues.

Figure 6

Bayesian phylogenetic analysis of candidate GRs from Anastrepha ludens with homologs from seven Tephritidae species and Drosophila melanogaster. Distinct colors represent clusters of AludGRs members based on putative functions reported in previous studies. Gray bars delimit branch expansions of AludGRs and their orthologues. Circles showed posterior probability values higher than 70%.

Figure 7

Bayesian phylogenetic analysis of candidate iGluRs/IRs from Anastrepha ludens with homologs from seven Tephritidae species and Drosophila melanogaster. Distinct colors represent clusters of AludIRs members based on putative functions reported in previous studies. Gray bars delimit the branch expansions of the AludIRs and their orthologues. Circles showed posterior probability values higher than 70%.