Identification and preliminary characterization of chemosensory-related proteins in the gall fly, Procecidochares utilis by transcriptomic analysis

Andersson, 2014, Sex- and tissue-specific profiles of chemosensory gene expression in a herbivorous gall-inducing fly (Diptera: Cecidomyiidae), BMC Genomics, 15, 501, 10.1186/1471-2164-15-501 Bennett, 1986, Gall formation in crofton weed, Eupatorium adenophorum Spreng. (syn. Ageratina adenophora), by the Eupatorium gall fly Procecidochares utilis Stone (Diptera: Trypetidae), Aust. J. Bot., 34, 473, 10.1071/BT9860473 Benton, 2006, Atypical membrane topology and heteromeric function of Drosophila odorant receptors in vivo, PLoS Biol., 4, e20, 10.1371/journal.pbio.0040020 Benton, 2009, Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila, Cell, 136, 149, 10.1016/j.cell.2008.12.001 Bess, 1972, Biological control of pamakani, Eupatorium adenophorum, in Hawaii by a tephritid gall fly, Procecidochares utilis. 3. Status of the weed, fly and parasites of the fly in 1966-71 versus 1950-57, Proc. Hawaiian Entomol. Soc., 40, 244 Briscoe, 2013, Female behaviour drives expression and evolution of gustatory receptors in butterflies, PLoS Genet., 9, e1003620, 10.1371/journal.pgen.1003620 Brito, 2016, A look inside odorant-binding proteins in insect chemoreception, J. Insect Physiol., 95, 51, 10.1016/j.jinsphys.2016.09.008 Buccellato Bush, 1969, The cytogenetics of Procecidochares. I. The mitotic and polytene chromosomes of the pamakani fly, P. utilis Stone (Tephritidae-Diptera), Caryologia, 22, 311, 10.1080/00087114.1969.10796350 Chen, 2018, fastp: an ultra-fast all-in-one FASTQ preprocessor, Bioinformatics, 34, i884, 10.1093/bioinformatics/bty560 Chen, 2019, Genome-wide identification and expression profiling of odorant-binding proteins in the oriental fruit fly, Bactrocera dorsalis, Comp. Biochem. Physiol. Part D Genomics Proteomics, 31, 10.1016/j.cbd.2019.100605 Clyne, 1999, A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila, Neuron, 22, 327, 10.1016/S0896-6273(00)81093-4 Clyne, 2000, Candidate taste receptors in Drosophila, Science, 287, 1830, 10.1126/science.287.5459.1830 Cui, 2017, Odorant-binding and chemosensory proteins identified in the antennal transcriptome of Adelphocoris suturalis Jakovlev, Comp. Biochem. Physiol. -Part D Genomics Proteomics, 24, 139, 10.1016/j.cbd.2016.03.001 Cunningham, 2014, Understanding heliothine (Lepidoptera: Heliothinae) pests: what is a host plant?, J. Econ. Entomol., 107, 881, 10.1603/EC14036 Du, 2018, Identification and characterization of chemosensory genes in the antennal transcriptome of Spodoptera exigua, Comp. Biochem. Physiol. Part D Genomics Proteomics, 7, 54, 10.1016/j.cbd.2018.05.001 Elfekih, 2016, Identifcation and preliminary characterization of chemosensory perception-associated proteins in the melon fly Bactrocera cucurbitae using RNA-seq, Sci. Rep., 6, 19112, 10.1038/srep19112 Engsontia, 2008, The red four beetle’s large nose: an expanded odorant receptor gene family in Tribolium castaneum, Insect Biochem. Mol. Biol., 38, 387, 10.1016/j.ibmb.2007.10.005 Fishilevich, 2005, Chemotaxis behavior mediated by single larval olfactory neurons in Drosophila, Curr. Biol., 15, 2086, 10.1016/j.cub.2005.11.016 Fleischer, 2018, Access to the odor world: olfactory receptors and their role for signal transduction in insects, Cell. Mol. Life Sci., 75, 485, 10.1007/s00018-017-2627-5 Forstner, 2005, Differential expression of SNMP-1 and SNMP-2 proteins in pheromone-sensitive hairs of moths, Chem. Senses, 33, 291, 10.1093/chemse/bjm087 Fujii, 2015, Drosophila sugar receptors in sweet taste perception, olfaction, and internal nutrient sensing, Curr. Biol., 25, 621, 10.1016/j.cub.2014.12.058 Galindo, 2001, A large family of divergent Drosophila odorant-binding proteins expressed in gustatory and olfactory sensilla, Genetics, 159, 1059, 10.1093/genetics/159.3.1059 Gao, 2014, Transcriptome profiling of the crofton weed gall fly Procecidochares utilis, Genet. Mol. Res., 13, 2857, 10.4238/2014.March.19.1 Gomez-Diaz, 2018, The two main olfactory receptor families in Drosophila, ORs and IRs: a comparative approach, Front. Cell. Neurosci., 12, 253, 10.3389/fncel.2018.00253 Gouin, 2017, Two genomes of highly polyphagous lepidopteran pests (Spodoptera frugiperda, Noctuidae) with different host-plant ranges, Sci Rep, 7, 10.1038/s41598-017-10461-4 Grabherr, 2011, Full-length transcriptome assembly from RNA-Seq data without a reference genom, Nat. Biotechnol., 29, 644, 10.1038/nbt.1883 Hallem, 2004, The molecular basis of odor coding in the Drosophila antenna, Cell, 117, 965, 10.1016/j.cell.2004.05.012 Haseler, 1965, Life history and behavior of the crofton weed gall fly Procecidochares utillis stone (Diptera: Trypetidae), Aust. J. Entomol., 4, 27, 10.1111/j.1440-6055.1965.tb00642.x He, 2018, Molecular characterization and evolution of a chemosensory receptor gene family in three notorious rice planthoppers, Nilaparvata lugens, Sogatella furcifera and Laodelphax striatellus, based on genome and transcriptome analyses, Pest Manag. Sci. Doi, 10.1002/ps.4912 Hiroi, 2004, Two antagonistic gustatory receptor neurons responding to sweet-salty and bitter taste in Drosophila, J. Neurobiol., 61, 333, 10.1002/neu.20063 Hu, 2015, Gr33a modulates Drosophila male courtship preference, Sci. Rep., 5, 7777, 10.1038/srep07777 Jeong, 2013, An odorant-binding protein required for suppression of sweet taste by bitter chemicals, Neuron, 79, 725, 10.1016/j.neuron.2013.06.025 Jones, 2007, Two chemosensory receptors together mediate carbon dioxide detection in Drosophila, Nature, 445, 86, 10.1038/nature05466 Joseph, 2015, Drosophila chemoreceptors: a molecular interface between the chemical world and the brain, Trends Genet., 31, 683, 10.1016/j.tig.2015.09.005 Kanost, 2016, Multifaceted biological insights from a draft genome sequence of the tobacco hornworm moth, Manduca sexta, Insect Biochem. Mol. Biol., 76, 118, 10.1016/j.ibmb.2016.07.005 Katoh, 2002, MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform, Nucleic Acids Res., 30, 3059, 10.1093/nar/gkf436 Kim, 1998, LUSH odorant-binding protein mediates chemosensory responses to alcohols in Drosophila melanogaster, Genetics, 150, 711, 10.1093/genetics/150.2.711 Kohl, 2015, Pheromone processing in Drosophila, Curr. Opin. Neurobiol., 34, 149, 10.1016/j.conb.2015.06.009 Krogh, 2001, Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes, J. Mol. Biol., 305, 567, 10.1006/jmbi.2000.4315 Kwon, 2007, The molecular basis of CO2 reception in Drosophila, Proc. Natl. Acad. Sci. U. S. A., 104, 3574, 10.1073/pnas.0700079104 Lee, 2009, Multiple gustatory receptors required for the caffeine response in Drosophila, Proc. Natl. Acad. Sci. U. S. A., 106, 4495, 10.1073/pnas.0811744106 Leitch, 2015, Chemosensory genes identified in the antennal transcriptome of the blowfly Calliphora stygia, BMC Genomics, 16, 255, 10.1186/s12864-015-1466-8 Li, 2017, Identification of odorant-binding protein genes in Galeruca daurica (Coleoptera: Chrysomelidae) and analysis of their expression profiles, Bull. Entomol. Res., 107, 550, 10.1017/S0007485317000402 Lin, 2015, Food odors trigger Drosophila males to deposit a pheromone that guides aggregation and female oviposition decisions, Elife, 4, 10.7554/eLife.08688 Liu, 2018, Transcriptome characterization and gene expression analysis related to chemoreception in Trichogramma chilonis, an egg parasitoid, Gene, 678, 288, 10.1016/j.gene.2018.07.065 Livak, 2001, Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta DeltaC(T)) method, Methods, 25, 402, 10.1006/meth.2001.1262 Love, 2014, Moderated estimation of fold change and dispersion for RNAseq data with DESeq2, Genome Biol., 15, 550, 10.1186/s13059-014-0550-8 Miyamoto, 2012, A fructose receptor functions as a nutrient sensor in the Drosophila brain, Cell, 151, 1113, 10.1016/j.cell.2012.10.024 Miyazaki, 2018, Functional characterization of olfactory receptors in the oriental fruit fly Bactrocera dorsalis that respond to plant volatiles, Insect Biochem. Mol. Biol., 101, 32, 10.1016/j.ibmb.2018.07.002 Moon, 2006, A taste receptor required for the caffeine response in vivo, Curr. Biol., 16, 1812, 10.1016/j.cub.2006.07.024 Moon, 2009, A Drosophila gustatory receptor essential for aversive taste and inhibiting male-to-male courtship, Curr. Biol., 19, 1623, 10.1016/j.cub.2009.07.061 Mortazavi, 2008, Mapping and quantifying mammalian transcriptomes by RNA-Seq, Nat. Methods, 5, 621, 10.1038/nmeth.1226 Nguyen, 2015, IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies, Mol. Biol. Evol., 32, 268, 10.1093/molbev/msu300 Ni, 2016, The Ionotropic receptors IR21a and IR25a mediate cool sensing in Drosophila, Elife, 5, 10.7554/eLife.13254 Obiero, 2014, Odorant and gustatory receptors in the tsetse Fly Glossina morsitans morsitans, PLoS Negl. Trop. Dis., 8, 10.1371/journal.pntd.0002663 Papanicolaou, 2016, The whole genome sequence of the Mediterranean fruit fly, Ceratitis capitata (Wiedemann), reveals insights into the biology and adaptive evolution of a highly invasive pest species, Genome Biol., 17, 192, 10.1186/s13059-016-1049-2 Pearce, S.L., Clarke, D.F., East, P.D., Elfekih, S., Gordon, K., Jermiin, L.S., McGaughran, A., Oakeshott, J.G., Papanicolaou, A., Perera, O.P., Rane, R.V., Richards, S., Tay, W.T., Walsh, T.K., Anderson, A., Anderson, C.J., Asgari, S., Board, P.G., Bretschneider, A., Campbell, P.M., Wu, Y.D, 2017. Genomic innovations, transcriptional plasticity and gene loss underlying the evolution and divergence of two highly polyphagous and invasive Helicoverpa pest species. BMC Biol. 15(1), 63. Pelosi, 2018, Beyond chemoreception: diverse tasks of soluble olfactory proteins in insects, Biol. Rev. Camb. Philos. Soc., 93, 184, 10.1111/brv.12339 Petersen, 2011, SignalP 4.0: discriminating signal peptides from transmembrane regions, Nat. Methods, 8, 785, 10.1038/nmeth.1701 Prieto-Godino, 2016, Olfactory receptor pseudopseudogenes, Nature, 539, 93, 10.1038/nature19824 Qiu, 2018, Transcriptomics reveal the molecular underpinnings of chemosensory proteins in Chlorops oryzae, BMC Genomics, 19, 890, 10.1186/s12864-018-5315-4 Rimal, 2018, The multidimensional ionotropic receptors of Drosophila melanogaster, Insect Mol. Biol., 27, 1, 10.1111/imb.12347 Rinker, 2013, Antennal transcriptome profiles of anopheline mosquitoes reveal human host olfactory specialization in Anopheles gambiae, BMC Genomics, 14, 749, 10.1186/1471-2164-14-749 Robertson, 2006, The chemoreceptor superfamily in the honey bee, Apis mellifera expansion of the odorant, but not gustatory, receptor family, Genome Res., 16, 1395, 10.1101/gr.5057506 Robertson, 2003, Molecular evolution of the insect chemoreceptor gene superfamily in Drosophila melanogaster, Proc Natl Acad Sci US A., 100, 14537, 10.1073/pnas.2335847100 Rogers, 1997, Snmp-1, a novel membrane protein of olfactory neurons of the silk moth Antheraea polyphemus with homology to the CD36 family of membrane proteins, J. Biol. Chem., 272, 14792, 10.1074/jbc.272.23.14792 Rogers, 2001, Expression of SNMP-1 in olfactory neurons and sensilla of male and female antennae of the silkmoth Antheraea polyphemus, Cell Tissue Res., 303, 433, 10.1007/s004410000305 Scott, 2018, Gustatory processing in Drosophila melanogaster, Annu. Rev. Entomol., 63, 15, 10.1146/annurev-ento-020117-043331 Scott, 2014, Genome of the house fly, Musca domestica L., a global vector of diseases with adaptations to a septic environment, Genome Biol., 15, 466, 10.1186/s13059-014-0466-3 Sengul, 2010, Identification and characterization of odorant-binding protein 1 gene from the Asian malaria mosquito, Anopheles stephensi, Insect Mol. Biol., 19, 49, 10.1111/j.1365-2583.2009.00929.x Siciliano, 2014, Identification of pheromone components and their binding affinity to the odorant binding protein CcapOBP83a-2 of the Mediterranean fruit fly, Ceratitis capitata, Insect Biochem. Mol. Biol., 48, 51, 10.1016/j.ibmb.2014.02.005 Silbering, 2011, Complementary function and integrated wiring of the evolutionarily distinct Drosophila olfactory subsystems, J. Neurosci., 31, 13357, 10.1523/JNEUROSCI.2360-11.2011 Song, 2018, Identification and tissue distribution of chemosensory protein and odorant binding protein genes in Tropidothorax elegans distant (Hemiptera: Lygaeidae), Sci. Rep., 8, 7803, 10.1038/s41598-018-26137-6 Sun, 2004, Review on studies of Eupatorium adenophoruman important invasive species in China, J. Forestry Res., 15, 319, 10.1007/BF02844961 Sun, 2017, Identification and characterization of odorant binding proteins in the forelegs of Adelphocoris lineolatus (Goeze), Front. Physiol., 8, 735, 10.3389/fphys.2017.00735 Tanaka, 2009, Highly selective tuning of a silkworm olfactory receptor to a key mulberry leaf volatile, Current biology: CB, 19, 881, 10.1016/j.cub.2009.04.035 Tang, 2019, Expression and functional analysis of two odorant-binding proteins from Bradysia odoriphaga (Diptera: Sciaridae), J. Agric. Food Chem., 67, 3565, 10.1021/acs.jafc.9b00568 Tian, 2018, Antennal transcriptome analysis of the chemosensory gene families in Carposina sasakii (Lepidoptera: Carposinidae), BMC Genomics, 19, 544, 10.1186/s12864-018-4900-x Vieira, 2011, Comparative genomics of the odorant-binding and chemosensory protein gene families across the Arthropoda: origin and evolutionary history of the chemosensory system, Genome Biol. Evol., 3, 476, 10.1093/gbe/evr033 Vogt, 1981, Pheromone binding and inactivation by moth antennae, Nature, 293, 161, 10.1038/293161a0 Walker, 2019, Transcriptome analysis of gene families involved in chemosensory function in Spodoptera littoralis (Lepidoptera: Noctuidae), BMC Genomics, 20, 428, 10.1186/s12864-019-5815-x Wang, 2006, Invasion dynamics and potential spread of the invasive alien species Ageratina adenophora (Asteraceae) in China, Divers. Distrib., 12, 397, 10.1111/j.1366-9516.2006.00250.x Wang, 2015, The developmental transcriptome of the synanthropic fly Chrysomya megacephala and insights into olfactory proteins, BMC Genomics, 16, 20, 10.1186/s12864-014-1200-y Wang, 2017, Chemosensory genes in the antennal transcriptome of two syrphid species, Episyrphus balteatus and Eupeodes corolla (Diptera: Syrphidae), BMC Genomics, 18, 586, 10.1186/s12864-017-3939-4 Waris, 2018, The role of chemosensory protein 10 in the detection of behaviorally active compounds in brown planthopper, Nilaparvata lugens, Insect Sci. Watanabe, 2011, Gr39a, a highly diversifed gustatory receptor in Drosophila, has a role in sexual behavior, Behav. Genet., 41, 746, 10.1007/s10519-011-9461-6 Wei, 2017, Identification of candidate chemosensory genes by transcriptome analysis in Loxostege sticticalis Linnaeus, PLoS One, 12 Weiss, 2011, The molecular and cellular basis of bitter taste in Drosophila, Neuron, 69, 258, 10.1016/j.neuron.2011.01.001 Wu, 2015, Discovery of chemosensory genes in the oriental fruit Fly, Bactrocera dorsalis, PLoS One, 10 Wu, 2019, Candidates for chemosensory genes identified in the Chinese citrus fly, Bactrocera minax, through a transcriptomic analysis, BMC Genomics, 20, 646, 10.1186/s12864-019-6022-5 Xu, 2005, Drosophila OBP LUSH is required for activity of pheromone-sensitive neurons, Neuron, 45, 193, 10.1016/j.neuron.2004.12.031 Xu, 2009, Large-scale identification of odorant-binding proteins and chemosensory proteins from expressed sequence tags in insects, BMC Genomics, 10, 632, 10.1186/1471-2164-10-632 Xu, 2016, Expansion of a bitter taste receptor family in a polyphagous insect herbivore, Sci. Rep., 6, 23666, 10.1038/srep23666 Xu, 2019, Chemosensory gene families in the oligophagous pear pest Cacopsylla chinensis (Hemiptera: Psyllidae), Insects, 10, 175, 10.3390/insects10060175 Yang, 2016, Identification of novel odorant binding protein genes and functional characterization of OBP8 in Chilo suppressalis (Walker), Gene, 591, 425, 10.1016/j.gene.2016.06.052 Younas, 2018, A chemosensory protein MsepCSP5 involved in chemoreception of oriental armyworm Mythimna separate, Int. J. Biol. Sci., 14, 1935, 10.7150/ijbs.27315 Zhan, 2011, The monarch butterfly genome yields insights into long-distance migration, Cell, 147, 1171, 10.1016/j.cell.2011.09.052 Zhang, 2018, Identification and expression profiles of novel odorant binding proteins and functional analysis of OBP99a in Bactrocera dorsalis, Arch. Insect Biochem. Physiol., 98, 10.1002/arch.21452 Zhang, 2020, A phylogenomics approach to characterizing sensory neuron membrane proteins (SNMPs) in Lepidoptera, Insect Biochem. Mol. Biol., 118, 103313, 10.1016/j.ibmb.2020.103313 Zhou, 2004, “Plus-C” odorant-binding protein genes in two Drosophila species and the malaria mosquito Anopheles gambiae, Gene, 327, 117, 10.1016/j.gene.2003.11.007 Zhou, 2009, Plasticity of the chemoreceptor repertoire in Drosophila melanogaster, PLoS Genet., 5, 10.1371/journal.pgen.1000681 Zhou, 2012, Phylogenetic and transcriptomic analysis of chemosensory receptors in a pair of divergent ant species reveals sex-specific signatures of odor coding, PLoS Genet., 8, 10.1371/journal.pgen.1002930 Zhou, 2015, Identification of host-plant volatiles and characterization of two novel general odorant-binding proteins from the legume pod borer, Maruca vitrata Fabricius (Lepidoptera: Crambidae), PLoS One, 10, 10.1371/journal.pone.0141208