Mining Genes Involved in Insecticide Resistance of Liposcelis bostrychophila Badonnel by Transcriptome and Expression Profile Analysis

Background Recent studies indicate that infestations of psocids pose a new risk for global food security. Among the psocids species, Liposcelis bostrychophila Badonnel has gained recognition in importance because of its parthenogenic reproduction, rapid adaptation, and increased worldwide distribution. To date, the molecular data available for L. bostrychophila is largely limited to genes identified through homology. Also, no transcriptome data relevant to psocids infection is available. Methodology and Principal Findings In this study, we generated de novo assembly of L. bostrychophila transcriptome performed through the short read sequencing technology (Illumina). In a single run, we obtained more than 51 million sequencing reads that were assembled into 60,012 unigenes (mean size = 711 bp) by Trinity. The transcriptome sequences from different developmental stages of L. bostrychophila including egg, nymph and adult were annotated with non-redundant (Nr) protein database, gene ontology (GO), cluster of orthologous groups of proteins (COG), and KEGG orthology (KO). The analysis revealed three major enzyme families involved in insecticide metabolism as differentially expressed in the L. bostrychophila transcriptome. A total of 49 P450-, 31 GST- and 21 CES-specific genes representing the three enzyme families were identified. Besides, 16 transcripts were identified to contain target site sequences of resistance genes. Furthermore, we profiled gene expression patterns upon insecticide (malathion and deltamethrin) exposure using the tag-based digital gene expression (DGE) method. Conclusion The L. bostrychophila transcriptome and DGE data provide gene expression data that would further our understanding of molecular mechanisms in psocids. In particular, the findings of this investigation will facilitate identification of genes involved in insecticide resistance and designing of new compounds for control of psocids.

[1]  Andrew K. Jones,et al.  The nicotinic acetylcholine receptor gene family of the honey bee, Apis mellifera. , 2006, Genome research.

[2]  K. Dong.  Insect sodium channels and insecticide resistance , 2007, Invertebrate Neuroscience.

[3]  W. Dou,et al.  Toxicological and biochemical characterizations of GSTs in Liposcelis bostrychophila Badonnel (Psocop., Liposcelididae) , 2006 .

[4]  Guanrong Chen,et al.  Synchronous Bursts on Scale-Free Neuronal Networks with Attractive and Repulsive Coupling , 2010, PloS one.

[5]  J. Wang,et al.  Accumulation and utilization of triacylglycerol and polysaccharides in Liposcelis bostrychophila (Psocoptera, Liposcelididae) selected for resistance to carbon dioxide , 2003 .

[6]  B. Turner.  Liposcelis bostrychophila (Psocoptera: Liposcelididae), a stored food pest in the UK. , 1994 .

[7]  G. M. Clarke,et al.  Tracing the geographic origin of the cosmopolitan parthenogenetic insect pest Liposcelis bostrychophila (Psocoptera: Liposcelididae) , 2006, Bulletin of Entomological Research.

[8]  G. Daglish,et al.  Effectiveness of spinosad as a grain protectant against resistant beetle and psocid pests of stored grain in Australia , 2005 .

[9]  Wen-Jer Wu,et al.  Discovery of Genes Related to Insecticide Resistance in Bactrocera dorsalis by Functional Genomic Analysis of a De Novo Assembled Transcriptome , 2012, PloS one.

[10]  D. M. Soderlund,et al.  Pyrethroids, knockdown resistance and sodium channels. , 2008, Pest management science.

[11]  A. Enayati,et al.  Insect glutathione transferases and insecticide resistance , 2005, Insect molecular biology.

[12]  M. Berenbaum,et al.  A deficit of detoxification enzymes: pesticide sensitivity and environmental response in the honeybee , 2006, Insect molecular biology.

[13]  W. Low,et al.  Molecular Evolution of Glutathione S-Transferases in the Genus Drosophila , 2007, Genetics.

[14]  J. Claverie,et al.  The significance of digital gene expression profiles. , 1997, Genome research.

[15]  Yude Yu,et al.  The next-generation sequencing technology and application , 2010, Protein & Cell.

[16]  Structure, function and evolution of glutathione transferases: implications for classification of non-mammalian members of an ancient enzyme superfamily. , 2001 .

[17]  N. Friedman,et al.  Trinity: reconstructing a full-length transcriptome without a genome from RNA-Seq data , 2011, Nature Biotechnology.

[18]  Janet Hemingway,et al.  Evolution of Supergene Families Associated with Insecticide Resistance , 2002, Science.

[19]  P. Collins,et al.  Residual toxicities and persistence of organophosphorus insecticides mixed with carbaryl as structural treatments against three liposcelidid psocid species (Psocoptera: Liposcelididae) infesting stored grain , 2003 .

[20]  R. Feyereisen.  Insect P450 enzymes. , 1999, Annual review of entomology.

[21]  Juan Du,et al.  Transcriptome and Gene Expression Analysis of the Rice Leaf Folder, Cnaphalocrosis medinalis , 2012, PloS one.

[22]  Jinjun Wang,et al.  Purification and biochemical characterization of glutathione S-transferases from three strains of Liposcelis bostrychophila Badonnel (Psocoptera: Liposcelididae): Implication of insecticide resistance , 2009 .

[23]  M. Metzker.  Sequencing technologies — the next generation , 2010, Nature Reviews Genetics.

[24]  Thomas D. Schmittgen,et al.  Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. , 2001, Methods.

[25]  A. Baz,et al.  Occurrence of psocids and natural predators on organic rice in Calasparra (Murcia, Spain) , 2005 .

[26]  May R Berenbaum,et al.  Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. , 2007, Annual review of entomology.

[27]  Jinjun Wang,et al.  Transcription and Induction Profiles of Three Novel P450 Genes in Liposcelis bostrychophila (Psocoptera: Liposcelididae) , 2012, Journal of economic entomology.

[28]  A. Assefa,et al.  Therapeutic efficacy of Artemether/Lumefantrine (Coartem®) against Plasmodium falciparum in Kersa, South West Ethiopia , 2010, Parasites & Vectors.

[29]  J. Throne,et al.  Effects of Diet on Population Growth of the Psocids Lepinotus reticulatus and Liposcelis entomophila , 2008, Journal of economic entomology.

[30]  S. H. Ho,et al.  The response of Liposcelis bostrychophila Badonnel and L. entomophila (Enderlein) (Psocoptera) to phosphine , 1995 .

[31]  Evgeny M. Zdobnov,et al.  Genome sequences of the human body louse and its primary endosymbiont provide insights into the permanent parasitic lifestyle , 2010, Proceedings of the National Academy of Sciences.

[32]  J. Throne,et al.  Efficacy of grain protectants against four psocid species on maize, rice and wheat. , 2009, Pest management science.

[33]  S. Reynaud,et al.  Transcriptome response to pollutants and insecticides in the dengue vector Aedes aegypti using next-generation sequencing technology , 2010, BMC Genomics.

[34]  Soon-Mi Lee,et al.  Expression of heat shock protein and hemoglobin genes in Chironomus tentans (Diptera, chironomidae) larvae exposed to various environmental pollutants: a potential biomarker of freshwater monitoring. , 2006, Chemosphere.

[35]  Ligang Zhou,et al.  Identification of Insecticidal Constituents of the Essential Oil of Curcuma wenyujin Rhizomes Active against Liposcelis bostrychophila Badonnel , 2012, Molecules.

[36]  J. Tsai,et al.  Development and Reproduction of the Psocid Liposcelis bostrychophila (Psocoptera: Liposcelididae) as a Function of Temperature , 2000 .

[37]  Wenjia Yang,et al.  Transcriptome Analysis of the Oriental Fruit Fly (Bactrocera dorsalis) , 2011, PloS one.

[38]  G. Daglish,et al.  Combined treatments of spinosad and chlorpyrifos-methyl for management of resistant psocid pests (Psocoptera: Liposcelididae) of stored grain. , 2007, Pest management science.

[39]  J. Hemingway,et al.  Two duplicated P450 genes are associated with pyrethroid resistance in Anopheles funestus, a major malaria vector. , 2008, Genome research.

[40]  G. Smagghe,et al.  Transcriptome analysis of the citrus red mite, Panonychus citri, and its gene expression by exposure to insecticide/acaricide , 2012, Insect molecular biology.

[41]  B. Dastugue,et al.  Drosophila melanogaster P‐glycoprotein: A membrane detoxification system toward polycyclic aromatic hydrocarbon pollutants , 2006, Environmental toxicology and chemistry.

[42]  Ryan D. Morin,et al.  Next-generation tag sequencing for cancer gene expression profiling. , 2009, Genome research.

[43]  P. Collins,et al.  Influence of concentration, temperature and humidity on the toxicity of phosphine to the strongly phosphine-resistant psocid Liposcelis bostrychophila Badonnel (Psocoptera: Liposcelididae). , 2008, Pest management science.

[44]  R. Feyereisen.  Arthropod CYPomes illustrate the tempo and mode in P450 evolution. , 2011, Biochimica et biophysica acta.

[45]  M. Schuler.  P450s in plant-insect interactions. , 2011, Biochimica et biophysica acta.

[46]  Juan Miguel García-Gómez,et al.  BIOINFORMATICS APPLICATIONS NOTE Sequence analysis Manipulation of FASTQ data with Galaxy , 2005 .

[47]  Simon C. Potter,et al.  A Genome-Wide Association Search for Type 2 Diabetes Genes in African Americans , 2012, PLoS ONE.

[48]  J. Throne,et al.  Temporospatial Distribution of the Psocids Liposcelis entomophila and L. decolor (Psocoptera: Liposcelididae) in Steel Bins Containing Wheat , 2009, Journal of economic entomology.

[49]  R. Feyereisen,et al.  Evolution of insect P450. , 2006, Biochemical Society transactions.

[50]  M. Coetzee,et al.  Cuticle thickening associated with pyrethroid resistance in the major malaria vector Anopheles funestus , 2010, Parasites & Vectors.

[51]  Alastair M. Hosie,et al.  Actions of the insecticide fipronil, on dieldrin‐sensitive and ‐resistant GABA receptors of Drosophila melanogaster , 1995, British journal of pharmacology.

[52]  D. Sheehan,et al.  Structure, function and evolution of glutathione transferases: implications for classification of non-mammalian members of an ancient enzyme superfamily. , 2001, The Biochemical journal.

[53]  Andrew K. Jones,et al.  The nicotinic acetylcholine receptor gene family of the malaria mosquito, Anopheles gambiae. , 2005, Genomics.

[54]  K. Dong,et al.  The nicotinic acetylcholine receptor gene family of the silkworm, Bombyx mori , 2007, BMC Genomics.

[55]  B. Roe,et al.  Comparative analysis of detoxification enzymes in Acyrthosiphon pisum and Myzus persicae , 2010, Insect molecular biology.

[56]  Robert C. Thompson,et al.  NGSQC: cross-platform quality analysis pipeline for deep sequencing data , 2010, BMC Genomics.

[57]  F. Rinkevich,et al.  Transcriptional diversity and allelic variation in nicotinic acetylcholine receptor subunits of the red flour beetle, Tribolium castaneum , 2009, Insect molecular biology.

[58]  Jinjun Wang,et al.  Molecular characterization of two nicotinic acetylcholine receptor subunits from Liposcelis bostrychophila Badonnel (Psocoptera: Liposcelididae). , 2009, Archives of insect biochemistry and physiology.

[59]  R. Shao,et al.  The Multipartite Mitochondrial Genome of Liposcelis bostrychophila: Insights into the Evolution of Mitochondrial Genomes in Bilateral Animals , 2012, PloS one.