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Article ; Online: Phylogenomics of the Ecdysteroid Kinase-like (EcKL) Gene Family in Insects Highlights Roles in Both Steroid Hormone Metabolism and Detoxification.

Scanlan, Jack L / Robin, Charles

2024 Volume 16, Issue 2

Abstract: The evolutionary dynamics of large gene families can offer important insights into the functions of their individual members. While the ecdysteroid kinase-like (EcKL) gene family has previously been linked to the metabolism of both steroid molting ... ...

Abstract	The evolutionary dynamics of large gene families can offer important insights into the functions of their individual members. While the ecdysteroid kinase-like (EcKL) gene family has previously been linked to the metabolism of both steroid molting hormones and xenobiotic toxins, the functions of nearly all EcKL genes are unknown, and there is little information on their evolution across all insects. Here, we perform comprehensive phylogenetic analyses on a manually annotated set of EcKL genes from 140 insect genomes, revealing the gene family is comprised of at least 13 subfamilies that differ in retention and stability. Our results show the only two genes known to encode ecdysteroid kinases belong to different subfamilies and therefore ecdysteroid metabolism functions must be spread throughout the EcKL family. We provide comparative phylogenomic evidence that EcKLs are involved in detoxification across insects, with positive associations between family size and dietary chemical complexity, and we also find similar evidence for the cytochrome P450 and glutathione S-transferase gene families. Unexpectedly, we find that the size of the clade containing a known ecdysteroid kinase is positively associated with host plant taxonomic diversity in Lepidoptera, possibly suggesting multiple functional shifts between hormone and xenobiotic metabolism. Our evolutionary analyses provide hypotheses of function and a robust framework for future experimental studies of the EcKL gene family. They also open promising new avenues for exploring the genomic basis of dietary adaptation in insects, including the classically studied coevolution of butterflies with their host plants.
MeSH term(s)	Animals ; Ecdysteroids/genetics ; Ecdysteroids/metabolism ; Phylogeny ; Butterflies ; Xenobiotics ; Insecta/genetics
Chemical Substances	Ecdysteroids ; Xenobiotics
Language	English
Publishing date	2024-01-30
Publishing country	England
Document type	Journal Article
ZDB-ID	2495328-3
ISSN	1759-6653 ; 1759-6653
ISSN (online)	1759-6653
ISSN	1759-6653
DOI	10.1093/gbe/evae019
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Ecdysteroid kinase-like (EcKL) paralogs confer developmental tolerance to caffeine in

Scanlan, Jack L / Battlay, Paul / Robin, Charles

Current research in insect science

2022 Volume 2, Page(s) 100030

Abstract: A unique aspect of metabolic detoxification in insects compared to other animals is the presence of xenobiotic phosphorylation, about which little is currently understood. Our previous work raised the hypothesis that members of the taxonomically ... ...

Abstract	A unique aspect of metabolic detoxification in insects compared to other animals is the presence of xenobiotic phosphorylation, about which little is currently understood. Our previous work raised the hypothesis that members of the taxonomically restricted ecdysteroid kinase-like (EcKL) gene family encode the enzymes responsible for xenobiotic phosphorylation in the model insect
Language	English
Publishing date	2022-01-16
Publishing country	Netherlands
Document type	Journal Article
ISSN	2666-5158
ISSN (online)	2666-5158
DOI	10.1016/j.cris.2022.100030
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Article ; Online: Rethinking the ecdysteroid source during Drosophila pupal-adult development.

Scanlan, Jack L / Robin, Charles / Mirth, Christen K

Insect biochemistry and molecular biology

2022 Volume 152, Page(s) 103891

Abstract: Ecdysteroids, typified by 20-hydroxyecdysone (20E), are essential hormones for the development, reproduction and physiology of insects and other arthropods. For over half a century, the vinegar fly Drosophila melanogaster (Ephydroidea: Diptera) has been ... ...

Abstract	Ecdysteroids, typified by 20-hydroxyecdysone (20E), are essential hormones for the development, reproduction and physiology of insects and other arthropods. For over half a century, the vinegar fly Drosophila melanogaster (Ephydroidea: Diptera) has been used as a model of ecdysteroid biology. Many aspects of the biosynthesis and regulation of ecdysteroids in this species are understood at the molecular level, particularly with respect to their secretion from the prothoracic gland (PG) cells of the ring gland, widely considered the dominant biosynthetic tissue during development. Discrete pulses of 20E orchestrate transitions during the D. melanogaster life cycle, the sources of which are generally well understood, apart from the large 20E pulse at the onset of pharate adult development, which has received little recent attention. As the source of this pharate adult pulse (PAP) is a curious blind spot in Drosophila endocrinology, we evaluate published biochemical and genetic data as they pertain to three hypotheses for the source of PAP 20E: the PG; an alternative biosynthetic tissue; or the recycling of stored 20E. Based on multiple lines of evidence, we contend the PAP cannot be derived from biosynthesis, with other data consistent with D. melanogaster able to recycle ecdysteroids before and during metamorphosis. Published data also suggest the PAP is conserved across Diptera, with evidence for pupal-adult ecdysteroid recycling occurring in other cyclorrhaphan flies. Further experimental work is required to test the ecdysteroid recycling hypothesis, which would establish fundamental knowledge of the function, regulation, and evolution of metamorphic hormones in dipterans and other insects.
MeSH term(s)	Animals ; Ecdysteroids ; Drosophila melanogaster/genetics ; Drosophila ; Insecta/genetics ; Drosophila Proteins/genetics ; Metamorphosis, Biological/genetics ; Larva/genetics
Chemical Substances	Ecdysteroids ; Drosophila Proteins
Language	English
Publishing date	2022-12-06
Publishing country	England
Document type	Journal Article ; Review ; Research Support, Non-U.S. Gov't
ZDB-ID	1483248-3
ISSN	1879-0240 ; 0965-1748
ISSN (online)	1879-0240
ISSN	0965-1748
DOI	10.1016/j.ibmb.2022.103891
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Article: Ecdysteroid kinase-like (EcKL) paralogs confer developmental tolerance to caffeine in Drosophila melanogaster

Scanlan, Jack L. / Battlay, Paul / Robin, Charles

Current research in insect science. 2022, v. 2

2022

Abstract	A unique aspect of metabolic detoxification in insects compared to other animals is the presence of xenobiotic phosphorylation, about which little is currently understood. Our previous work raised the hypothesis that members of the taxonomically restricted ecdysteroid kinase-like (EcKL) gene family encode the enzymes responsible for xenobiotic phosphorylation in the model insect Drosophila melanogaster (Diptera: Ephydroidea)—however, candidate detoxification genes identified in the EcKL family have yet to be functionally validated. Here, we test the hypothesis that EcKL genes in the rapidly evolving Dro5 clade are involved in the detoxification of plant and fungal toxins in D. melanogaster. The mining and reanalysis of existing data indicated multiple Dro5 genes are transcriptionally induced by the plant alkaloid caffeine and that adult caffeine susceptibility is associated with a novel naturally occurring indel in CG31370 (Dro5-8) in the Drosophila Genetic Reference Panel (DGRP). CRISPR-Cas9 mutagenesis of five Dro5 EcKLs substantially decreased developmental tolerance of caffeine, while individual overexpression of two of these genes—CG31300 (Dro5-1) and CG13659 (Dro5-7)—in detoxification-related tissues increased developmental tolerance. In addition, we found Dro5 loss-of-function animals also have decreased developmental tolerance of the fungal secondary metabolite kojic acid. Taken together, this work provides the first compelling functional evidence that EcKLs encode detoxification enzymes and suggests that EcKLs in the Dro5 clade are involved in the metabolism of multiple ecologically relevant toxins in D. melanogaster. We also propose a biochemical hypothesis for EcKL involvement in caffeine detoxification and highlight the many unknown aspects of caffeine metabolism in D. melanogaster and other insects.
Keywords	CRISPR-Cas systems ; Drosophila melanogaster ; adults ; caffeine ; fungi ; genes ; insects ; kojic acid ; loss-of-function mutation ; metabolic detoxification ; mutagenesis ; phosphorylation ; research ; secondary metabolites ; transcription (genetics) ; xenobiotics
Language	English
Publishing place	Elsevier B.V.
Document type	Article
ISSN	2666-5158
DOI	10.1016/j.cris.2022.100030
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Article ; Online: Acetylcholine esterase of Drosophila melanogaster: a laboratory model to explore insecticide susceptibility gene drives.

Hernandes, Natalia / Qi, Xiaomeng Mollyann / Bhide, Soumitra / Brown, Courtney / Camm, Benjamin J / Baxter, Simon W / Robin, Charles

Pest management science

2024

Abstract: Background: One of the proposed applications of gene drives has been to revert pesticide resistant mutations back to the ancestral susceptible state. Insecticides that have become ineffective because of the rise of resistance could have reinvigorated ... ...

Abstract	Background: One of the proposed applications of gene drives has been to revert pesticide resistant mutations back to the ancestral susceptible state. Insecticides that have become ineffective because of the rise of resistance could have reinvigorated utility and be used to suppress pest populations again, perhaps at lower application doses. Results: We have created a laboratory model for susceptibility gene drives that replaces field-selected resistant variants of the acetylcholine esterase (Ace) locus of Drosophila melanogaster with ancestral susceptible variants. We constructed a CRISPR/Cas9 homing drive and found that homing occurred in many genetic backgrounds with varying efficiencies. While the drive itself could not be homozygous, it converted resistant alleles into susceptible ones and produced recessive lethal alleles that could suppress populations. Our studies provided evidence for two distinct classes of gene drive resistance (GDR): rather than being mediated by the conventional non-homologous end-joining (NHEJ) pathway, one seemed to involve short homologous repair and the other was defined by genetic background. Additionally, we used simulations to explore a distinct application of susceptibility drives; the use of chemicals to prevent the spread of synthetic gene drives into protected areas. Conclusions: Insecticide susceptibility gene drives could be useful tools to control pest insects however problems with particularities of target loci and GDR will need to be overcome for them to be effective. Furthermore, realistic patterns of pest dispersal and high insecticide exposure rates would be required if susceptibility were to be useful as a 'safety-switch' to prevent the unwanted spread of gene drives. © 2024 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.
Language	English
Publishing date	2024-02-12
Publishing country	England
Document type	Journal Article
ZDB-ID	2001705-4
ISSN	1526-4998 ; 1526-498X
ISSN (online)	1526-4998
ISSN	1526-498X
DOI	10.1002/ps.8003
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Article ; Online: Reconciliation of a gene network and species tree.

Chan, Yao-Ban / Robin, Charles

Journal of theoretical biology

2019 Volume 472, Page(s) 54–66

Abstract: The phylogenetic trees of genes and the species which they belong to are similar, but distinct due to various evolutionary processes which affect genes but do not create new species. Reconciliations map the gene tree into the species tree, explaining the ...

Abstract	The phylogenetic trees of genes and the species which they belong to are similar, but distinct due to various evolutionary processes which affect genes but do not create new species. Reconciliations map the gene tree into the species tree, explaining the discrepancies by events including gene duplications and losses. However, when duplicate genes undergo recombination (a phenomenon known as paralog exchange, or non-allelic homologous recombination), the phylogeny of the genes becomes a network, not a tree. In this paper, we explore how to reconcile a gene network to a species tree with duplications and losses. We propose an extension of the lowest common ancestor (LCA) mapping which solves the problem for tree-child gene networks, show that a restricted version of the problem is polynomial-time solvable and bounds the optimal position of each gene node in the full problem, and show that the full problem is fixed-parameter tractable in the level of the gene network. This provides a formal foundation for the development of efficient algorithms to solve this problem.
MeSH term(s)	Algorithms ; Gene Regulatory Networks ; Models, Genetic ; Phylogeny
Language	English
Publishing date	2019-04-03
Publishing country	England
Document type	Journal Article
ZDB-ID	2972-5
ISSN	1095-8541 ; 0022-5193
ISSN (online)	1095-8541
ISSN	0022-5193
DOI	10.1016/j.jtbi.2019.04.001
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Article ; Online: The haplolethal gene wupA of Drosophila exhibits potential as a target for an X-poisoning gene drive.

Lawler, Clancy D / Nuñez, Ana Karla Parra / Hernandes, Natalia / Bhide, Soumitra / Lohrey, Isabelle / Baxter, Simon / Robin, Charles

G3 (Bethesda, Md.)

2024 Volume 14, Issue 4

Abstract: A synthetic gene drive that targets haplolethal genes on the X chromosome can skew the sex ratio toward males. Like an "X-shredder," it does not involve "homing," and that has advantages including the reduction of gene drive resistance allele formation. ... ...

Abstract	A synthetic gene drive that targets haplolethal genes on the X chromosome can skew the sex ratio toward males. Like an "X-shredder," it does not involve "homing," and that has advantages including the reduction of gene drive resistance allele formation. We examine this "X-poisoning" strategy by targeting 4 of the 11 known X-linked haplolethal/haplosterile genes of Drosophila melanogaster with CRISPR/Cas9. We find that targeting the wupA gene during spermatogenesis skews the sex ratio so fewer than 14% of progeny are daughters. That is unless we cross the mutagenic males to X^XY female flies that bear attached-X chromosomes, which reverses the inheritance of the poisoned X chromosome so that sons inherit it from their father, in which case only 2% of the progeny are sons. These sex ratio biases suggest that most of the CRISPR/Cas9 mutants we induced in the wupA gene are haplolethal but some are recessive lethal. The males generating wupA mutants do not suffer from reduced fertility; rather, the haplolethal mutants arrest development in the late stages of embryogenesis well after fertilized eggs have been laid. This provides a distinct advantage over genetic manipulation strategies involving sterility which can be countered by the remating of females. We also find that wupA mutants that destroy the nuclear localization signal of shorter isoforms are not haplolethal as long as the open reading frame remains intact. Like D. melanogaster, wupA orthologs of Drosophila suzukii and Anopheles mosquitos are found on X chromosomes making wupA a viable X-poisoning target in multiple species.
MeSH term(s)	Animals ; Female ; Male ; Drosophila/genetics ; Drosophila melanogaster/genetics ; Drosophila Proteins/genetics ; Gene Drive Technology/methods ; Troponin I/genetics ; X Chromosome/genetics
Chemical Substances	Drosophila Proteins ; Troponin I ; wupA protein, Drosophila
Language	English
Publishing date	2024-02-29
Publishing country	England
Document type	Journal Article
ZDB-ID	2629978-1
ISSN	2160-1836 ; 2160-1836
ISSN (online)	2160-1836
ISSN	2160-1836
DOI	10.1093/g3journal/jkae025
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Article: Mining insect genomes for functionally affiliated genes

Perry, Caitlyn / Robin, Charles / Scanlan, Jack

Current opinion in insect science. 2019 Feb., v. 31

2019

Abstract: Several hundred insect genome assemblies are already publicly available, and this total grows on a weekly basis. A major challenge now confronting insect science is how best to use genomic data to improve our understanding of insect biology. We consider ... ...

Abstract	Several hundred insect genome assemblies are already publicly available, and this total grows on a weekly basis. A major challenge now confronting insect science is how best to use genomic data to improve our understanding of insect biology. We consider a framework for genome analysis based on functional affiliation, that is, groups of genes involved in the same biological process or pathway, and explore how such an approach furthers our understanding of several aspects of insect phenotype. We anticipate that this approach will prove useful for future research across the breadth of insect studies, whatever organism or trait it involves.Genome assemblies are an as-yet underutilised resource for understanding phenotypic diversity among insects. Examining genes that act together, for instance in metabolic or developmental pathways, can improve understanding of the molecular basis of insect biodiversity. Elaboration or simplification of genetic networks, particularly at terminal stages, is common in insect evolution. Loss of genes may indicate changes to a pathway or development of alternative mechanisms to maintain it (including complementation by genes of endosymbiotic origin). Genetic model organisms can be poorly representative of insects, and species with contrasting phenotypes should be prioritised for genome sequencing.
Keywords	biodiversity ; evolution ; genes ; genetic models ; genome assembly ; genomics ; insect biology ; insects ; phenotype ; phenotypic variation
Language	English
Dates of publication	2019-02
Size	p. 114-122.
Publishing place	Elsevier Inc.
Document type	Article
ZDB-ID	2772833-X
ISSN	2214-5753 ; 2214-5745
ISSN (online)	2214-5753
ISSN	2214-5745
DOI	10.1016/j.cois.2018.12.006
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Article: What can genetic association panels tell us about evolutionary processes in insects?

Robin, Charles / Battlay, Paul / Fournier-Level, Alexandre

Current opinion in insect science. 2019 Feb., v. 31

2019

Abstract: If we are to fully comprehend the evolution of insect diversity at a genomic level we need to understand how natural selection can alter genetically encoded characters within populations. Genetic association panels have the potential to be standard ... ...

Abstract	If we are to fully comprehend the evolution of insect diversity at a genomic level we need to understand how natural selection can alter genetically encoded characters within populations. Genetic association panels have the potential to be standard bearers in this endeavour. They enable the mapping of phenotypes to genotypes at unprecedented resolution while simultaneously providing population genomic samples that can be interrogated for the tell-tale signs of selection. Analyses of these panels promise to elucidate the entanglement of gene ontologies, pathways, developmental processes and evolutionary constraints, and inform how these are shaped by adaptation.
Keywords	genes ; genomics ; genotype ; insects ; natural selection ; phenotype
Language	English
Dates of publication	2019-02
Size	p. 99-105.
Publishing place	Elsevier Inc.
Document type	Article
ZDB-ID	2772833-X
ISSN	2214-5753 ; 2214-5745
ISSN (online)	2214-5753
ISSN	2214-5745
DOI	10.1016/j.cois.2018.12.004
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Article: Population genomics provides insights into lineage divergence and local adaptation within the cotton bollworm

Zhang, Jianpeng / Zhang, Feng / Tay, Wee Tek / Robin, Charles / Shi, Yu / Guan, Fang / Yang, Yihua / Wu, Yidong

Molecular ecology resources. 2022 July, v. 22, no. 5

2022

Abstract: The cotton bollworm Helicoverpa armigera is a cosmopolitan pest and its diverse habitats plausibly contribute to the formation of diverse lineages. Despite the significant threat it poses to economic crops worldwide, its evolutionary history and genetic ... ...

Abstract	The cotton bollworm Helicoverpa armigera is a cosmopolitan pest and its diverse habitats plausibly contribute to the formation of diverse lineages. Despite the significant threat it poses to economic crops worldwide, its evolutionary history and genetic basis of local adaptation are poorly understood. In this study, we de novo assembled a high‐quality chromosome‐level reference genome of H. a. armigera (contig N50 = 7.34 Mb), with 99.13% of the HaSCD2 assembly assigned to 31 chromosomes (Z‐chromosome + 30 autosomes). We constructed an ultradense variation map across 14 cotton bollworm populations and identified a novel lineage in northwestern China. Historical inference showed that effective population size changes coincided with global temperature fluctuation. We identified nine differentiated genes in the three H. armigera lineages (H. a. armigera, H. a. conferta and the new northwestern Chinese lineage), of which per and clk genes are involved in circadian rhythm. Selective sweep analyses identified a series of Gene Ontology categories related to climate adaptation, feeding behaviour and insecticide tolerance. Our findings reveal fundamental knowledge of the local adaptation of different cotton bollworm lineages and will guide the formulation of cotton bollworm management measures at different scales.
Keywords	Helicoverpa armigera ; Z chromosome ; autosomes ; circadian rhythm ; climate ; effective population size ; gene ontology ; insecticides ; metagenomics ; pests ; temperature ; China
Language	English
Dates of publication	2022-07
Size	p. 1875-1891.
Publishing place	John Wiley & Sons, Ltd
Document type	Article
Note	JOURNAL ARTICLE
ZDB-ID	2406816-0
ISSN	1471-8286 ; 1755-098X
ISSN (online)	1471-8286
ISSN	1755-098X
DOI	10.1111/1755-0998.13581
Database	NAL-Catalogue (AGRICOLA)

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