Drukewitz SH et al. (2019), Toxins from scratch? Diverse, multimodal gene o...

ECB-ART-47307

Gigascience 2019 Jul 01;87:. doi: 10.1093/gigascience/giz081.

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Toxins from scratch? Diverse, multimodal gene origins in the predatory robber fly Dasypogon diadema indicate a dynamic venom evolution in dipteran insects.

Drukewitz SH , Bokelmann L , Undheim EAB , von Reumont BM .

Abstract
BACKGROUND: Venoms and the toxins they contain represent molecular adaptations that have evolved on numerous occasions throughout the animal kingdom. However, the processes that shape venom protein evolution are poorly understood because of the scarcity of whole-genome data available for comparative analyses of venomous species. RESULTS: We performed a broad comparative toxicogenomic analysis to gain insight into the genomic mechanisms of venom evolution in robber flies (Asilidae). We first sequenced a high-quality draft genome of the hymenopteran hunting robber fly Dasypogon diadema, analysed its venom by a combined proteotranscriptomic approach, and compared our results with recently described robber fly venoms to assess the general composition and major components of asilid venom. We then applied a comparative genomics approach, based on 1 additional asilid genome, 10 high-quality dipteran genomes, and 2 lepidopteran outgroup genomes, to reveal the evolutionary mechanisms and origins of identified venom proteins in robber flies. CONCLUSIONS: While homologues were identified for 15 of 30 predominant venom protein in the non-asilid genomes, the remaining 15 highly expressed venom proteins appear to be unique to robber flies. Our results reveal that the venom of D. diadema likely evolves in a multimodal fashion comprising (i) neofunctionalization after gene duplication, (ii) expression-dependent co-option of proteins, and (iii) asilid lineage-specific orphan genes with enigmatic origin. The role of such orphan genes is currently being disputed in evolutionary genomics but has not been discussed in the context of toxin evolution. Our results display an unexpected dynamic venom evolution in asilid insects, which contrasts the findings of the only other insect toxicogenomic evolutionary analysis, in parasitoid wasps (Hymenoptera), where toxin evolution is dominated by single gene co-option. These findings underpin the significance of further genomic studies to cover more neglected lineages of venomous taxa and to understand the importance of orphan genes as possible drivers for venom evolution.

PubMed ID: 31289835
PMC ID: PMC6615979
Article link: Gigascience

Genes referenced: adcy10

Article Images: [+] show captions

	Fig. 1:. The 3D reconstructed venom delivery system of female and male Dasypogon diadema. The general anatomy of D. diadema is similar between both sexes and to the structures described for Eutolmus rufibarbis.A pair of elongated sac-like glands located in the first and second thoracic segments (right and left glands coloured red and orange, respectively) open separately into ducts (coloured green), which fuse just before entering the head capsule and continue to the tip of the proboscis. Compared with the glands of E. rufibarbis, the glands of D. diadema are more elongated, featuring a larger volume and sub-compartmentalization. The labial glands (coloured blue) are located in the middle part of the proboscis and open into the lumen between theca and the labium at the tip of the proboscis.

	Fig. 3:. (a) Phylogenetic relationships of the included taxa. Dasypogon diadema was used as the focal species for the analyses of the orthogroups. Boxes on the split show the number of orthogroups shared by D. diadema and the respective clade of the split (upper number: number of shared orthogroups; middle number: number of orthogroups with putative toxins; lower number: number of orthogroups associated with the 30 predominant putative toxins). (b) Heat map showing the expression level (TPM) in the 3 tissues of the putative toxins of both sexes. The white numbers in the black circle refer to the affiliated orthogroups and splits in 3a (Vg-♂: venom gland male; Vg-♀: venom gland female; Pb-♂: proboscis male; Pb-♀: proboscis female; Bt-♂: body tissue male; Bt-♀: body tissue female). (c) Summarized expression level (TPM) of the putative toxin transcripts in the venom gland of both sexes. The white numbers in the black circle refer to the affiliated orthogroups and splits in 3a (number of putative toxins for all nodes: Node 1: 130; Node 2: 3; Node 3: 0; Node 4: 5; Node 5: 18; Node 6: 1; *no orthogroup: 4).
	Fig. 4:. The evolutionary pattern and the origin of the top 30 putative toxins. The node numbering refers to the nodes in Fig. 3a. Putative toxins present in Dasypogon diadema but missing in Eutolmus rufibarbis or Machimus arthriticus are coloured red. Single-copy genes: putative toxins with only 1 copy on the protein-coding genome of D. diadema; multi-copy genes: protein-coding genes that belong to orthogroups assembled of ≥2 protein-coding genes in D. diadema. Only 1 member of the orthogroup is present in the venom; multi-copy genes*: protein-coding genes that belong to orthogroups assembled of ≥2 protein-coding genes in D. diadema. Two or more members of the same orthogroup are present in the venom.

References [+] :

Bairoch, The SWISS-PROT protein sequence database and its supplement TrEMBL in 2000. 2000, Pubmed