Venom gland components of the ectoparasitoid wasp, Anisopteromalus calandrae

The wasp Anisopteromalus calandrae is a small ectoparasitoid that attacks stored product pest beetle larvae that develop inside grain kernels, and is thus a potential insect control tool. The components of A. calandrae venom have not been studied, but venom from other organisms contains proteins with potential applications, such as pest management tools and treatments for human diseases. We dissected female A. calandrae and collected venom and associated glands. Using high throughput sequencing, a venom gland transcriptome was assembled that contained 45,432 contigs, 25,726 of which had BLASTx hits. The majority of hits were to Nasonia vitripennis, an ectoparasitoid from the same taxonomic family, as well as other bees, wasps, and ants. Gene ontology grouped sequences into eleven molecular functions, among which binding and catalytic activity had the most representatives. In this study, we highlighted the most abundant sequences, including those that are likely the functional components of the venom. Specifically, we focused on genes encoding proteins potentially involved in host developmental arrest, disrupting the host immune system, host paralysis, and transcripts that support these functions. Our report is the first to characterize components of the A. calandrae venom gland that may be useful as control tools for insect pests and other applications.

[1]  Yonggyun Kim,et al.  Calreticulin in Cotesia plutellae suppresses immune response of Plutella xylostella (L.) , 2015 .

[2]  Q. Fang,et al.  Venom of the parasitoid wasp Pteromalus puparum contains an odorant binding protein. , 2015, Archives of insect biochemistry and physiology.

[3]  Bo Yeon Kim,et al.  Molecular characterization of a venom acid phosphatase Acph-1-like protein from the Asiatic honeybee Apis cerana , 2014 .

[4]  Mrinalini,et al.  Nasonia vitripennis venom causes targeted gene expression changes in its fly host , 2014, Molecular ecology.

[5]  Z. Kokot,et al.  Shotgun proteome analysis of honeybee venom using targeted enrichment strategies. , 2014, Toxicon : official journal of the International Society on Toxinology.

[6]  Li-xia Huang,et al.  Cloning, expression and chitin‐binding activity of two peritrophin‐like protein genes in the common cutworm, Spodoptera litura , 2014, Insect science.

[7]  D. Stanley,et al.  Parasitization by Scleroderma guani influences protein expression in Tenebrio molitor pupae. , 2014, Journal of insect physiology.

[8]  J. Poulain,et al.  Identification of the main venom protein components of Aphidius ervi, a parasitoid wasp of the aphid model Acyrthosiphon pisum , 2014, BMC Genomics.

[9]  P Gopalakrishnakone,et al.  Scorpion venoms as a potential source of novel cancer therapeutic compounds , 2014, Experimental biology and medicine.

[10]  Koichiro Tamura,et al.  MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. , 2013, Molecular biology and evolution.

[11]  J. Oh,et al.  Comparative transcriptome analysis of the venom sac and gland of social wasp Vespa tropica and solitary wasp Rhynchium brunneum , 2013 .

[12]  Q. Fang,et al.  Inhibition of host cell encapsulation through inhibiting immune gene expression by the parasitic wasp venom calreticulin. , 2013, Insect biochemistry and molecular biology.

[13]  A. James,et al.  Molecular and Functional Characterization of Odorant-Binding Protein Genes in an Invasive Vector Mosquito, Aedes albopictus , 2013, PloS one.

[14]  S. Blank,et al.  Vitellogenins Are New High Molecular Weight Components and Allergens (Api m 12 and Ves v 6) of Apis mellifera and Vespula vulgaris Venom , 2013, PloS one.

[15]  F. Markland,et al.  Snake venom metalloproteinases. , 2013, Toxicon : official journal of the International Society on Toxinology.

[16]  Z. Zhang,et al.  Molecular cloning and characterization of peroxiredoxin 4 involved in protection against oxidative stress in the silkworm Bombyx mori , 2012, Insect molecular biology.

[17]  Nathan T. Mortimer,et al.  Mgat1-dependent N-glycosylation of Membrane Components Primes Drosophila melanogaster Blood Cells for the Cellular Encapsulation Response , 2012, PLoS pathogens.

[18]  A. Conesa,et al.  Transcriptome Profiling of the Intoxication Response of Tenebrio molitor Larvae to Bacillus thuringiensis Cry3Aa Protoxin , 2012, PloS one.

[19]  Fei Wang,et al.  Venom of Parasitoid, Pteromalus puparum, Suppresses Host, Pieris rapae, Immune Promotion by Decreasing Host C-Type Lectin Gene Expression , 2011, PloS one.

[20]  J. Gatti,et al.  Extracellular Superoxide Dismutase in Insects , 2011, The Journal of Biological Chemistry.

[21]  L. Nielsen,et al.  Deep sequencing-based transcriptome analysis of Plutella xylostella larvae parasitized by Diadegma semiclausum , 2011, BMC Genomics.

[22]  Xiang Xiao,et al.  Molecular characterization of the modular chitin binding protein Cbp50 from Bacillus thuringiensis serovar konkukian , 2011, Antonie van Leeuwenhoek.

[23]  Julio Rozas,et al.  Comparative Genomics of the Odorant-Binding and Chemosensory Protein Gene Families across the Arthropoda: Origin and Evolutionary History of the Chemosensory System , 2011, Genome biology and evolution.

[24]  Joaquín Dopazo,et al.  Genome analysis Advance Access publication February 18, 2011 B2G-FAR, a species-centered GO annotation repository , 2022 .

[25]  J. Poulain,et al.  The venom composition of the parasitic wasp Chelonus inanitus resolved by combined expressed sequence tags analysis and proteomic approach , 2010, BMC Genomics.

[26]  G. King,et al.  Spider-Venom Peptides as Therapeutics , 2010, Toxins.

[27]  Ji Hyeong Baek,et al.  Identification and characterization of venom proteins of two solitary wasps, Eumenes pomiformis and Orancistrocerus drewseni. , 2010, Toxicon : official journal of the International Society on Toxinology.

[28]  Q. Fang,et al.  Proteomic analysis of the venom from the endoparasitoid wasp Pteromalus puparum (Hymenoptera: Pteromalidae). , 2010, Archives of insect biochemistry and physiology.

[29]  J. Ring,et al.  Identification, Recombinant Expression, and Characterization of the 100 kDa High Molecular Weight Hymenoptera Venom Allergens Api m 5 and Ves v 3 , 2010, The Journal of Immunology.

[30]  A. Tassanakajon,et al.  Structure and function of invertebrate Kazal-type serine proteinase inhibitors. , 2010, Developmental and comparative immunology.

[31]  D. D. de Graaf,et al.  Venom Proteins of the Parasitoid Wasp Nasonia vitripennis: Recent Discovery of an Untapped Pharmacopee , 2010, Toxins.

[32]  N. Simões,et al.  Biochemical study and in vitro insect immune suppression by a trypsin‐like secreted protease from the nematode Steinernema carpocapsae , 2010, Parasite immunology.

[33]  J. Werren,et al.  Insights into the venom composition of the ectoparasitoid wasp Nasonia vitripennis from bioinformatic and proteomic studies , 2010, Insect molecular biology.

[34]  J. Werren,et al.  Two novel proteins expressed by the venom glands of Apis mellifera and Nasonia vitripennis share an ancient C1q‐like domain , 2010, Insect molecular biology.

[35]  A. Gomes,et al.  Anti-arthritic activity of Indian monocellate cobra (Naja kaouthia) venom on adjuvant induced arthritis. , 2010, Toxicon : official journal of the International Society on Toxinology.

[36]  J. Werren,et al.  Data mining cDNAs reveals three new single stranded RNA viruses in Nasonia (Hymenoptera: Pteromalidae) , 2010, Insect molecular biology.

[37]  Erich Bornberg-Bauer,et al.  Functional and Evolutionary Insights from the Genomes of Three Parasitoid Nasonia Species , 2010, Science.

[38]  B. Jin,et al.  Molecular cloning and characterization of 1-Cys and 2-Cys peroxiredoxins from the bumblebee Bombus ignitus. , 2009, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[39]  Q. Fang,et al.  Proteome changes in the plasma of Papilio xuthus (Lepidoptera: Papilionidae): effect of parasitization by the endoparasitic wasp Pteromalus puparum (Hymenoptera: Pteromalidae) , 2009, Journal of Zhejiang University SCIENCE B.

[40]  Daniel R. G. Price,et al.  A venom metalloproteinase from the parasitic wasp Eulophus pennicornis is toxic towards its host, tomato moth (Lacanobia oleracae) , 2009, Insect molecular biology.

[41]  M. Tufail,et al.  Insect vitellogenin/lipophorin receptors: molecular structures, role in oogenesis, and regulatory mechanisms. , 2009, Journal of insect physiology.

[42]  G. Yè,et al.  Molecular cloning and characterization of acid phosphatase in venom of the endoparasitoid wasp Pteromalus puparum (Hymenoptera: Pteromalidae). , 2008, Toxicon : official journal of the International Society on Toxinology.

[43]  Misook Kim,et al.  A tarantula spider toxin, GsMTx4, reduces mechanical and neuropathic pain , 2008, PAIN®.

[44]  M. Robles,et al.  University of Birmingham High throughput functional annotation and data mining with the Blast2GO suite , 2022 .

[45]  C. Kaito,et al.  Phosphodiesterase Activity of CvfA Is Required for Virulence in Staphylococcus aureus* , 2008, Journal of Biological Chemistry.

[46]  P. Vogt,et al.  The Growth-hormone inducible transmembrane protein (Ghitm) belongs to the Bax inhibitory protein-like family , 2007, International journal of biological sciences.

[47]  P. Falabella,et al.  A gamma-glutamyl transpeptidase of Aphidius ervi venom induces apoptosis in the ovaries of host aphids. , 2007, Insect biochemistry and molecular biology.

[48]  T. Hance,et al.  Potential of Anisopteromalus calandrae (Hymenoptera: Pteromalidae) as biocontrol agent of Callosobruchus maculatus (F.) (Coleopetera: Bruchidae) , 2007 .

[49]  Y. Oba,et al.  Identification of proteins from venom of the paralytic spider wasp, Cyphononyx dorsalis. , 2007, Insect biochemistry and molecular biology.

[50]  A. Armugam,et al.  Snake venom components and their applications in biomedicine , 2006, Cellular and Molecular Life Sciences CMLS.

[51]  K. Anderson,et al.  Rel/NF-κB double mutants reveal that cellular immunity is central to Drosophila host defense , 2006, Proceedings of the National Academy of Sciences.

[52]  B. Lemaître,et al.  Two Proteases Defining a Melanization Cascade in the Immune System of Drosophila* , 2006, Journal of Biological Chemistry.

[53]  J. Kastrup,et al.  Structure of recombinant Ves v 2 at 2.0 Angstrom resolution: structural analysis of an allergenic hyaluronidase from wasp venom. , 2006, Acta crystallographica. Section D, Biological crystallography.

[54]  Dennis van Hoof,et al.  Sequence analysis of the non-recurring C-terminal domains shows that insect lipoprotein receptors constitute a distinct group of LDL receptor family members. , 2006, Insect biochemistry and molecular biology.

[55]  S. Luckhart,et al.  A mosquito 2-Cys peroxiredoxin protects against nitrosative and oxidative stresses associated with malaria parasite infection. , 2006, Free radical biology & medicine.

[56]  H. Kataoka,et al.  Ghitm is an ortholog of the Bombyx mori prothoracic gland-derived receptor (Pgdr) that is ubiquitously expressed in mammalian cells and requires an N-terminal signal sequence for expression. , 2006, Biochemical and biophysical research communications.

[57]  H. Kataoka,et al.  A Novel Type of Receptor cDNA from the Prothoracic Glands of the Silkworm, Bombyx mori , 2006, Bioscience, biotechnology, and biochemistry.

[58]  E. H. Richards,et al.  Hydrolase activity in the venom of the pupal endoparasitic wasp, Pimpla hypochondriaca. , 2005, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[59]  G. Flik,et al.  The remarkable conservation of corticotropin-releasing hormone (CRH)-binding protein in the honeybee (Apis mellifera) dates the CRH system to a common ancestor of insects and vertebrates. , 2005, Endocrinology.

[60]  B. Jin,et al.  Molecular cloning and characterization of a peroxiredoxin gene from the mole cricket, Gryllotalpa orientalis. , 2005, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[61]  A. Tanaka,et al.  Identification and characterization of a novel factor XIIa inhibitor in the hematophagous insect, Triatoma infestans (Hemiptera: Reduviidae) , 2004, FEBS letters.

[62]  Bmc Immunology,et al.  Identification of genes differentially expressed in T cells following stimulation with the chemokines CXCL12 and CXCL10 , 2004, BMC Immunology.

[63]  N. Audsley,et al.  Towards a comprehensive view of the primary structure of venom proteins from the parasitoid wasp Pimpla hypochondriaca. , 2004, Insect biochemistry and molecular biology.

[64]  G. Flik,et al.  Structural characterisation of a cyprinid (Cyprinus carpio L.) CRH, CRH-BP and CRH-R1, and the role of these proteins in the acute stress response. , 2004, Journal of molecular endocrinology.

[65]  S. Govind,et al.  Genetic Analysis of Contributions of Dorsal Group and JAK-Stat92E Pathway Genes to Larval Hemocyte Concentration and the Egg Encapsulation Response in Drosophila , 2004, Genetics.

[66]  T. V. Gowda,et al.  Isolation and characterization of hyaluronidase a "spreading factor" from Indian cobra (Naja naja) venom. , 2004, Biochimie.

[67]  S. Asgari,et al.  A serine proteinase homolog venom protein from an endoparasitoid wasp inhibits melanization of the host hemolymph. , 2003, Insect biochemistry and molecular biology.

[68]  J. Baker,et al.  Morphology and chemistry of Dufour glands in four ectoparasitoids: Cephalonomia tarsalis, C. waterstoni (Hymenoptera: Bethylidae), Anisopteromalus calandrae, and Pteromalus cerealellae (Hymenoptera: Pteromalidae). , 2003, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[69]  Chun-Fu Wu,et al.  Expression of an antitumor-analgesic peptide from the venom of Chinese scorpion Buthus martensii karsch in Escherichia coli. , 2003, Protein expression and purification.

[70]  Toshiharu Tanaka,et al.  Venom of ectoparasitoid, Euplectrus sp near plathypenae (Hymenoptera: Eulophidae) regulates the physiological state of Pseudaletia separata (Lepidoptera: Noctuidae) host as a food resource. , 2003, Journal of insect physiology.

[71]  D. Rivers,et al.  The ectoparasitic wasp Nasonia vitripennis (Walker) (Hymenoptera: Pteromalidae) differentially affects cells mediating the immune response of its flesh fly host, Sarcophaga bullata Parker (Diptera: Sarcophagidae). , 2002, Journal of insect physiology.

[72]  B. Lemaître,et al.  An immune-responsive Serpin regulates the melanization cascade in Drosophila. , 2002, Developmental cell.

[73]  E. H. Richards,et al.  Analysis of venom constituents from the parasitoid wasp Pimpla hypochondriaca and cloning of a cDNA encoding a venom protein. , 2002, Insect biochemistry and molecular biology.

[74]  J. Broeck,et al.  Structural and functional properties of a novel serine protease inhibiting peptide family in arthropods. , 2002, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[75]  M. Sugumaran Comparative biochemistry of eumelanogenesis and the protective roles of phenoloxidase and melanin in insects. , 2002, Pigment cell research.

[76]  C. Conyers,et al.  A venom protein from the endoparasitoid wasp Pimpla hypochondriaca is similar to snake venom reprolysin-type metalloproteases. , 2002, Journal of invertebrate pathology.

[77]  W C Orr,et al.  The peroxiredoxin gene family in Drosophila melanogaster. , 2001, Free radical biology & medicine.

[78]  A. Sesso,et al.  Cytochemical analysis of acid phosphatase activity in the venom secretory cells of Bothrops jararaca. , 2001, Tissue & cell.

[79]  J. Kopchick,et al.  Identification, isolation, and cloning of growth hormone (GH)-inducible interscapular brown adipose complementary deoxyribonucleic acid from GH antagonist mice. , 2001, Endocrinology.

[80]  J. Rossier,et al.  Ponericins, New Antibacterial and Insecticidal Peptides from the Venom of the Ant Pachycondyla goeldii * , 2001, The Journal of Biological Chemistry.

[81]  F. Sehnal,et al.  Insect silk contains both a Kunitz-type and a unique Kazal-type proteinase inhibitor. , 2001, European journal of biochemistry.

[82]  L. Schoofs,et al.  Peptidomics of the pars intercerebralis-corpus cardiacum complex of the migratory locust, Locusta migratoria. , 2001, European journal of biochemistry.

[83]  Gillespie,et al.  Acid phosphatases in the haemolymph of the desert locust, Schistocerca gregaria, infected with the entomopathogenic fungus Metarhizium anisopliae. , 2000, Journal of insect physiology.

[84]  E. H. Richards,et al.  Venom from the endoparasitic wasp Pimpla hypochondriaca adversely affects the morphology, viability, and immune function of hemocytes from larvae of the tomato moth, Lacanobia oleracea. , 2000, Journal of invertebrate pathology.

[85]  R. Weaver,et al.  Identity and mode of action of host endocrine disrupters from the venom of parasitoid wasps , 2000 .

[86]  C. Choi,et al.  Purification and characterization of chitin-binding proteins from the hemolymph of sweet potato hornworm, Agrius convolvuli. , 1999, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[87]  M. Kanost Serine proteinase inhibitors in arthropod immunity. , 1999, Developmental and comparative immunology.

[88]  J. Broeck,et al.  Peptides in the Locusts, Locusta migratoria and Schistocerca gregaria 1 1 Taken in part from a paper presented at a satellite symposium on Insect Neuropeptides during the Seventh Annual Neuropeptide Conference, February 1–6, 1996, Breckenridge, CO. , 1997, Peptides.

[89]  L. Gilbert,et al.  Control of ecdysteroidogenesis: Activation and inhibition of prothoracic gland activity , 1997, Invertebrate Neuroscience.

[90]  K. Zaner,et al.  Release of calreticulin from neutrophils may alter C1q-mediated immune functions. , 1997, The Biochemical journal.

[91]  S. L. Brandt,et al.  Characteristics of a developmental arrestant in the venom of the ectoparasitoid wasp Euplectrus comstockii. , 1996, Toxicon : official journal of the International Society on Toxinology.

[92]  T. P. King,et al.  Yellow jacket venom allergens, hyaluronidase and phospholipase: sequence similarity and antigenic cross-reactivity with their hornet and wasp homologs and possible implications for clinical allergy. , 1996, The Journal of allergy and clinical immunology.

[93]  Theo Wallimann,et al.  Structure of mitochondrial creatine kinase , 1996, Nature.

[94]  T. Vuocolo,et al.  Characterization of a Major Peritrophic Membrane Protein, Peritrophin-44, from the Larvae of Lucilia cuprina , 1996, The Journal of Biological Chemistry.

[95]  K. Ahmed Studies on the ectoparasitoid, Anisopteromalus calandrae How. (Hymenoptera: Pteromalidae) as a biocontrol agent against the lesser grain borer, Rhyzopertha dominica (Fab.) in Saudi Arabia , 1996 .

[96]  D. Denlinger,et al.  Venom-Induced Alterations in Fly Lipid Metabolism and Its Impact on Larval Development of the Ectoparasitoid Nasonia vitripennis (Walker) (Hymenoptera: Pteromalidae) , 1995 .

[97]  T. K. Hayes,et al.  Isolation and characterization of a diuretic peptide common to the house fly and stable fly , 1994, Peptides.

[98]  M. Lagueux,et al.  Cloning of a Locusta cDNA encoding a precursor peptide for two structurally related proteinase inhibitors. , 1994, Insect biochemistry and molecular biology.

[99]  D. Denlinger,et al.  Redirection of metabolism in the flesh fly, Sarcophaga bullata, following envenomation by the ectoparasitoid Nasonia vitripennis and correlation of metabolic effects with the diapause status of the host , 1994 .

[100]  J. Reagan Expression cloning of an insect diuretic hormone receptor. A member of the calcitonin/secretin receptor family. , 1994, The Journal of biological chemistry.

[101]  P. Tempst,et al.  Apidaecins: antibacterial peptides from honeybees. , 1989, The EMBO journal.

[102]  H. Kataoka,et al.  Isolation and identification of a diuretic hormone from the tobacco hornworm, Manduca sexta. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[103]  K. Söderhäll,et al.  Purification and characterization of a high-Mr proteinase inhibitor of pro-phenol oxidase activation from crayfish plasma. , 1987, The Biochemical journal.

[104]  M. D. Owen,et al.  The morphology of the honey bee (Apis mellifera L.) venom gland and reservoir , 1984, Journal of morphology.

[105]  J. Burnett,et al.  Purification of an Endonuclease Present in Chrysaora quinquecirrha Venom , 1981, Proceedings of the Society for Experimental Biology and Medicine. Society for Experimental Biology and Medicine.

[106]  N. Ratcliffe,et al.  Morphological, ultrastructural, histochemical and electrophoretic studies on the venom system of Nasonia vitripennis walker (hymenoptera: Pteromalidae) , 1969 .

[107]  M. Laskowski,et al.  Purification of an endonuclease from the venom of Bothrops atrox. , 1962, Biochemistry.

[108]  N. Oršolić Bee venom in cancer therapy , 2011, Cancer and Metastasis Reviews.

[109]  Q. Yao,et al.  Identification and characterization of a novel 1-Cys peroxiredoxin from silkworm, Bombyx mori. , 2008, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[110]  N. Beckage,et al.  Wasp parasitoid disruption of host development: implications for new biologically based strategies for insect control. , 2004, Annual review of entomology.

[111]  L. Gilbert,et al.  Control and biochemical nature of the ecdysteroidogenic pathway. , 2002, Annual review of entomology.

[112]  R. Weaver,et al.  A new form of arthropod phenoloxidase is abundant in venom of the parasitoid wasp Pimpla hypochondriaca. , 2001, Insect biochemistry and molecular biology.

[113]  A. Grossman,et al.  Association of human corticotropin-releasing hormone to its binding protein in blood may trigger clearance of the complex. , 1994, The Journal of clinical endocrinology and metabolism.

[114]  R. Rizki,et al.  Encapsulation of parasitoid eggs in phenoloxidase-deficient mutants of Drosophila melanogaster , 1990 .

[115]  A. McMichael,et al.  The hyaluronidase activities of some Southeast Asian snake venoms. , 1988, Toxicon : official journal of the International Society on Toxinology.

[116]  A. Tu,et al.  Characterization of lizard venom hyaluronidase and evidence for its action as a spreading factor. , 1983, Comparative biochemistry and physiology. B, Comparative biochemistry.

[117]  I. Neeman,et al.  Purification and characterization of the endonuclease present in Physalia physalis venom , 1980 .

[118]  J. Humphrey,et al.  Hyaluronidase: correlation between biological assay and other methods of assay. , 1953, The Biochemical journal.