De novo assembly and sex-specific transcriptome profiling in the sand fly Phlebotomus perniciosus (Diptera, Phlebotominae), a major Old World vector of Leishmania infantum

. 2015 Oct 23 ; 16 () : 847. [epub] 20151023

Jazyk angličtina Země Velká Británie, Anglie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid26493315
Odkazy

PubMed 26493315
PubMed Central PMC4619268
DOI 10.1186/s12864-015-2088-x
PII: 10.1186/s12864-015-2088-x
Knihovny.cz E-zdroje

BACKGROUND: The phlebotomine sand fly Phlebotomus perniciosus (Diptera: Psychodidae, Phlebotominae) is a major Old World vector of the protozoan Leishmania infantum, the etiological agent of visceral and cutaneous leishmaniases in humans and dogs, a worldwide re-emerging diseases of great public health concern, affecting 101 countries. Despite the growing interest in the study of this sand fly species in the last years, the development of genomic resources has been limited so far. To increase the available sequence data for P. perniciosus and to start studying the molecular basis of the sexual differentiation in sand flies, we performed whole transcriptome Illumina RNA sequencing (RNA-seq) of adult males and females and de novo transcriptome assembly. RESULTS: We assembled 55,393 high quality transcripts, of which 29,292 were unique, starting from adult whole body male and female pools. 11,736 transcripts had at least one functional annotation, including full-length low abundance salivary transcripts, 981 transcripts were classified as putative long non-coding RNAs and 244 transcripts encoded for putative novel proteins specific of the Phlebotominae sub-family. Differential expression analysis identified 8590 transcripts significantly biased between sexes. Among them, some show relaxation of selective constraints when compared to their orthologs of the New World sand fly species Lutzomyia longipalpis. CONCLUSIONS: In this paper, we present a comprehensive transcriptome resource for the sand fly species P. perniciosus built from short-read RNA-seq and we provide insights into sex-specific gene expression at adult stage. Our analysis represents a first step towards the identification of sex-specific genes and pathways and a foundation for forthcoming investigations into this important vector species, including the study of the evolution of sex-biased genes and of the sexual differentiation in phlebotomine sand flies.

Zobrazit více v PubMed

Maroli M, Feliciangeli MD, Bichaud L, Charrel RN, Gradoni L. Phlebotomine sandflies and the spreading of leishmaniases and other diseases of public health concern. Med Vet Entomol. 2013;27(2):123–147. doi: 10.1111/j.1365-2915.2012.01034.x. PubMed DOI

Gradoni L. Epidemiological surveillance of leishmaniasis in the European Union: operational and research challenges. Euro Surveill. 2013;18(30):20539. PubMed

Dostalova A, Volf P. Leishmania development in sand flies: parasite-vector interactions overview. Parasit Vectors. 2012;5:276. doi: 10.1186/1756-3305-5-276. PubMed DOI PMC

Alkan C, Bichaud L, de Lamballerie X, Alten B, Gould EA, Charrel RN. Sandfly-borne phleboviruses of Eurasia and Africa: epidemiology, genetic diversity, geographic range, control measures. Antiviral Res. 2013;100(1):54–74. doi: 10.1016/j.antiviral.2013.07.005. PubMed DOI

Depaquit J, Grandadam M, Fouque F, Andry PE, Peyrefitte C. Arthropod-borne viruses transmitted by Phlebotomine sandflies in Europe: a review. Euro Surveill. 2010;15(10):19507. PubMed

Gramiccia M, Scalone A, Di Muccio T, Orsini S, Fiorentino E, Gradoni L. The burden of visceral leishmaniasis in Italy from 1982 to 2012: a retrospective analysis of the multi-annual epidemic that occurred from 1989 to 2009. Euro Surveill. 2013;18(29):20535. PubMed

Alvar J, Velez ID, Bern C, Herrero M, Desjeux P, Cano J, et al. Leishmaniasis worldwide and global estimates of its incidence. PLoS One. 2012;7(5):e35671. doi: 10.1371/journal.pone.0035671. PubMed DOI PMC

Antoniou M, Gramiccia M, Molina R, Dvorak V, Volf P. The role of indigenous phlebotomine sandflies and mammals in the spreading of leishmaniasis agents in the Mediterranean region. Euro Surveill. 2013;18(30):20540. PubMed

Bates PA, Depaquit J, Galati EA, Kamhawi S, Maroli M, McDowell MA, et al. Recent advances in phlebotomine sand fly research related to leishmaniasis control. Parasit Vectors. 2015;8:131. doi: 10.1186/s13071-015-0712-x. PubMed DOI PMC

Killick-Kendrick R, Killick-Kendrick M. Canine Leishmaniasis: an Update: 1999. Barcelona: Proc Intern Canine Leishmaniasis Forum; 1999. Biology of sand fly vectors of Mediterranean canine leishmaniasis; pp. 26–31.

Gu XC, Zhang YN, Kang K, Dong SL, Zhang LW. Antennal transcriptome analysis of odorant reception genes in the red turpentine beetle (RTB) dendroctonus valens. PLoS One. 2015;10(5):e0125159. doi: 10.1371/journal.pone.0125159. PubMed DOI PMC

Meng X, Zhang Y, Bao H, Liu Z. Sequence analysis of insecticide action and detoxification-related genes in the insect pest natural enemy pardosa pseudoannulata. PLoS One. 2015;10(4):e0125242. doi: 10.1371/journal.pone.0125242. PubMed DOI PMC

Chauhan P, Hansson B, Kraaijeveld K, de Knijff P, Svensson EI, Wellenreuther M. De novo transcriptome of Ischnura elegans provides insights into sensory biology, colour and vision genes. BMC Genomics. 2014;15:808. doi: 10.1186/1471-2164-15-808. PubMed DOI PMC

Misof B, Liu S, Meusemann K, Peters RS, Donath A, Mayer C, et al. Phylogenomics resolves the timing and pattern of insect evolution. Science. 2014;346(6210):763–767. doi: 10.1126/science.1257570. PubMed DOI

Vlkova M, Sima M, Rohousova I, Kostalova T, Sumova P, Volfova V, et al. Comparative analysis of salivary gland transcriptomes of Phlebotomus orientalis sand flies from endemic and non-endemic foci of visceral leishmaniasis. PLoS Negl Trop Dis. 2014;8(2):e2709. doi: 10.1371/journal.pntd.0002709. PubMed DOI PMC

Abdeladhim M, Jochim RC, Ben Ahmed M, Zhioua E, Chelbi I, Cherni S, et al. Updating the salivary gland transcriptome of Phlebotomus papatasi (Tunisian strain): the search for sand fly-secreted immunogenic proteins for humans. PLoS One. 2012;7(11):e47347. doi: 10.1371/journal.pone.0047347. PubMed DOI PMC

Kato H, Anderson JM, Kamhawi S, Oliveira F, Lawyer PG, Pham VM, et al. High degree of conservancy among secreted salivary gland proteins from two geographically distant Phlebotomus duboscqi sandflies populations (Mali and Kenya) BMC Genomics. 2006;7:226. doi: 10.1186/1471-2164-7-226. PubMed DOI PMC

Kato H, Jochim RC, Gomez EA, Uezato H, Mimori T, Korenaga M, et al. Analysis of salivary gland transcripts of the sand fly Lutzomyia ayacuchensis, a vector of Andean-type cutaneous leishmaniasis. Infect Genet Evol. 2013;13:56–66. doi: 10.1016/j.meegid.2012.08.024. PubMed DOI PMC

Rohousova I, Subrahmanyam S, Volfova V, Mu J, Volf P, Valenzuela JG, et al. Salivary gland transcriptomes and proteomes of Phlebotomus tobbi and Phlebotomus sergenti, vectors of leishmaniasis. PLoS Negl Trop Dis. 2012;6(5):e1660. doi: 10.1371/journal.pntd.0001660. PubMed DOI PMC

Hostomska J, Volfova V, Mu J, Garfield M, Rohousova I, Volf P, et al. Analysis of salivary transcripts and antigens of the sand fly Phlebotomus arabicus. BMC Genomics. 2009;10:282. doi: 10.1186/1471-2164-10-282. PubMed DOI PMC

Pitaluga AN, Beteille V, Lobo AR, Ortigao-Farias JR, Davila AM, Souza AA, et al. EST sequencing of blood-fed and Leishmania-infected midgut of Lutzomyia longipalpis, the principal visceral leishmaniasis vector in the Americas. Mol Genet Genomics. 2009;282(3):307–317. doi: 10.1007/s00438-009-0466-2. PubMed DOI

Jochim RC, Teixeira CR, Laughinghouse A, Mu J, Oliveira F, Gomes RB, et al. The midgut transcriptome of Lutzomyia longipalpis: comparative analysis of cDNA libraries from sugar-fed, blood-fed, post-digested and Leishmania infantum chagasi-infected sand flies. BMC Genomics. 2008;9:15. doi: 10.1186/1471-2164-9-15. PubMed DOI PMC

Ramalho-Ortigao M, Jochim RC, Anderson JM, Lawyer PG, Pham VM, Kamhawi S, et al. Exploring the midgut transcriptome of Phlebotomus papatasi: comparative analysis of expression profiles of sugar-fed, blood-fed and Leishmania-major-infected sandflies. BMC Genomics. 2007;8:300. doi: 10.1186/1471-2164-8-300. PubMed DOI PMC

Gonzalez-Caballero N, Valenzuela JG, Ribeiro JM, Cuervo P, Brazil RP. Transcriptome exploration of the sex pheromone gland of Lutzomyia longipalpis (Diptera: Psychodidae: Phlebotominae) Parasit Vectors. 2013;6:56. doi: 10.1186/1756-3305-6-56. PubMed DOI PMC

Dillon RJ, Ivens AC, Churcher C, Holroyd N, Quail MA, Rogers ME, et al. Analysis of ESTs from Lutzomyia longipalpis sand flies and their contribution toward understanding the insect-parasite relationship. Genomics. 2006;88(6):831–840. doi: 10.1016/j.ygeno.2006.06.011. PubMed DOI PMC

Abrudan J, Ramalho-Ortigao M, O’Neil S, Stayback G, Wadsworth M, Bernard M, et al. The characterization of the Phlebotomus papatasi transcriptome. Insect Mol Biol. 2013;22(2):211–232. doi: 10.1111/imb.12015. PubMed DOI PMC

McCarthy CB, Santini MS, Pimenta PF, Diambra LA. First comparative transcriptomic analysis of wild adult male and female Lutzomyia longipalpis, vector of visceral leishmaniasis. PLoS One. 2013;8(3):e58645. doi: 10.1371/journal.pone.0058645. PubMed DOI PMC

Anderson JM, Oliveira F, Kamhawi S, Mans BJ, Reynoso D, Seitz AE, et al. Comparative salivary gland transcriptomics of sandfly vectors of visceral leishmaniasis. BMC Genomics. 2006;7:52. doi: 10.1186/1471-2164-7-52. PubMed DOI PMC

Dostalova A, Votypka J, Favreau AJ, Barbian KD, Volf P, Valenzuela JG, et al. The midgut transcriptome of Phlebotomus (Larroussius) perniciosus, a vector of Leishmania infantum: comparison of sugar fed and blood fed sand flies. BMC Genomics. 2011;12:223. doi: 10.1186/1471-2164-12-223. PubMed DOI PMC

Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol. 2011;29(7):644–652. doi: 10.1038/nbt.1883. PubMed DOI PMC

Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, et al. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc. 2013;8(8):1494–1512. doi: 10.1038/nprot.2013.084. PubMed DOI PMC

Davidson NM, Oshlack A. Corset: enabling differential gene expression analysis for de novo assembled transcriptomes. Genome Biol. 2014;15(7):410. PubMed PMC

O’Neil ST, Dzurisin JD, Carmichael RD, Lobo NF, Emrich SJ, Hellmann JJ. Population-level transcriptome sequencing of nonmodel organisms Erynnis propertius and Papilio zelicaon. BMC Genomics. 2010;11:310. doi: 10.1186/1471-2164-11-310. PubMed DOI PMC

Ewen-Campen B, Shaner N, Panfilio KA, Suzuki Y, Roth S, Extavour CG. The maternal and early embryonic transcriptome of the milkweed bug Oncopeltus fasciatus. BMC Genomics. 2011;12:61. doi: 10.1186/1471-2164-12-61. PubMed DOI PMC

Van Belleghem SM, Roelofs D, Van Houdt J, Hendrickx F. De novo transcriptome assembly and SNP discovery in the wing polymorphic salt marsh beetle Pogonus chalceus (Coleoptera, Carabidae) PLoS One. 2012;7(8):e42605. doi: 10.1371/journal.pone.0042605. PubMed DOI PMC

Salvemini M, Arunkumar KP, Nagaraju J, Sanges R, Petrella V, Tomar A, et al. De novo assembly and transcriptome analysis of the Mediterranean fruit fly Ceratitis capitata early embryos. PLoS One. 2014;9(12):e114191. doi: 10.1371/journal.pone.0114191. PubMed DOI PMC

Li W, Godzik A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics. 2006;22(13):1658–1659. doi: 10.1093/bioinformatics/btl158. PubMed DOI

Musacchia F, Basu S, Petrosino G, Salvemini M, Sanges R. Annocript: a flexible pipeline for the annotation of transcriptomes able to identify putative long noncoding RNAs. Bioinformatics. 2015;31(13):2199–2201. doi: 10.1093/bioinformatics/btv106. PubMed DOI

Gong ZJ, Wu YQ, Miao J, Duan Y, Jiang YL, Li T. Global transcriptome analysis of orange wheat blossom midge, Sitodiplosis mosellana (Gehin) (Diptera: Cecidomyiidae) to identify candidate transcripts regulating diapause. PLoS One. 2013;8(8):e71564. doi: 10.1371/journal.pone.0071564. PubMed DOI PMC

Chen B, Zhang YJ, He Z, Li W, Si F, Tang Y, et al. De novo transcriptome sequencing and sequence analysis of the malaria vector Anopheles sinensis (Diptera: Culicidae) Parasit Vectors. 2014;7:314. doi: 10.1186/1756-3305-7-314. PubMed DOI PMC

Arrial RT, Togawa RC, Brigido Mde M. Screening non-coding RNAs in transcriptomes from neglected species using PORTRAIT: case study of the pathogenic fungus Paracoccidioides brasiliensis. BMC Bioinf. 2009;10:239. doi: 10.1186/1471-2105-10-239. PubMed DOI PMC

Wang L, Park HJ, Dasari S, Wang S, Kocher JP, Li W. CPAT: coding-potential assessment tool using an alignment-free logistic regression model. Nucleic Acids Res. 2013;41(6):e74. doi: 10.1093/nar/gkt006. PubMed DOI PMC

Kong L, Zhang Y, Ye ZQ, Liu XQ, Zhao SQ, Wei L, et al. CPC: assess the protein-coding potential of transcripts using sequence features and support vector machine. Nucleic Acids Res. 2007;35(Web Server issue):W345–349. doi: 10.1093/nar/gkm391. PubMed DOI PMC

Niazi F, Valadkhan S. Computational analysis of functional long noncoding RNAs reveals lack of peptide-coding capacity and parallels with 3’ UTRs. RNA. 2012;18(4):825–843. doi: 10.1261/rna.029520.111. PubMed DOI PMC

Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods. 2008;5(7):621–628. doi: 10.1038/nmeth.1226. PubMed DOI

Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinf. 2011;12:323. doi: 10.1186/1471-2105-12-323. PubMed DOI PMC

Smartt CT, Kim AP, Grossman GL, James AA. The Apyrase gene of the vector mosquito, Aedes aegypti, is expressed specifically in the adult female salivary glands. Exp Parasitol. 1995;81(3):239–248. doi: 10.1006/expr.1995.1114. PubMed DOI

Vyazunova I, Lan Q. Stage-specific expression of two actin genes in the yellow fever mosquito, Aedes aegypti. Insect Mol Biol. 2004;13(3):241–249. doi: 10.1111/j.0962-1075.2004.00481.x. PubMed DOI

Andersen CL, Jensen JL, Orntoft TF. Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res. 2004;64(15):5245–5250. doi: 10.1158/0008-5472.CAN-04-0496. PubMed DOI

Leger N, Pesson B, Madulo-Leblond G, Abonnenc E. [Differentiation of females of the subgenus Larroussius Nitzulescu 1931 (Diptera-Phlebotomidae) of the Mediterranean region] Ann Parasitol Hum Comp. 1983;58(6):611–623. PubMed

Killick-Kendrick R, Tang Y, Killick-Kendrick M, Sang DK, Sirdar MK, Ke L, et al. The identification of female sandflies of the subgenus Larroussius by the morphology of the spermathecal ducts. Parassitologia. 1991;33(Suppl):335–347. PubMed

Mank JE. Sex chromosomes and the evolution of sexual dimorphism: lessons from the genome. Am Nat. 2009;173(2):141–150. doi: 10.1086/595754. PubMed DOI

Robinson MD, McCarthy DJ, Smyth GK. edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26(1):139–140. doi: 10.1093/bioinformatics/btp616. PubMed DOI PMC

Graveley BR, Brooks AN, Carlson JW, Duff MO, Landolin JM, Yang L, et al. The developmental transcriptome of Drosophila melanogaster. Nature. 2011;471(7339):473–479. doi: 10.1038/nature09715. PubMed DOI PMC

Magnusson K, Mendes AM, Windbichler N, Papathanos PA, Nolan T, Dottorini T, et al. Transcription regulation of sex-biased genes during ontogeny in the malaria vector Anopheles gambiae. PLoS One. 2011;6(6):e21572. doi: 10.1371/journal.pone.0021572. PubMed DOI PMC

Wen Z, Scott JG. Cytochrome P450 CYP6L1 is specifically expressed in the reproductive tissues of adult male German cockroaches, Blattella germanica (L.) Insect Biochem Mol Biol. 2001;31(2):179–187. doi: 10.1016/S0965-1748(00)00116-8. PubMed DOI

Kasai S, Tomita T. Male specific expression of a cytochrome P450 (Cyp312a1) in Drosophila melanogaster. Biochem Biophys Res Commun. 2003;300(4):894–900. doi: 10.1016/S0006-291X(02)02950-9. PubMed DOI

Huber DP, Erickson ML, Leutenegger CM, Bohlmann J, Seybold SJ. Isolation and extreme sex-specific expression of cytochrome P450 genes in the bark beetle, Ips paraconfusus, following feeding on the phloem of host ponderosa pine, Pinus ponderosa. Insect Mol Biol. 2007;16(3):335–349. doi: 10.1111/j.1365-2583.2007.00731.x. PubMed DOI

Zhang Z, Xiao J, Wu J, Zhang H, Liu G, Wang X, et al. ParaAT: a parallel tool for constructing multiple protein-coding DNA alignments. Biochem Biophys Res Commun. 2012;419(4):779–781. doi: 10.1016/j.bbrc.2012.02.101. PubMed DOI

Hunt BG, Ometto L, Wurm Y, Shoemaker D, Yi SV, Keller L, et al. Relaxed selection is a precursor to the evolution of phenotypic plasticity. Proc Natl Acad Sci U S A. 2011;108(38):15936–15941. doi: 10.1073/pnas.1104825108. PubMed DOI PMC

Volf P, Volfova V. Establishment and maintenance of sand fly colonies. J Vector Ecol. 2011;36(Suppl 1):S1–9. doi: 10.1111/j.1948-7134.2011.00106.x. PubMed DOI

Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009;10(3):R25. doi: 10.1186/gb-2009-10-3-r25. PubMed DOI PMC

Anders S, Huber W. Differential expression analysis for sequence count data. Genome Biol. 2010;11(10):R106. doi: 10.1186/gb-2010-11-10-r106. PubMed DOI PMC

Zhao S, Fernald RD. Comprehensive algorithm for quantitative real-time polymerase chain reaction. J Comput Biol. 2005;12(8):1047–1064. doi: 10.1089/cmb.2005.12.1047. PubMed DOI PMC

Salvemini M, Mauro U, Velaeti S, Polito C, Saccone G. A new Minos vector for eye-specific expression of white+ marker in Ceratitis capitata and in distantly related dipteran species. Insect Mol Biol. 2006;15(3):341–349. doi: 10.1111/j.1365-2583.2006.00651.x. PubMed DOI

Yang Z, Nielsen R. Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol Biol Evol. 2000;17(1):32–43. doi: 10.1093/oxfordjournals.molbev.a026236. PubMed DOI

Zhang Z, Li J, Zhao XQ, Wang J, Wong GK, Yu J. KaKs_Calculator: calculating Ka and Ks through model selection and model averaging. Genomics Proteomics Bioinformatics. 2006;4(4):259–263. doi: 10.1016/S1672-0229(07)60007-2. PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...