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Heiko Vogel
Entomology Department, Max-Planck Institute for Chemical Ecology, Hans-Knoell-Strasse 8, 07745 Jena, Germany

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Journal article
Published: 22 July 2021 in Genes
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The clothes moth Tineola bisselliella is one of a few insects that can digest keratin, leading to the destruction of clothing, textiles and artwork. The mechanism of keratin digestion is not yet fully understood, partly reflecting the lack of publicly available genomic and transcriptomic data. Here we present a high-quality gut transcriptome of T. bisselliella generated from larvae reared on keratin-rich and keratin-free diets. The overall transcriptome consists of 428,221 contigs that were functionally annotated and screened for candidate enzymes involved in keratin utilization. As a mechanism for keratin digestion, we identified cysteine synthases, cystathionine β-synthases and cystathionine γ-lyases. These enzymes release hydrogen sulfite, which may reduce the disulfide bonds in keratin. The dataset also included 27 differentially expressed contigs with trypsin domains, among which 20 were associated with keratin feeding. Finally, we identified seven collagenases that were upregulated on the keratin-rich diet. In addition to this enzymatic repertoire potentially involved in breaking down keratin, our analysis of poly(A)-enriched and poly(A)-depleted transcripts suggested that T. bisselliella larvae possess an unstable intestinal microbiome that may nevertheless contribute to keratin digestion.

ACS Style

Michael Schwabe; Sven Griep; Henrike Schmidtberg; Rudy Plarre; Alexander Goesmann; Andreas Vilcinskas; Heiko Vogel; Karina Brinkrolf. Next-Generation Sequencing Analysis of the Tineola bisselliella Larval Gut Transcriptome Reveals Candidate Enzymes for Keratin Digestion. Genes 2021, 12, 1113 .

AMA Style

Michael Schwabe, Sven Griep, Henrike Schmidtberg, Rudy Plarre, Alexander Goesmann, Andreas Vilcinskas, Heiko Vogel, Karina Brinkrolf. Next-Generation Sequencing Analysis of the Tineola bisselliella Larval Gut Transcriptome Reveals Candidate Enzymes for Keratin Digestion. Genes. 2021; 12 (8):1113.

Chicago/Turabian Style

Michael Schwabe; Sven Griep; Henrike Schmidtberg; Rudy Plarre; Alexander Goesmann; Andreas Vilcinskas; Heiko Vogel; Karina Brinkrolf. 2021. "Next-Generation Sequencing Analysis of the Tineola bisselliella Larval Gut Transcriptome Reveals Candidate Enzymes for Keratin Digestion." Genes 12, no. 8: 1113.

Journal article
Published: 14 July 2021 in Biomedicines
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Assassin bug venoms are potent and exert diverse biological functions, making them potential biomedical goldmines. Besides feeding functions on arthropods, assassin bugs also use their venom for defense purposes causing localized and systemic reactions in vertebrates. However, assassin bug venoms remain poorly characterized. We collected the venom from the assassin bug Rhynocoris iracundus and investigated its composition and bioactivity in vitro and in vivo. It caused lysis of murine neuroblastoma, hepatoma cells, and healthy murine myoblasts. We demonstrated, for the first time, that assassin bug venom induces neurolysis and suggest that it counteracts paralysis locally via the destruction of neural networks, contributing to tissue digestion. Furthermore, the venom caused paralysis and melanization of Galleria mellonella larvae and pupae, whilst also possessing specific antibacterial activity against Escherichia coli, but not Listeria grayi and Pseudomonas aeruginosa. A combinatorial proteo-transcriptomic approach was performed to identify potential toxins responsible for the observed effects. We identified neurotoxic Ptu1, an inhibitory cystin knot (ICK) toxin homologous to ω-conotoxins from cone snails, cytolytic redulysins homologous to trialysins from hematophagous kissing bugs, and pore-forming hemolysins. Additionally, chitinases and kininogens were found and may be responsible for insecticidal and cytolytic activities. We demonstrate the multifunctionality and complexity of assassin bug venom, which renders its molecular components interesting for potential biomedical applications.

ACS Style

Nicolai Rügen; Timothy Jenkins; Natalie Wielsch; Heiko Vogel; Benjamin-Florian Hempel; Roderich Süssmuth; Stuart Ainsworth; Alejandro Cabezas-Cruz; Andreas Vilcinskas; Miray Tonk. Hexapod Assassins’ Potion: Venom Composition and Bioactivity from the Eurasian Assassin Bug Rhynocoris iracundus. Biomedicines 2021, 9, 819 .

AMA Style

Nicolai Rügen, Timothy Jenkins, Natalie Wielsch, Heiko Vogel, Benjamin-Florian Hempel, Roderich Süssmuth, Stuart Ainsworth, Alejandro Cabezas-Cruz, Andreas Vilcinskas, Miray Tonk. Hexapod Assassins’ Potion: Venom Composition and Bioactivity from the Eurasian Assassin Bug Rhynocoris iracundus. Biomedicines. 2021; 9 (7):819.

Chicago/Turabian Style

Nicolai Rügen; Timothy Jenkins; Natalie Wielsch; Heiko Vogel; Benjamin-Florian Hempel; Roderich Süssmuth; Stuart Ainsworth; Alejandro Cabezas-Cruz; Andreas Vilcinskas; Miray Tonk. 2021. "Hexapod Assassins’ Potion: Venom Composition and Bioactivity from the Eurasian Assassin Bug Rhynocoris iracundus." Biomedicines 9, no. 7: 819.

Preprint content
Published: 11 June 2021
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Belowground herbivores are overseen and underestimated, even though they can cause significant economic losses in agriculture. The cabbage root fly Delia radicum (Anthomyiidae) is a common pest in Brassica species, including agriculturally important crops, such as oil seed rape. The damage is caused by the larvae, which feed specifically on the taproots of Brassica plants until they pupate. The adults are aboveground-living generalists feeding on pollen and nectar. Female flies are attracted by chemical cues in Brassica plants for oviposition. An assembled and annotated genome can elucidate which genetic mechanisms underlie the adaptation of D. radicum to its host plants and their specific chemical defenses, in particular isothiocyanates. Therefore, we assembled, annotated and analyzed the D. radicum genome using a combination of different Next Generation Sequencing and bioinformatic approaches. We assembled a chromosome-level D. radicum genome using PacBio and Hi-C Illumina sequence data. Combining Canu and 3D-DNA genome assembler, we constructed a 1.3 Gbp genome with an N50 of 242 Mbp and 6 pseudo-chromosomes. To annotate the assembled D. radicum genome, we combined homology-, transcriptome- and ab initio-prediction approaches. In total, we annotated 13,618 genes that were predicted by at least two approaches. We analyzed egg, larval, pupal and adult transcriptomes in relation to life-stage specific molecular functions. This high-quality annotated genome of D. radicum is a first step to understanding the genetic mechanisms underlying host plant adaptation. As such, it will be an important resource to find novel and sustainable approaches to reduce crop losses to these pests.

ACS Style

Rebekka Sontowski; Yvonne Poeschl; Yu Okamura; Heiko Vogel; Cervin Guyomar; Anne-Marie Cortesero; Nicole M. van Dam. A high-quality functional genome assembly of Delia radicum L. (Diptera: Anthomiidae) annotated from egg to adult. 2021, 1 .

AMA Style

Rebekka Sontowski, Yvonne Poeschl, Yu Okamura, Heiko Vogel, Cervin Guyomar, Anne-Marie Cortesero, Nicole M. van Dam. A high-quality functional genome assembly of Delia radicum L. (Diptera: Anthomiidae) annotated from egg to adult. . 2021; ():1.

Chicago/Turabian Style

Rebekka Sontowski; Yvonne Poeschl; Yu Okamura; Heiko Vogel; Cervin Guyomar; Anne-Marie Cortesero; Nicole M. van Dam. 2021. "A high-quality functional genome assembly of Delia radicum L. (Diptera: Anthomiidae) annotated from egg to adult." , no. : 1.

Journal article
Published: 11 May 2021 in Nature Communications
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Many herbivorous insects selectively accumulate plant toxins for defense against predators; however, little is known about the transport processes that enable insects to absorb and store defense compounds in the body. Here, we investigate how a specialist herbivore, the horseradish flea beetle, accumulates glucosinolate defense compounds from Brassicaceae in the hemolymph. Using phylogenetic analyses of coleopteran major facilitator superfamily transporters, we identify a clade of glucosinolate-specific transporters (PaGTRs) belonging to the sugar porter family. PaGTRs are predominantly expressed in the excretory system, the Malpighian tubules. Silencing of PaGTRs leads to elevated glucosinolate excretion, significantly reducing the levels of sequestered glucosinolates in beetles. This suggests that PaGTRs reabsorb glucosinolates from the Malpighian tubule lumen to prevent their loss by excretion. Ramsay assays corroborated the selective retention of glucosinolates by Malpighian tubules of P. armoraciae in situ. Thus, the selective accumulation of plant defense compounds in herbivorous insects can depend on the ability to prevent excretion.

ACS Style

Zhi-Ling Yang; Hussam Hassan Nour-Eldin; Sabine Hänniger; Michael Reichelt; Christoph Crocoll; Fabian Seitz; Heiko Vogel; Franziska Beran. Sugar transporters enable a leaf beetle to accumulate plant defense compounds. Nature Communications 2021, 12, 1 -12.

AMA Style

Zhi-Ling Yang, Hussam Hassan Nour-Eldin, Sabine Hänniger, Michael Reichelt, Christoph Crocoll, Fabian Seitz, Heiko Vogel, Franziska Beran. Sugar transporters enable a leaf beetle to accumulate plant defense compounds. Nature Communications. 2021; 12 (1):1-12.

Chicago/Turabian Style

Zhi-Ling Yang; Hussam Hassan Nour-Eldin; Sabine Hänniger; Michael Reichelt; Christoph Crocoll; Fabian Seitz; Heiko Vogel; Franziska Beran. 2021. "Sugar transporters enable a leaf beetle to accumulate plant defense compounds." Nature Communications 12, no. 1: 1-12.

Journal article
Published: 16 April 2021 in International Journal of Molecular Sciences
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Flower colour is an important trait for plants to attract pollinators and ensure their reproductive success. Among yellow flower pigments, the nudicaulins in Papaver nudicaule L. (Iceland poppy) are unique due to their rarity and unparalleled flavoalkaloid structure. Nudicaulins are derived from pelargonidin glycoside and indole, products of the flavonoid and indole/tryptophan biosynthetic pathway, respectively. To gain insight into the molecular and chemical basis of nudicaulin biosynthesis, we combined transcriptome, differential gel electrophoresis (DIGE)-based proteome, and ultra-performance liquid chromatography–high resolution mass spectrometry (UPLC-HRMS)-based metabolome data of P. nudicaule petals with chemical investigations. We identified candidate genes and proteins for all biosynthetic steps as well as some key metabolites across five stages of petal development. Candidate genes of amino acid biosynthesis showed a relatively stable expression throughout petal development, whereas most candidate genes of flavonoid biosynthesis showed increasing expression during development followed by downregulation in the final stage. Notably, gene candidates of indole-3-glycerol-phosphate lyase (IGL), sharing characteristic sequence motifs with known plant IGL genes, were co-expressed with flavonoid biosynthesis genes, and are probably providing free indole. The fusion of indole with pelargonidin glycosides was retraced synthetically and promoted by high precursor concentrations, an excess of indole, and a specific glycosylation pattern of pelargonidin. Thus, nudicaulin biosynthesis combines the enzymatic steps of two different pathways with a spontaneous fusion of indole and pelargonidin glycoside under precisely tuned reaction conditions.

ACS Style

Bettina Dudek; Anne-Christin Warskulat; Heiko Vogel; Natalie Wielsch; Riya Menezes; Yvonne Hupfer; Christian Paetz; Steffi Gebauer-Jung; Aleš Svatoš; Bernd Schneider. An Integrated—Omics/Chemistry Approach Unravels Enzymatic and Spontaneous Steps to Form Flavoalkaloidal Nudicaulin Pigments in Flowers of Papaver nudicaule L. International Journal of Molecular Sciences 2021, 22, 4129 .

AMA Style

Bettina Dudek, Anne-Christin Warskulat, Heiko Vogel, Natalie Wielsch, Riya Menezes, Yvonne Hupfer, Christian Paetz, Steffi Gebauer-Jung, Aleš Svatoš, Bernd Schneider. An Integrated—Omics/Chemistry Approach Unravels Enzymatic and Spontaneous Steps to Form Flavoalkaloidal Nudicaulin Pigments in Flowers of Papaver nudicaule L. International Journal of Molecular Sciences. 2021; 22 (8):4129.

Chicago/Turabian Style

Bettina Dudek; Anne-Christin Warskulat; Heiko Vogel; Natalie Wielsch; Riya Menezes; Yvonne Hupfer; Christian Paetz; Steffi Gebauer-Jung; Aleš Svatoš; Bernd Schneider. 2021. "An Integrated—Omics/Chemistry Approach Unravels Enzymatic and Spontaneous Steps to Form Flavoalkaloidal Nudicaulin Pigments in Flowers of Papaver nudicaule L." International Journal of Molecular Sciences 22, no. 8: 4129.

Journal article
Published: 09 April 2021 in BMC Plant Biology
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Background Protease inhibitors are defense proteins widely distributed in the plant kingdom. By reducing the activity of digestive enzymes in insect guts, they reduce the availability of nutrients and thus impair the growth and development of the attacking herbivore. One well-characterized class of protease inhibitors are Kunitz-type trypsin inhibitors (KTIs), which have been described in various plant species, including Populus spp. Long-lived woody perennials like poplar trees encounter a huge diversity of herbivores, but the specificity of tree defenses towards different herbivore species is hardly studied. We therefore aimed to investigate the induction of KTIs in black poplar (P. nigra) leaves upon herbivory by three different chewing herbivores, Lymantria dispar and Amata mogadorensis caterpillars, and Phratora vulgatissima beetles. Results We identified and generated full-length cDNA sequences of 17 KTIs that are upregulated upon herbivory in black poplar leaves, and analyzed the expression patterns of the eight most up-regulated KTIs via qRT-PCR. We found that beetles elicited higher transcriptional induction of KTIs than caterpillars, and that both caterpillar species induced similar KTI expression levels. Furthermore, KTI expression strongly correlated with the trypsin-inhibiting activity in the herbivore-damaged leaves, but was not dependent on damage severity, i.e. leaf area loss, for most of the genes. Conclusions We conclude that the induction of KTIs in black poplar is controlled at the transcriptional level in a threshold-based manner and is strongly influenced by the species identity of the herbivore. However, the underlying molecular mechanisms and ecological consequences of these patterns remain to be investigated.

ACS Style

Franziska Eberl; Thomas Fabisch; Katrin Luck; Tobias G. Köllner; Heiko Vogel; Jonathan Gershenzon; Sybille B. Unsicker. Poplar protease inhibitor expression differs in an herbivore specific manner. BMC Plant Biology 2021, 21, 1 -11.

AMA Style

Franziska Eberl, Thomas Fabisch, Katrin Luck, Tobias G. Köllner, Heiko Vogel, Jonathan Gershenzon, Sybille B. Unsicker. Poplar protease inhibitor expression differs in an herbivore specific manner. BMC Plant Biology. 2021; 21 (1):1-11.

Chicago/Turabian Style

Franziska Eberl; Thomas Fabisch; Katrin Luck; Tobias G. Köllner; Heiko Vogel; Jonathan Gershenzon; Sybille B. Unsicker. 2021. "Poplar protease inhibitor expression differs in an herbivore specific manner." BMC Plant Biology 21, no. 1: 1-11.

Journal article
Published: 19 March 2021 in Genome Biology and Evolution
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We report a chromosome-level assembly for Pieris macdunnoughii, a North American butterfly whose involvement in an evolutionary trap imposed by an invasive Eurasian mustard has made it an emerging model system for studying maladaptation in plant–insect interactions. Assembled using nearly 100× coverage of Oxford Nanopore long reads, the contig-level assembly comprised 106 contigs totaling 316,549,294 bases, with an N50 of 5.2 Mb. We polished the assembly with PoolSeq Illumina short-read data, demonstrating for the first time the comparable performance of individual and pooled short reads as polishing data sets. Extensive synteny between the reported contig-level assembly and a published, chromosome-level assembly of the European butterfly Pieris napi allowed us to generate a pseudochromosomal assembly of 47 contigs, placing 91.1% of our 317 Mb genome into a chromosomal framework. Additionally, we found support for a Z chromosome arrangement in P. napi, showing that the fusion event leading to this rearrangement predates the split between European and North American lineages of Pieris butterflies. This genome assembly and its functional annotation lay the groundwork for future research into the genetic basis of adaptive and maladaptive egg-laying behavior by P. macdunnoughii, contributing to our understanding of the susceptibility and responses of insects to evolutionary traps.

ACS Style

Rachel A Steward; Yu Okamura; Carol L Boggs; Heiko Vogel; Christopher W Wheat. The Genome of the Margined White Butterfly (Pieris macdunnoughii): Sex Chromosome Insights and the Power of Polishing with PoolSeq Data. Genome Biology and Evolution 2021, 13, 1 .

AMA Style

Rachel A Steward, Yu Okamura, Carol L Boggs, Heiko Vogel, Christopher W Wheat. The Genome of the Margined White Butterfly (Pieris macdunnoughii): Sex Chromosome Insights and the Power of Polishing with PoolSeq Data. Genome Biology and Evolution. 2021; 13 (4):1.

Chicago/Turabian Style

Rachel A Steward; Yu Okamura; Carol L Boggs; Heiko Vogel; Christopher W Wheat. 2021. "The Genome of the Margined White Butterfly (Pieris macdunnoughii): Sex Chromosome Insights and the Power of Polishing with PoolSeq Data." Genome Biology and Evolution 13, no. 4: 1.

Journal article
Published: 03 March 2021 in Scientific Reports
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During oviposition, ectoparasitoid wasps not only inject their eggs but also a complex mixture of proteins and peptides (venom) in order to regulate the host physiology to benefit their progeny. Although several endoparasitoid venom proteins have been identified, little is known about the components of ectoparasitoid venom. To characterize the protein composition of Torymus sinensis Kamijo (Hymenoptera: Torymidae) venom, we used an integrated transcriptomic and proteomic approach and identified 143 venom proteins. Moreover, focusing on venom gland transcriptome, we selected additional 52 transcripts encoding putative venom proteins. As in other parasitoid venoms, hydrolases, including proteases, phosphatases, esterases, and nucleases, constitute the most abundant families in T. sinensis venom, followed by protease inhibitors. These proteins are potentially involved in the complex parasitic syndrome, with different effects on the immune system, physiological processes and development of the host, and contribute to provide nutrients to the parasitoid progeny. Although additional in vivo studies are needed, initial findings offer important information about venom factors and their putative host effects, which are essential to ensure the success of parasitism.

ACS Style

Carmen Scieuzo; Rosanna Salvia; Antonio Franco; Marco Pezzi; Flora Cozzolino; Milvia Chicca; Chiara Scapoli; Heiko Vogel; Maria Monti; Chiara Ferracini; Pietro Pucci; Alberto Alma; Patrizia Falabella. An integrated transcriptomic and proteomic approach to identify the main Torymus sinensis venom components. Scientific Reports 2021, 11, 1 -25.

AMA Style

Carmen Scieuzo, Rosanna Salvia, Antonio Franco, Marco Pezzi, Flora Cozzolino, Milvia Chicca, Chiara Scapoli, Heiko Vogel, Maria Monti, Chiara Ferracini, Pietro Pucci, Alberto Alma, Patrizia Falabella. An integrated transcriptomic and proteomic approach to identify the main Torymus sinensis venom components. Scientific Reports. 2021; 11 (1):1-25.

Chicago/Turabian Style

Carmen Scieuzo; Rosanna Salvia; Antonio Franco; Marco Pezzi; Flora Cozzolino; Milvia Chicca; Chiara Scapoli; Heiko Vogel; Maria Monti; Chiara Ferracini; Pietro Pucci; Alberto Alma; Patrizia Falabella. 2021. "An integrated transcriptomic and proteomic approach to identify the main Torymus sinensis venom components." Scientific Reports 11, no. 1: 1-25.

Review
Published: 17 February 2021 in Experientia
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Misuse and overuse of antibiotics have contributed in the last decades to a phenomenon known as antibiotic resistance which is currently considered one of the principal threats to global public health by the World Health Organization. The aim to find alternative drugs has been demonstrated as a real challenge. Thanks to their biodiversity, insects represent the largest class of organisms in the animal kingdom. The humoral immune response includes the production of antimicrobial peptides (AMPs) that are released into the insect hemolymph after microbial infection. In this review, we have focused on insect immune responses, particularly on AMP characteristics, their mechanism of action and applications, especially in the biomedical field. Furthermore, we discuss the Toll, Imd, and JAK-STAT pathways that activate genes encoding for the expression of AMPs. Moreover, we focused on strategies to improve insect peptides stability against proteolytic susceptibility such as D-amino acid substitutions, N-terminus modification, cyclization and dimerization.

ACS Style

M. D. Manniello; A. Moretta; R. Salvia; C. Scieuzo; D. Lucchetti; H. Vogel; A. Sgambato; P. Falabella. Insect antimicrobial peptides: potential weapons to counteract the antibiotic resistance. Experientia 2021, 78, 4259 -4282.

AMA Style

M. D. Manniello, A. Moretta, R. Salvia, C. Scieuzo, D. Lucchetti, H. Vogel, A. Sgambato, P. Falabella. Insect antimicrobial peptides: potential weapons to counteract the antibiotic resistance. Experientia. 2021; 78 (9):4259-4282.

Chicago/Turabian Style

M. D. Manniello; A. Moretta; R. Salvia; C. Scieuzo; D. Lucchetti; H. Vogel; A. Sgambato; P. Falabella. 2021. "Insect antimicrobial peptides: potential weapons to counteract the antibiotic resistance." Experientia 78, no. 9: 4259-4282.

Editorial
Published: 01 October 2020 in Current Opinion in Insect Science
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ACS Style

Spencer T Behmer; Heiko Vogel. Editorial overview: Molecular physiology of the multifunctional insect gut. Current Opinion in Insect Science 2020, 41, 1 .

AMA Style

Spencer T Behmer, Heiko Vogel. Editorial overview: Molecular physiology of the multifunctional insect gut. Current Opinion in Insect Science. 2020; 41 ():1.

Chicago/Turabian Style

Spencer T Behmer; Heiko Vogel. 2020. "Editorial overview: Molecular physiology of the multifunctional insect gut." Current Opinion in Insect Science 41, no. : 1.

Journal article
Published: 14 September 2020 in Microorganisms
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The evolutionary success of insects is promoted by their association with beneficial microbes that enable the utilization of unusual diets. The synanthropic clothing moth Tineola bisselliella provides an intriguing example of this phenomenon. The caterpillars of this species have adapted to feed on keratin-rich diets such as feathers and wool, which cannot be digested by most other animals and are resistant to common digestive enzymes. Inspired by the hypothesis that this ability may be conferred by symbiotic microbes, we utilized a simple assay to detect keratinase activity and a method to screen gut bacteria for candidate enzymes, which were isolated from feather-fed larvae. The isolation of DNA from keratin-degrading bacterial strains followed by de novo genome sequencing resulted in the identification of a novel bacterial strain related to Bacillus sp. FDAARGOS_235. Genome annotation identified 20 genes with keratinase domains. Proteomic analysis of the culture supernatant from this gut bacterium grown in non-nutrient buffer supplemented with feathers revealed several candidate enzymes potentially responsible for keratin degradation, including a thiol-disulfide oxidoreductase and multiple proteases. Our results suggest that the unusual diet of T. bisselliella larvae promotes their association with keratinolytic microorganisms and that the ability of larvae to feed on keratin can at least partially be attributed to bacteria that produce a cocktail of keratin-degrading enzymes.

ACS Style

Andreas Vilcinskas; Michael Schwabe; Karina Brinkrolf; Rudy Plarre; Natalie Wielsch; Heiko Vogel. Larvae of the Clothing Moth Tineola bisselliella Maintain Gut Bacteria that Secrete Enzyme Cocktails to Facilitate the Digestion of Keratin. Microorganisms 2020, 8, 1415 .

AMA Style

Andreas Vilcinskas, Michael Schwabe, Karina Brinkrolf, Rudy Plarre, Natalie Wielsch, Heiko Vogel. Larvae of the Clothing Moth Tineola bisselliella Maintain Gut Bacteria that Secrete Enzyme Cocktails to Facilitate the Digestion of Keratin. Microorganisms. 2020; 8 (9):1415.

Chicago/Turabian Style

Andreas Vilcinskas; Michael Schwabe; Karina Brinkrolf; Rudy Plarre; Natalie Wielsch; Heiko Vogel. 2020. "Larvae of the Clothing Moth Tineola bisselliella Maintain Gut Bacteria that Secrete Enzyme Cocktails to Facilitate the Digestion of Keratin." Microorganisms 8, no. 9: 1415.

Original research
Published: 17 August 2020 in Ecology and Evolution
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The Heteroptera are a diverse suborder of phytophagous, hematophagous, and zoophagous insects. The shift to zoophagy can be traced back to the transformation of salivary glands into venom glands, but the venom is used not only to kill and digest invertebrate prey but also as a defense strategy, mainly against vertebrates. In this study, we used an integrated transcriptomics and proteomics approach to compare the composition of venoms from the anterior main gland (AMG) and posterior main gland (PMG) of the reduviid bugs Platymeris biguttatus L. and Psytalla horrida Stål. In both species, the AMG and PMG secreted distinct protein mixtures with few interspecific differences. PMG venom consisted mostly of S1 proteases, redulysins, Ptu1‐like peptides, and uncharacterized proteins, whereas AMG venom contained hemolysins and cystatins. There was a remarkable difference in biological activity between the AMG and PMG venoms, with only PMG venom conferring digestive, neurotoxic, hemolytic, antibacterial, and cytotoxic effects. Proteomic analysis of venom samples revealed the context‐dependent use of AMG and PMG venom. Although both species secreted PMG venom alone to overwhelm their prey and facilitate digestion, the deployment of defensive venom was species‐dependent. P. biguttatus almost exclusively used PMG venom for defense, whereas P. horrida secreted PMG venom in response to mild harassment but AMG venom in response to more intense harassment. This intriguing context‐dependent use of defensive venom indicates that future research should focus on species‐dependent differences in venom composition and defense strategies among predatory Heteroptera.

ACS Style

Maike L. Fischer; Natalie Wielsch; David G. Heckel; Andreas Vilcinskas; Heiko Vogel. Context‐dependent venom deployment and protein composition in two assassin bugs. Ecology and Evolution 2020, 10, 9932 -9947.

AMA Style

Maike L. Fischer, Natalie Wielsch, David G. Heckel, Andreas Vilcinskas, Heiko Vogel. Context‐dependent venom deployment and protein composition in two assassin bugs. Ecology and Evolution. 2020; 10 (18):9932-9947.

Chicago/Turabian Style

Maike L. Fischer; Natalie Wielsch; David G. Heckel; Andreas Vilcinskas; Heiko Vogel. 2020. "Context‐dependent venom deployment and protein composition in two assassin bugs." Ecology and Evolution 10, no. 18: 9932-9947.

Journal article
Published: 25 April 2020 in Microorganisms
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The spread of multidrug-resistant Gram-negative bacteria is an increasing threat to human health, because novel compound classes for the development of antibiotics have not been discovered for decades. Antimicrobial peptides (AMPs) may provide a much-needed breakthrough because these immunity-related defense molecules protect many eukaryotes against Gram-negative pathogens. Recent concepts in evolutionary immunology predict the presence of potent AMPs in insects that have adapted to survive in habitats with extreme microbial contamination. For example, the saprophagous and coprophagous maggots of the drone fly Eristalis tenax (Diptera) can flourish in polluted aquatic habitats, such as sewage tanks and farmyard liquid manure storage pits. We used next-generation sequencing to screen the E. tenax immunity-related transcriptome for AMPs that are synthesized in response to the injection of bacterial lipopolysaccharide. We identified 22 AMPs and selected nine for larger-scale synthesis to test their activity against a broad spectrum of pathogens, including multidrug-resistant Gram-negative bacteria. Two cecropin-like peptides (EtCec1-a and EtCec2-a) and a diptericin-like peptide (EtDip) displayed strong activity against the pathogens, even under simulated physiological conditions, and also achieved a good therapeutic window. Therefore, these AMPs could be used as leads for the development of novel antibiotics.

ACS Style

Rolf Hirsch; Jochen Wiesner; Armin Bauer; Alexander Marker; Heiko Vogel; Peter Eugen Hammann; Andreas Vilcinskas. Antimicrobial Peptides from Rat-Tailed Maggots of the Drone Fly Eristalis tenax Show Potent Activity against Multidrug-Resistant Gram-Negative Bacteria. Microorganisms 2020, 8, 626 .

AMA Style

Rolf Hirsch, Jochen Wiesner, Armin Bauer, Alexander Marker, Heiko Vogel, Peter Eugen Hammann, Andreas Vilcinskas. Antimicrobial Peptides from Rat-Tailed Maggots of the Drone Fly Eristalis tenax Show Potent Activity against Multidrug-Resistant Gram-Negative Bacteria. Microorganisms. 2020; 8 (5):626.

Chicago/Turabian Style

Rolf Hirsch; Jochen Wiesner; Armin Bauer; Alexander Marker; Heiko Vogel; Peter Eugen Hammann; Andreas Vilcinskas. 2020. "Antimicrobial Peptides from Rat-Tailed Maggots of the Drone Fly Eristalis tenax Show Potent Activity against Multidrug-Resistant Gram-Negative Bacteria." Microorganisms 8, no. 5: 626.

Journal article
Published: 07 February 2020 in Scientific Reports
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An animal’s fitness strongly depends on successful feeding, avoidance of predators and reproduction. All of these behaviours commonly involve chemosensation. As a consequence, when species’ ecological niches and life histories differ, their chemosensory abilities need to be adapted accordingly. The intertidal insect Clunio marinus (Diptera: Chironomidae) has tuned its olfactory system to two highly divergent niches. The long-lived larvae forage in a marine environment. During the few hours of terrestrial adult life, males have to find the female pupae floating on the water surface, free the cryptic females from their pupal skin, copulate and carry the females to the oviposition sites. In order to explore the possibility for divergent olfactory adaptations within the same species, we investigated the chemosensory system of C. marinus larvae, adult males and adult females at the morphological and molecular level. The larvae have a well-developed olfactory system, but olfactory gene expression only partially overlaps with that of adults, likely reflecting their marine vs. terrestrial lifestyles. The olfactory system of the short-lived adults is simple, displaying no glomeruli in the antennal lobes. There is strong sexual dimorphism, the female olfactory system being particularly reduced in terms of number of antennal annuli and sensilla, olfactory brain centre size and gene expression. We found hints for a pheromone detection system in males, including large trichoid sensilla and expression of specific olfactory receptors and odorant binding proteins. Taken together, this makes C. marinus an excellent model to study within-species evolution and adaptation of chemosensory systems.

ACS Style

Christine Missbach; Heiko Vogel; Bill S. Hansson; Ewald Große-Wilde; Andreas Vilcinskas; Tobias S. Kaiser. Developmental and sexual divergence in the olfactory system of the marine insect Clunio marinus. Scientific Reports 2020, 10, 1 -17.

AMA Style

Christine Missbach, Heiko Vogel, Bill S. Hansson, Ewald Große-Wilde, Andreas Vilcinskas, Tobias S. Kaiser. Developmental and sexual divergence in the olfactory system of the marine insect Clunio marinus. Scientific Reports. 2020; 10 (1):1-17.

Chicago/Turabian Style

Christine Missbach; Heiko Vogel; Bill S. Hansson; Ewald Große-Wilde; Andreas Vilcinskas; Tobias S. Kaiser. 2020. "Developmental and sexual divergence in the olfactory system of the marine insect Clunio marinus." Scientific Reports 10, no. 1: 1-17.

Journal article
Published: 10 December 2019 in Toxins
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Within mega-diverse Hymenoptera, non-aculeate parasitic wasps represent 75% of all hymenopteran species. Their ovipositor dual-functionally injects venom and employs eggs into (endoparasitoids) or onto (ectoparasitoids) diverse host species. Few endoparasitoid wasps such as Pimpla turionellae paralyze the host and suppress its immune responses, such as encapsulation and melanization, to guarantee their offspring’s survival. Here, the venom and its possible biology and function of P. turionellae are characterized in comparison to the few existing proteo-transcriptomic analyses on parasitoid wasp venoms. Multiple transcriptome assembly and custom-tailored search and annotation strategies were applied to identify parasitoid venom proteins. To avoid false-positive hits, only transcripts were finally discussed that survived strict filter settings, including the presence in the proteome and higher expression in the venom gland. P. turionella features a venom that is mostly composed of known, typical parasitoid enzymes, cysteine-rich peptides, and other proteins and peptides. Several venom proteins were identified and named, such as pimplin2, 3, and 4. However, the specification of many novel candidates remains difficult, and annotations ambiguous. Interestingly, we do not find pimplin, a paralytic factor in Pimpla hypochondriaca, but instead a new cysteine inhibitor knot (ICK) family (pimplin2), which is highly similar to known, neurotoxic asilid1 sequences from robber flies.

ACS Style

Rabia Özbek; Natalie Wielsch; Heiko Vogel; Günter Lochnit; Frank Förster; Andreas Vilcinskas; Björn Marcus Von Reumont. Proteo-Transcriptomic Characterization of the Venom from the Endoparasitoid Wasp Pimpla turionellae with Aspects on Its Biology and Evolution. Toxins 2019, 11, 721 .

AMA Style

Rabia Özbek, Natalie Wielsch, Heiko Vogel, Günter Lochnit, Frank Förster, Andreas Vilcinskas, Björn Marcus Von Reumont. Proteo-Transcriptomic Characterization of the Venom from the Endoparasitoid Wasp Pimpla turionellae with Aspects on Its Biology and Evolution. Toxins. 2019; 11 (12):721.

Chicago/Turabian Style

Rabia Özbek; Natalie Wielsch; Heiko Vogel; Günter Lochnit; Frank Förster; Andreas Vilcinskas; Björn Marcus Von Reumont. 2019. "Proteo-Transcriptomic Characterization of the Venom from the Endoparasitoid Wasp Pimpla turionellae with Aspects on Its Biology and Evolution." Toxins 11, no. 12: 721.

Preprint content
Published: 21 November 2019
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Evidence is accumulating that evolutionary changes are not only common during biological invasions but may also contribute directly to invasion success. The genomic basis of such changes is still largely unexplored. Yet, understanding the genomic response to invasion may help to predict the conditions under which invasiveness can be enhanced or suppressed. Here we characterized the genome response of the spotted wing drosophilaDrosophila suzukiiduring the worldwide invasion of this pest insect species, by conducting a genome-wide association study to identify genes involved in adaptive processes during invasion. Genomic data from 22 population samples were analyzed to detect genetic variants associated with the status (invasive versus native) of the sampled populations based on a newly developed statistic, we calledC 2, that contrasts allele frequencies corrected for population structure. This new statistical framework has been implemented in an upgraded version of the program BayPass. We identified a relatively small set of single nucleotide polymorphisms (SNPs) that show a highly significant association with the invasive status of populations. In particular, two genesRhoGEF64Candcpo, the latter contributing to natural variation in several life-history traits (including diapause) inDrosophila melanogaster, contained SNPs significantly associated with the invasive status in the two separate main invasion routes ofD. suzukii. Our methodological approaches can be applied to any other invasive species, and more generally to any evolutionary model for species characterized by non-equilibrium demographic conditions for which binary covariables of interest can be defined at the population level.

ACS Style

Laure Olazcuaga; Anne Loiseau; Hugues Parrinello; Mathilde Paris; Antoine Fraimout; Christelle Guedot; Lauren M. Diepenbrock; Marc Kenis; Jinping Zhang; Xiao Chen; Nicolas Borowieck; Benoit Facon; Heidrun Vogt; Donald K. Price; Heiko Vogel; Benjamin Prud’Homme; Arnaud Estoup; Mathieu Gautier. A whole-genome scan for association with invasion success in the fruit flyDrosophila suzukiiusing contrasts of allele frequencies corrected for population structure. 2019, 851303 .

AMA Style

Laure Olazcuaga, Anne Loiseau, Hugues Parrinello, Mathilde Paris, Antoine Fraimout, Christelle Guedot, Lauren M. Diepenbrock, Marc Kenis, Jinping Zhang, Xiao Chen, Nicolas Borowieck, Benoit Facon, Heidrun Vogt, Donald K. Price, Heiko Vogel, Benjamin Prud’Homme, Arnaud Estoup, Mathieu Gautier. A whole-genome scan for association with invasion success in the fruit flyDrosophila suzukiiusing contrasts of allele frequencies corrected for population structure. . 2019; ():851303.

Chicago/Turabian Style

Laure Olazcuaga; Anne Loiseau; Hugues Parrinello; Mathilde Paris; Antoine Fraimout; Christelle Guedot; Lauren M. Diepenbrock; Marc Kenis; Jinping Zhang; Xiao Chen; Nicolas Borowieck; Benoit Facon; Heidrun Vogt; Donald K. Price; Heiko Vogel; Benjamin Prud’Homme; Arnaud Estoup; Mathieu Gautier. 2019. "A whole-genome scan for association with invasion success in the fruit flyDrosophila suzukiiusing contrasts of allele frequencies corrected for population structure." , no. : 851303.

Preprint content
Published: 14 November 2019
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Background Parasitoid wasps have fascinating life cycles and play an important role in trophic networks, yet little is known about their genome content and function. Parasitoids that infect aphids are an important group with the potential for biocontrol, and infecting aphids requires overcoming both aphid defenses and their defensive endosymbionts. Results We present thede novogenome assemblies, detailed annotation, and comparative analysis of two closely related parasitoid wasps that target pest aphids:Aphidius erviandLysiphlebus fabarum(Hymenoptera: Braconidae: Aphidiinae). The genomes are small (139 and 141 Mbp), highly syntenic, and the most AT-rich reported thus far for any arthropod (GC content: 25.8% and 23.8%). This nucleotide bias is accompanied by skewed codon usage, and is stronger in genes with adult-biased expression. AT-richness may be the consequence of reduced genome size, a near absence of DNA methylation, and age-specific energy demands. We identify expansions of F-box/Leucine-rich-repeat proteins, suggesting that diversification in this gene family may be associated with their broad host range or with countering defenses from aphids’ endosymbionts. The absence of some immune genes (Toll and Imd pathways) resembles similar losses in their aphid hosts, highlighting the potential impact of symbiosis on both aphids and their parasitoids. Conclusions These findings are of fundamental interest for insect evolution and beyond. This will provide a strong foundation for further functional studies including coevolution with respect to their hosts, the basis of successful infection, and biocontrol. Both genomes are available athttps://bipaa.genouest.org.

ACS Style

Alice B. Dennis; Gabriel I. Ballesteros; Stéphanie Robin; Lukas Schrader; Jens Bast; Jan Berghöfer; Leo Beukeboom; Maya Belghazi; Anthony Bretaudeau; Jan Büllesbach; Elizabeth Cash; Dominique Colinet; Zoé Dumas; Patrizia Falabella; Jean-Luc Gatti; Elzemiek Geuverink; Joshua D. Gibson; Corinne Hertäg; Stefanie Hartmann; Emmanuelle Jacquin-Joly; Mark Lammers; Blas I. Lavandero; Ina Lindenbaum; Lauriane Massardier-Galata; Camille Meslin; Nicolas Montagné; Nina Pak; Marylène Poirié; Rosanna Salvia; Chris R. Smith; Denis Tagu; Sophie Tares; Heiko Vogel; Tanja Schwander; Jean-Christophe Simon; Christian C. Figueroa; Christoph Vorburger; Fabrice Legeai; Jürgen Gadau. Functional insights from the GC-poor genomes of two aphid parasitoids,Aphidius erviandLysiphlebus fabarum. 2019, 841288 .

AMA Style

Alice B. Dennis, Gabriel I. Ballesteros, Stéphanie Robin, Lukas Schrader, Jens Bast, Jan Berghöfer, Leo Beukeboom, Maya Belghazi, Anthony Bretaudeau, Jan Büllesbach, Elizabeth Cash, Dominique Colinet, Zoé Dumas, Patrizia Falabella, Jean-Luc Gatti, Elzemiek Geuverink, Joshua D. Gibson, Corinne Hertäg, Stefanie Hartmann, Emmanuelle Jacquin-Joly, Mark Lammers, Blas I. Lavandero, Ina Lindenbaum, Lauriane Massardier-Galata, Camille Meslin, Nicolas Montagné, Nina Pak, Marylène Poirié, Rosanna Salvia, Chris R. Smith, Denis Tagu, Sophie Tares, Heiko Vogel, Tanja Schwander, Jean-Christophe Simon, Christian C. Figueroa, Christoph Vorburger, Fabrice Legeai, Jürgen Gadau. Functional insights from the GC-poor genomes of two aphid parasitoids,Aphidius erviandLysiphlebus fabarum. . 2019; ():841288.

Chicago/Turabian Style

Alice B. Dennis; Gabriel I. Ballesteros; Stéphanie Robin; Lukas Schrader; Jens Bast; Jan Berghöfer; Leo Beukeboom; Maya Belghazi; Anthony Bretaudeau; Jan Büllesbach; Elizabeth Cash; Dominique Colinet; Zoé Dumas; Patrizia Falabella; Jean-Luc Gatti; Elzemiek Geuverink; Joshua D. Gibson; Corinne Hertäg; Stefanie Hartmann; Emmanuelle Jacquin-Joly; Mark Lammers; Blas I. Lavandero; Ina Lindenbaum; Lauriane Massardier-Galata; Camille Meslin; Nicolas Montagné; Nina Pak; Marylène Poirié; Rosanna Salvia; Chris R. Smith; Denis Tagu; Sophie Tares; Heiko Vogel; Tanja Schwander; Jean-Christophe Simon; Christian C. Figueroa; Christoph Vorburger; Fabrice Legeai; Jürgen Gadau. 2019. "Functional insights from the GC-poor genomes of two aphid parasitoids,Aphidius erviandLysiphlebus fabarum." , no. : 841288.

Journal article
Published: 12 June 2019 in Science Advances
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Chromosome evolution presents an enigma in the mega-diverse Lepidoptera. Most species exhibit constrained chromosome evolution with nearly identical haploid chromosome counts and chromosome-level gene collinearity among species more than 140 million years divergent. However, a few species possess radically inflated chromosomal counts due to extensive fission and fusion events. To address this enigma of constraint in the face of an exceptional ability to change, we investigated an unprecedented reorganization of the standard lepidopteran chromosome structure in the green-veined white butterfly (Pieris napi). We find that gene content in P. napi has been extensively rearranged in large collinear blocks, which until now have been masked by a haploid chromosome number close to the lepidopteran average. We observe that ancient chromosome ends have been maintained and collinear blocks are enriched for functionally related genes suggesting both a mechanism and a possible role for selection in determining the boundaries of these genome-wide rearrangements.

ACS Style

Jason Hill; Pasi Rastas; Emily A. Hornett; Ramprasad Neethiraj; Nathan Clark; Nathan Morehouse; Maria De La Paz Celorio-Mancera; Jofre Carnicer Cols; Heinrich Dircksen; Camille Meslin; Naomi Keehnen; Peter Pruisscher; Kristin Sikkink; Maria Vives; Heiko Vogel; Christer Wiklund; Alyssa Woronik; Carol L. Boggs; Sören Nylin; Christopher W. Wheat. Unprecedented reorganization of holocentric chromosomes provides insights into the enigma of lepidopteran chromosome evolution. Science Advances 2019, 5, eaau3648 .

AMA Style

Jason Hill, Pasi Rastas, Emily A. Hornett, Ramprasad Neethiraj, Nathan Clark, Nathan Morehouse, Maria De La Paz Celorio-Mancera, Jofre Carnicer Cols, Heinrich Dircksen, Camille Meslin, Naomi Keehnen, Peter Pruisscher, Kristin Sikkink, Maria Vives, Heiko Vogel, Christer Wiklund, Alyssa Woronik, Carol L. Boggs, Sören Nylin, Christopher W. Wheat. Unprecedented reorganization of holocentric chromosomes provides insights into the enigma of lepidopteran chromosome evolution. Science Advances. 2019; 5 (6):eaau3648.

Chicago/Turabian Style

Jason Hill; Pasi Rastas; Emily A. Hornett; Ramprasad Neethiraj; Nathan Clark; Nathan Morehouse; Maria De La Paz Celorio-Mancera; Jofre Carnicer Cols; Heinrich Dircksen; Camille Meslin; Naomi Keehnen; Peter Pruisscher; Kristin Sikkink; Maria Vives; Heiko Vogel; Christer Wiklund; Alyssa Woronik; Carol L. Boggs; Sören Nylin; Christopher W. Wheat. 2019. "Unprecedented reorganization of holocentric chromosomes provides insights into the enigma of lepidopteran chromosome evolution." Science Advances 5, no. 6: eaau3648.

Journal article
Published: 10 May 2019 in Scientific Reports
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Specialist herbivores have often evolved highly sophisticated mechanisms to counteract defenses mediated by major plant secondary-metabolites. Plant species of the herbivore host range often display high chemical diversity and it is not well understood how specialist herbivores respond to this chemical diversity. Pieris larvae overcome toxic products from glucosinolate hydrolysis, the major chemical defense of their Brassicaceae hosts, by expressing nitrile-specifier proteins (NSP) in their gut. Furthermore, Pieris butterflies possess so-called major allergen (MA) proteins, which are multi-domain variants of a single domain major allergen (SDMA) protein expressed in the guts of Lepidopteran larvae. Here we show that Pieris larvae fine-tune NSP and MA gene expression depending on the glucosinolate profiles of their Brassicaceae hosts. Although the role of MA is not yet fully understood, the expression levels of NSP and MA in larvae that fed on plants whose glucosinolate composition varied was dramatically changed, whereas levels of SDMA expression remained unchanged. In addition, we found a similar regulation pattern among these genes in larvae feeding on Arabidopsis mutants with different glucosinolate profiles. Our results demonstrate that Pieris larvae appear to use different host plant adaptive genes to overcome a wide range of glucosinolate profiles in their host plants.

ACS Style

Yu Okamura; Ai Sato; Natsumi Tsuzuki; Yuji Sawada; Masami Yokota Hirai; Hanna Heidel-Fischer; Michael Reichelt; Masashi Murakami; Heiko Vogel. Differential regulation of host plant adaptive genes in Pieris butterflies exposed to a range of glucosinolate profiles in their host plants. Scientific Reports 2019, 9, 7256 .

AMA Style

Yu Okamura, Ai Sato, Natsumi Tsuzuki, Yuji Sawada, Masami Yokota Hirai, Hanna Heidel-Fischer, Michael Reichelt, Masashi Murakami, Heiko Vogel. Differential regulation of host plant adaptive genes in Pieris butterflies exposed to a range of glucosinolate profiles in their host plants. Scientific Reports. 2019; 9 (1):7256.

Chicago/Turabian Style

Yu Okamura; Ai Sato; Natsumi Tsuzuki; Yuji Sawada; Masami Yokota Hirai; Hanna Heidel-Fischer; Michael Reichelt; Masashi Murakami; Heiko Vogel. 2019. "Differential regulation of host plant adaptive genes in Pieris butterflies exposed to a range of glucosinolate profiles in their host plants." Scientific Reports 9, no. 1: 7256.

Preprint
Published: 05 May 2019
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Adaptive traits that enable organisms to conquer novel niches and experience subsequent diversification are ecologically and evolutionarily important. The larvae of Pieris butterflies express nitrile-specifier proteins (NSPs), a key innovation for overcoming the glucosinolate (GLS)-myrosinase-based defense system of their Brassicales host-plants. NSPs are a member of the NSP-like gene family, which includes the major allergen (MA) protein, a paralog of NSP with a GLS-disarming function, and a single domain major allergen (SDMA) protein, whose function is unknown. The arms-race between a highly variable host-plant defense system and members of the NSP-like gene family is suggested to mediate diversification in both Pierid butterflies and Brassicales plants. Here, we combined feeding experiments using 25 Brassicaceae plants and five Pieris species with larval transcriptome data to investigate the evolutionary forces acting on NSP-like gene family members associated with patterns of host-plant usage. Although we observed significantly elevated nonsynonymous to synonymous substitution ratios in NSPs, no such pattern was observed in MAs or SDMAs. Furthermore, we found a signature of positive selection of NSP at a phylogenetic branch which reflects different host-plant preferences. Our data indicate that NSPs have evolved in response to shifting preferences for host plants among five Pieris butterflies, whereas MAs and SDMAs appear to have more conserved functions. Our results show that the evolution and functional differentiation of key genes used in host-plant adaptation play a crucial role in the chemical arms-race between Pieris butterflies and their Brassicales host-plants.

ACS Style

Yu Okamura; Ai Sato; Natsumi Tsuzuki; Masashi Murakami; Hanna Heidel-Fischer; Heiko Vogel. Molecular signatures of selection associated with host-plant differences in Pieris butterflies. 2019, 627182 .

AMA Style

Yu Okamura, Ai Sato, Natsumi Tsuzuki, Masashi Murakami, Hanna Heidel-Fischer, Heiko Vogel. Molecular signatures of selection associated with host-plant differences in Pieris butterflies. . 2019; ():627182.

Chicago/Turabian Style

Yu Okamura; Ai Sato; Natsumi Tsuzuki; Masashi Murakami; Hanna Heidel-Fischer; Heiko Vogel. 2019. "Molecular signatures of selection associated with host-plant differences in Pieris butterflies." , no. : 627182.