Skip to main page content
U.S. flag

An official website of the United States government

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
Comparative Study
. 2017 Jan 1;9(1):178-196.
doi: 10.1093/gbe/evw296.

Evolution of Chemosensory Gene Families in Arthropods: Insight from the First Inclusive Comparative Transcriptome Analysis across Spider Appendages

Joel Vizueta  1 , Cristina Frías-López  1 , Nuria Macías-Hernández  2 , Miquel A Arnedo  2 , Alejandro Sánchez-Gracia  1 , Julio Rozas  1
Affiliations
Comparative Study

Evolution of Chemosensory Gene Families in Arthropods: Insight from the First Inclusive Comparative Transcriptome Analysis across Spider Appendages

Joel Vizueta et al. Genome Biol Evol. .

Abstract

Unlike hexapods and vertebrates, in chelicerates, knowledge of the specific molecules involved in chemoreception comes exclusively from the comparative analysis of genome sequences. Indeed, the genomes of mites, ticks and spiders contain several genes encoding homologs of some insect membrane receptors and small soluble chemosensory proteins. Here, we conducted for the first time a comprehensive comparative RNA-Seq analysis across different body structures of a chelicerate: the nocturnal wandering hunter spider Dysdera silvatica Schmidt 1981. Specifically, we obtained the complete transcriptome of this species as well as the specific expression profile in the first pair of legs and the palps, which are thought to be the specific olfactory appendages in spiders, and in the remaining legs, which also have hairs that have been morphologically identified as chemosensory. We identified several ionotropic (Ir) and gustatory (Gr) receptor family members exclusively or differentially expressed across transcriptomes, some exhibiting a distinctive pattern in the putative olfactory appendages. Furthermore, these IRs were the only known olfactory receptors identified in such structures. These results, integrated with an extensive phylogenetic analysis across arthropods, uncover a specialization of the chemosensory gene repertoire across the body of D. silvatica and suggest that some IRs likely mediate olfactory signaling in chelicerates. Noticeably, we detected the expression of a gene family distantly related to insect odorant-binding proteins (OBPs), suggesting that this gene family is more ancient than previously believed, as well as the expression of an uncharacterized gene family encoding small globular secreted proteins, which appears to be a good chemosensory gene family candidate.

Keywords: arthropods; chelicerates; chemosensory gene families; de novo transcriptome assembly; functional annotation; specific RNA-Seq.

PubMed Disclaimer

Figures

<sc>Fig</sc>. 1.—
Fig. 1.—
(A) Phylogenetic position of Dysdera silvatica within arthropods. Divergence times were obtained from TimeTree (Hedges et al. 2015). (B) D. silvatica feeding on a woodlouse.
<sc>Fig</sc>. 2.—
Fig. 2.—
Venn diagram showing the total number of transcripts (154,427 transcripts) specifically expressed in each experimental condition and their intersections (red, orange, green and blue indicate LEG#1, LEG#234, PALP and REST, respectively). Numbers in brackets indicate putative chemosensory protein encoding transcripts (117 in total).
<sc>Fig</sc>. 3.—
Fig. 3.—
Maximum likelihood phylogenetic tree of the IR/iGluR proteins across arthropods. The tree is based on the MSA of the LCD domain (PF00060). (A) Sequences of Drosophila melanogaster, Daphnia pulex, Strigamia maritima, Ixodes scapularis, Stegodyphus mimosarum and Dysdera silvatica are depicted in green, light blue, dark blue, orange, brown and red, respectively. Additionally, the translation of the D. silvatica transcripts are shadowed in grey. Nodes with bootstrap support values >75% are shown as solid circles. Nodes with five or more sequences from the same species were collapsed; the actual number of collapsed branches is indicated in each case. The two surrounding circles provide information regarding the expression pattern of some D. silvatica genes. The most external circle indicates the genes specifically expressed in palps (PALP; in green), legs (both LEG#1 and LEG#234; in pink) and palps and legs (PALP, LEG#1 and LEG#234; in orange). The inner circle shows the genes overexpressed in these conditions using the same color codes but with two color intensities, one more intense color for overexpression levels >5× over REST and another lighter color for 2–5× overexpression values. The branch length scale is in numbers of amino acid substitutions per amino acid position. (B) Simplified phylogenetic tree highlighting the main Ir sub-families.
<sc>Fig</sc>. 4.—
Fig. 4.—
Maximum likelihood phylogenetic tree of the GR proteins across arthropods. Species names, node support features and surrounding circles are colored as in figure 3.
<sc>Fig</sc>. 5.—
Fig. 5.—
Maximum likelihood phylogenetic relationships of spider OBP-like and insect OBP proteins. Species names, node support features and surrounding circles are colored as in figure 3. The inner circle labels the previously defined OBP phylogenetic subfamilies (Classic, Minus-C, Plus-C and ABPII in black, green, blue and grey, respectively).
<sc>Fig</sc>. 6.—
Fig. 6.—
Predicted 3D structure of two OBP-like proteins. (A) Structure of Anopheles gambiae OBP20 (PDB 3V2L). (B) Structure of A. gambiae OBP4 (PDB 3Q8I). (C) 3D model of the protein encoded by the transcript Dsil553. (D) Predicted 3D model of the Strigamia maritima Smar010094 protein. PBD files were viewed and manipulated in Swiss-PdbViewer version 4.1 (Guex and Peitsch 1997).
<sc>Fig</sc>. 7.—
Fig. 7.—
Maximum likelihood phylogenetic tree of the NPC2 proteins across arthropods. Species names, node support features and surrounding circles are colored as in figure 3. Sequences from Apis mellifera and Camponotus japonicus are colored in green.
<sc>Fig</sc>. 8.—
Fig. 8.—
Maximum likelihood phylogenetic tree of CD36-SNMP proteins across arthropods. Species names, node support features and surrounding circles are colored as in figure 3. The inner circle shows the different subfamilies.
See this image and copyright information in PMC

Similar articles

See all similar articles

Cited by

See all "Cited by" articles

References

    1. Adams MD, et al. 2000. The genome sequence of Drosophila melanogaster . Science 287:2185–2195. - PubMed
    1. Altschul S. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389–3402. - PMC - PubMed
    1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J Mol Biol. 215:403–410. - PubMed
    1. Ashburner M, et al. 2000. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet. 25:25–29. - PMC - PubMed
    1. Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc. 57:289–300.

Publication types

Substances

LinkOut - more resources