Genomic introgression mapping of field-derived multiple-anthelmintic resistance in Teladorsagia circumcincta

PLoS Genetics

Volumn 13, Issue 6, 2017, Pages

  Choi, Young Jun ^a   Bisset, Stewart A ^b   Doyle, Stephen R ^c,d   Hallsworth Pepin, Kymberlie ^a   Martin, John ^a   Grant, Warwick N ^c   Mitreva, Makedonka ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b AGRESEARCH GRASSLANDS   (New Zealand)

^c LA TROBE UNIVERSITY   (Australia)

^d WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

IVERMECTIN; LEVAMISOLE; OXFENDAZOLE; ANTHELMINTIC AGENT;

ANIMAL EXPERIMENT; ARTICLE; BACKCROSSING; CONTROLLED STUDY; DRUG RESISTANCE; FEMALE; GENE; GENE MAPPING; GENE TARGETING; GENETIC ANALYSIS; GENETIC IDENTIFICATION; GENETIC RESISTANCE; GENETIC SUSCEPTIBILITY; GENETIC VARIABILITY; GENETIC VARIATION; GENOTYPE; INTROGRESSION; MALE; NONHUMAN; PROGENY; RNA SEQUENCE; SINGLE NUCLEOTIDE POLYMORPHISM; TELADORSAGIA CIRCUMCINCTA; WHOLE GENOME SEQUENCING; ANIMAL; CHROMOSOMAL MAPPING; COPY NUMBER VARIATION; DRUG EFFECTS; GENETICS; HUMAN; PARASITOLOGY; PATHOGENICITY; SHEEP; TRICHOSTRONGYLOIDEA; TRICHOSTRONGYLOIDIASIS;

ANIMALS; ANTHELMINTICS; CHROMOSOME MAPPING; DNA COPY NUMBER VARIATIONS; DRUG RESISTANCE; GENOTYPE; HUMANS; SHEEP; TRICHOSTRONGYLOIDEA; TRICHOSTRONGYLOIDIASIS;

EID: 85021841493     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1006857     Document Type: Article

References (108)

1. Geary TG, Are new anthelmintics needed to eliminate human helminthiases?Current opinion in infectious diseases. 2012;25(6):709–17. doi: 10.1097/QCO.0b013e328359f04a 23041774
2. Kaplan RM, Drug resistance in nematodes of veterinary importance: a status report. Trends in parasitology. 2004;20(10):477–81. doi: 10.1016/j.pt.2004.08.001 15363441
3. Prichard RK, Basanez MG, Boatin BA, McCarthy JS, Garcia HH, Yang GJ, et al. A research agenda for helminth diseases of humans: intervention for control and elimination. PLoS neglected tropical diseases. 2012;6(4):e1549. doi: 10.1371/journal.pntd.0001549 22545163
4. Gilleard JS, Beech RN, Population genetics of anthelmintic resistance in parasitic nematodes. Parasitology. 2007;134(Pt 8):1133–47. doi: 10.1017/S0031182007000066 17608973
5. James CE, Hudson AL, Davey MW, Drug resistance mechanisms in helminths: is it survival of the fittest?Trends in parasitology. 2009;25(7):328–35. doi: 10.1016/j.pt.2009.04.004 19541539
6. Gilleard JS, Understanding anthelmintic resistance: the need for genomics and genetics. Int J Parasitol. 2006;36(12):1227–39. doi: 10.1016/j.ijpara.2006.06.010 16889782
7. Kotze AC, Hunt PW, Skuce P, von Samson-Himmelstjerna G, Martin RJ, Sager H, et al. Recent advances in candidate-gene and whole-genome approaches to the discovery of anthelmintic resistance markers and the description of drug/receptor interactions. Int J Parasitol Drugs Drug Resist. 2014;4(3):164–84. doi: 10.1016/j.ijpddr.2014.07.007 25516826
8. Gilleard JS, Haemonchus contortus as a paradigm and model to study anthelmintic drug resistance. Parasitology. 2013;140(12):1506–22. doi: 10.1017/S0031182013001145 23998513
9. Braisher TL, Gemmell NJ, Grenfell BT, Amos W, Host isolation and patterns of genetic variability in three populations of Teladorsagia from sheep. Int J Parasitol. 2004;34(10):1197–204. doi: 10.1016/j.ijpara.2004.06.005 15380691
10. Anderson TJ, Blouin MS, Beech RN, Population biology of parasitic nematodes: applications of genetic markers. Advances in parasitology. 1998;41:219–83. 9734295
11. Blouin MS, Yowell CA, Courtney CH, Dame JB, Host movement and the genetic structure of populations of parasitic nematodes. Genetics. 1995;141(3):1007–14. 8582607
12. Redman E, Sargison N, Whitelaw F, Jackson F, Morrison A, Bartley DJ, et al. Introgression of ivermectin resistance genes into a susceptible Haemonchus contortus strain by multiple backcrossing. PLoS pathogens. 2012;8(2):e1002534. doi: 10.1371/journal.ppat.1002534 22359506
13. Le Jambre LF, Lenane IJ, Wardrop AJ, A hybridisation technique to identify anthelmintic resistance genes in Haemonchus. Int J Parasitol. 1999;29(12):1979–85. 10961854
14. Chevalier FD, Valentim CL, LoVerde PT, Anderson TJ, Efficient linkage mapping using exome capture and extreme QTL in schistosome parasites. BMC Genomics. 2014;15:617. doi: 10.1186/1471-2164-15-617 25048426
15. Bisset SA. The genetic basis of multiple-anthelmintic resistance in Teladorsagia circumcincta, a gastrointestinal nematode parasite of sheep and goats. PhD thesis. Flinders University of South Australia. 2007.
16. Pomroy WE, Anthelmintic resistance in New Zealand: a perspective on recent findings and options for the future. New Zealand veterinary journal. 2006;54(6):265–70. doi: 10.1080/00480169.2006.36709 17151723
17. Scott I, Pomroy WE, Kenyon PR, Smith G, Adlington B, Moss A, Lack of efficacy of monepantel against Teladorsagia circumcincta and Trichostrongylus colubriformis. Vet Parasitol. 2013;198(1–2):166–71. doi: 10.1016/j.vetpar.2013.07.037 23953148
18. Parra G, Bradnam K, Korf I, CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes. Bioinformatics. 2007;23(9):1061–7. doi: 10.1093/bioinformatics/btm071 17332020
19. Barriere A, Yang SP, Pekarek E, Thomas CG, Haag ES, Ruvinsky I, Detecting heterozygosity in shotgun genome assemblies: Lessons from obligately outcrossing nematodes. Genome Res. 2009;19(3):470–80. doi: 10.1101/gr.081851.108 19204328
20. Laing R, Kikuchi T, Martinelli A, Tsai IJ, Beech RN, Redman E, et al. The genome and transcriptome of Haemonchus contortus, a key model parasite for drug and vaccine discovery. Genome Biol. 2013;14(8):R88. doi: 10.1186/gb-2013-14-8-r88 23985316
21. Huang S, Chen Z, Huang G, Yu T, Yang P, Li J, et al. HaploMerger: reconstructing allelic relationships for polymorphic diploid genome assemblies. Genome Res. 2012;22(8):1581–8. doi: 10.1101/gr.133652.111 22555592
22. Driscoll M, Dean E, Reilly E, Bergholz E, Chalfie M, Genetic and molecular analysis of a Caenorhabditis elegans beta-tubulin that conveys benzimidazole sensitivity. The Journal of cell biology. 1989;109(6 Pt 1):2993–3003.
23. Saunders GI, Wasmuth JD, Beech R, Laing R, Hunt M, Naghra H, et al. Characterization and comparative analysis of the complete Haemonchus contortus beta-tubulin gene family and implications for benzimidazole resistance in strongylid nematodes. Int J Parasitol. 2013;43(6):465–75. doi: 10.1016/j.ijpara.2012.12.011 23416426
24. Von Samson-Himmelstjerna G, Blackhall WJ, McCarthy JS, Skuce PJ, Single nucleotide polymorphism (SNP) markers for benzimidazole resistance in veterinary nematodes. Parasitology. 2007;134(Pt 8):1077–86. doi: 10.1017/S0031182007000054 17608967
25. Beech RN, Prichard RK, Scott ME, Genetic variability of the beta-tubulin genes in benzimidazole-susceptible and -resistant strains of Haemonchus contortus. Genetics. 1994;138(1):103–10. 8001777
26. Kwa MS, Kooyman FN, Boersema JH, Roos MH, Effect of selection for benzimidazole resistance in Haemonchus contortus on beta-tubulin isotype 1 and isotype 2 genes. Biochem Biophys Res Commun. 1993;191(2):413–9. doi: 10.1006/bbrc.1993.1233 8096381
27. Kwa MS, Veenstra JG, Van Dijk M, Roos MH, Beta-tubulin genes from the parasitic nematode Haemonchus contortus modulate drug resistance in Caenorhabditis elegans. Journal of molecular biology. 1995;246(4):500–10. doi: 10.1006/jmbi.1994.0102 7877171
28. Ghisi M, Kaminsky R, Maser P, Phenotyping and genotyping of Haemonchus contortus isolates reveals a new putative candidate mutation for benzimidazole resistance in nematodes. Vet Parasitol. 2007;144(3–4):313–20. doi: 10.1016/j.vetpar.2006.10.003 17101226
29. Redman E, Whitelaw F, Tait A, Burgess C, Bartley Y, Skuce PJ, et al. The emergence of resistance to the benzimidazole anthlemintics in parasitic nematodes of livestock is characterised by multiple independent hard and soft selective sweeps. PLoS neglected tropical diseases. 2015;9(2):e0003494. doi: 10.1371/journal.pntd.0003494 25658086
30. Aguayo-Ortiz R, Mendez-Lucio O, Romo-Mancillas A, Castillo R, Yepez-Mulia L, Medina-Franco JL, et al. Molecular basis for benzimidazole resistance from a novel beta-tubulin binding site model. J Mol Graph Model. 2013;45:26–37. doi: 10.1016/j.jmgm.2013.07.008 23995453
31. Devillers-Thiery A, Galzi JL, Eisele JL, Bertrand S, Bertrand D, Changeux JP, Functional architecture of the nicotinic acetylcholine receptor: a prototype of ligand-gated ion channels. J Membr Biol. 1993;136(2):97–112. 7508983
32. Jones AK, Davis P, Hodgkin J, Sattelle DB, The nicotinic acetylcholine receptor gene family of the nematode Caenorhabditis elegans: an update on nomenclature. Invert Neurosci. 2007;7(2):129–31. doi: 10.1007/s10158-007-0049-z 17503100
33. Holden-Dye L, Joyner M, O'Connor V, Walker RJ, Nicotinic acetylcholine receptors: a comparison of the nAChRs of Caenorhabditis elegans and parasitic nematodes. Parasitology international. 2013;62(6):606–15. doi: 10.1016/j.parint.2013.03.004 23500392
34. Neveu C, Charvet CL, Fauvin A, Cortet J, Beech RN, Cabaret J, Genetic diversity of levamisole receptor subunits in parasitic nematode species and abbreviated transcripts associated with resistance. Pharmacogenet Genomics. 2010;20(7):414–25. doi: 10.1097/FPC.0b013e328338ac8c 20531256
35. Boulin T, Fauvin A, Charvet CL, Cortet J, Cabaret J, Bessereau JL, et al. Functional reconstitution of Haemonchus contortus acetylcholine receptors in Xenopus oocytes provides mechanistic insights into levamisole resistance. Br J Pharmacol. 2011;164(5):1421–32. doi: 10.1111/j.1476-5381.2011.01420.x 21486278
36. Buxton SK, Charvet CL, Neveu C, Cabaret J, Cortet J, Peineau N, et al. Investigation of acetylcholine receptor diversity in a nematode parasite leads to characterization of tribendimidine- and derquantel-sensitive nAChRs. PLoS pathogens. 2014;10(1):e1003870. doi: 10.1371/journal.ppat.1003870 24497826
37. Betts MJ, Russell RB, Barnes MR, Gray IC, Amino Acid Properties and Consequences of Substitutions. In: Bioinformatics for Geneticists. Hoboken: John Wiley & Sons; 2003. p. 289–316.
38. Williamson SM, Storey B, Howell S, Harper KM, Kaplan RM, Wolstenholme AJ, Candidate anthelmintic resistance-associated gene expression and sequence polymorphisms in a triple-resistant field isolate of Haemonchus contortus. Mol Biochem Parasitol. 2011;180(2):99–105. doi: 10.1016/j.molbiopara.2011.09.003 21945142
39. Sarai RS, Kopp SR, Coleman GT, Kotze AC, Acetylcholine receptor subunit and P-glycoprotein transcription patterns in levamisole-susceptible and -resistant Haemonchus contortus. Int J Parasitol Drugs Drug Resist. 2013;3:51–8. doi: 10.1016/j.ijpddr.2013.01.002 24533293
40. Sarai RS, Kopp SR, Coleman GT, Kotze AC, Drug-efflux and target-site gene expression patterns in Haemonchus contortus larvae able to survive increasing concentrations of levamisole in vitro. Int J Parasitol Drugs Drug Resist. 2014;4(2):77–84. doi: 10.1016/j.ijpddr.2014.02.001 25057457
41. Kagawa H, Takuwa K, Sakube Y, Mutations and expressions of the tropomyosin gene and the troponin C gene of Caenorhabditis elegans. Cell Struct Funct. 1997;22(1):213–8. 9113409
42. Gottschalk A, Almedom RB, Schedletzky T, Anderson SD, Yates JR, 3rdSchafer WR, Identification and characterization of novel nicotinic receptor-associated proteins in Caenorhabditis elegans. EMBO J. 2005;24(14):2566–78. doi: 10.1038/sj.emboj.7600741 15990870
43. Hobert O. The neuronal genome of Caenorhabditis elegans. In: The C. elegans Research Community, editor. WormBook.2013.
44. Harris TW, Antoshechkin I, Bieri T, Blasiar D, Chan J, Chen WJ, et al. WormBase: a comprehensive resource for nematode research. Nucleic Acids Res. 2010;38(Database issue):D463–7. doi: 10.1093/nar/gkp952 19910365
45. Beech RN, Callanan MK, Rao VT, Dawe GB, Forrester SG, Characterization of cys-loop receptor genes involved in inhibitory amine neurotransmission in parasitic and free living nematodes. Parasitology international. 2013;62(6):599–605. doi: 10.1016/j.parint.2013.03.010 23602737
46. Ringstad N, Abe N, Horvitz HR, Ligand-gated chloride channels are receptors for biogenic amines in C. elegans. Science. 2009;325(5936):96–100. doi: 10.1126/science.1169243 19574391
47. Pirri JK, McPherson AD, Donnelly JL, Francis MM, Alkema MJ, A tyramine-gated chloride channel coordinates distinct motor programs of a Caenorhabditis elegans escape response. Neuron. 2009;62(4):526–38. doi: 10.1016/j.neuron.2009.04.013 19477154
48. Rao VT, Siddiqui SZ, Prichard RK, Forrester SG, A dopamine-gated ion channel (HcGGR3*) from Haemonchus contortus is expressed in the cervical papillae and is associated with macrocyclic lactone resistance. Mol Biochem Parasitol. 2009;166(1):54–61. doi: 10.1016/j.molbiopara.2009.02.011 19428673
49. Ghosh R, Andersen EC, Shapiro JA, Gerke JP, Kruglyak L, Natural variation in a chloride channel subunit confers avermectin resistance in C. elegans. Science. 2012;335(6068):574–8. doi: 10.1126/science.1214318 22301316
50. Lynagh T, Lynch JW, Molecular mechanisms of Cys-loop ion channel receptor modulation by ivermectin. Front Mol Neurosci. 2012;5:60. doi: 10.3389/fnmol.2012.00060 22586367
51. Hibbs RE, Gouaux E, Principles of activation and permeation in an anion-selective Cys-loop receptor. Nature. 2011;474(7349):54–60. doi: 10.1038/nature10139 21572436
52. McCavera S, Walsh TK, Wolstenholme AJ, Nematode ligand-gated chloride channels: an appraisal of their involvement in macrocyclic lactone resistance and prospects for developing molecular markers. Parasitology. 2007;134(Pt 8):1111–21. doi: 10.1017/S0031182007000042 17608971
53. Wolstenholme AJ, Glutamate-gated chloride channels. J Biol Chem. 2012;287(48):40232–8. doi: 10.1074/jbc.R112.406280 23038250
54. Urdaneta-Marquez L, Bae SH, Janukavicius P, Beech R, Dent J, Prichard R, A dyf-7 haplotype causes sensory neuron defects and is associated with macrocyclic lactone resistance worldwide in the nematode parasite Haemonchus contortus. Int J Parasitol. 2014;44(14):1063–71. doi: 10.1016/j.ijpara.2014.08.005 25224687
55. Guerrero J, Freeman AS, Amphids: the neuronal ultrastructure of macrocyclic-lactone-resistant Haemonchus contortus. Parassitologia. 2004;46(1–2):237–40. 15305725
56. Dent JA, Smith MM, Vassilatis DK, Avery L, The genetics of ivermectin resistance in Caenorhabditis elegans. Proc Natl Acad Sci U S A. 2000;97(6):2674–9. 10716995
57. Laing R, Maitland K, Lecova L, Skuce PJ, Tait A, Devaney E, Analysis of putative resistance gene loci in UK field populations of Haemonchus contortus after 6years of macrocyclic lactone use. Int J Parasitol. 2016;46(10):621–30. doi: 10.1016/j.ijpara.2016.03.010 27179994
58. Rezansoff AM, Laing R, Gilleard JS, Evidence from two independent backcross experiments supports genetic linkage of microsatellite Hcms8a20, but not other candidate loci, to a major ivermectin resistance locus in Haemonchus contortus. Int J Parasitol. 2016;46(10):653–61. doi: 10.1016/j.ijpara.2016.04.007 27216082
59. Lespine A, Menez C, Bourguinat C, Prichard RK, P-glycoproteins and other multidrug resistance transporters in the pharmacology of anthelmintics: Prospects for reversing transport-dependent anthelmintic resistance. Int J Parasitol Drugs Drug Resist. 2012;2:58–75. doi: 10.1016/j.ijpddr.2011.10.001 24533264
60. Dicker AJ, Nisbet AJ, Skuce PJ, Gene expression changes in a P-glycoprotein (Tci-pgp-9) putatively associated with ivermectin resistance in Teladorsagia circumcincta. Int J Parasitol. 2011;41(9):935–42. doi: 10.1016/j.ijpara.2011.03.015 21683705
61. Arnold B, Corbett-Detig RB, Hartl D, Bomblies K, RADseq underestimates diversity and introduces genealogical biases due to nonrandom haplotype sampling. Mol Ecol. 2013;22(11):3179–90. doi: 10.1111/mec.12276 23551379
62. Ardelli BF, Transport proteins of the ABC systems superfamily and their role in drug action and resistance in nematodes. Parasitology international. 2013;62(6):639–46. doi: 10.1016/j.parint.2013.02.008 23474412
63. Tyden E, Skarin M, Hoglund J, Gene expression of ABC transporters in Cooperia oncophora after field and laboratory selection with macrocyclic lactones. Mol Biochem Parasitol. 2014;198(2):66–70. doi: 10.1016/j.molbiopara.2015.01.002 25619799
64. De Graef J, Demeler J, Skuce P, Mitreva M, Von Samson-Himmelstjerna G, Vercruysse J, et al. Gene expression analysis of ABC transporters in a resistant Cooperia oncophora isolate following in vivo and in vitro exposure to macrocyclic lactones. Parasitology. 2013;140(4):499–508. doi: 10.1017/S0031182012001849 23279803
65. Laing ST, Ivens A, Butler V, Ravikumar SP, Laing R, Woods DJ, et al. The transcriptional response of Caenorhabditis elegans to Ivermectin exposure identifies novel genes involved in the response to reduced food intake. PLoS One. 2012;7(2):e31367. doi: 10.1371/journal.pone.0031367 22348077
66. Doyle SR, Bourguinat C, Nana-Djeunga HC, Kengne-Ouafo JA, Pion SDS, Bopda J, et al. Genome-wide analysis of ivermectin response by Onchocerca volvulus reveals that genetic drift and soft selective sweeps contribute to loss of drug sensitivity; 2016. Preprint. Availabel from bioRxiv. doi: 10.1101/094540
67. Wood WB, The nematode Caenorhabditis elegans. New York: Cold Spring Harbour Laboratory Press; 1988.
68. Sulston J, Hodgkin J, Wood WB, Methods. In: The Nematode Caenorhabditis elegans. New York: Cold Spring Harbour Laboratory Press; 1988. p. 587–606.
69. Tang YT, Gao X, Rosa BA, Abubucker S, Hallsworth-Pepin K, Martin J, et al. Genome of the human hookworm Necator americanus. Nat Genet. 2014;46(3):261–9. doi: 10.1038/ng.2875 24441737
70. Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, Bemben LA, et al. Genome sequencing in microfabricated high-density picolitre reactors. Nature. 2005;437(7057):376–80. doi: 10.1038/nature03959 16056220
71. Kent WJ, BLAT—the BLAST-like alignment tool. Genome Res. 2002;12(4):656–64. doi: 10.1101/gr.229202 11932250
72. Benson G, Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res. 1999;27(2):573–80. 9862982
73. Lagesen K, Hallin P, Rodland EA, Staerfeldt HH, Rognes T, Ussery DW, RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res. 2007;35(9):3100–8. doi: 10.1093/nar/gkm160 17452365
74. Lowe TM, Eddy SR, tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 1997;25(5):955–64. 9023104
75. Griffiths-Jones S, Bateman A, Marshall M, Khanna A, Eddy SR, Rfam: an RNA family database. Nucleic Acids Res. 2003;31(1):439–41. 12520045
76. Korf I, Gene finding in novel genomes. BMC Bioinformatics. 2004;5:59. doi: 10.1186/1471-2105-5-59 15144565
77. Salamov AA, Solovyev VV, Ab initio gene finding in Drosophila genomic DNA. Genome Res. 2000;10(4):516–22. 10779491
78. Stanke M, Diekhans M, Baertsch R, Haussler D, Using native and syntenically mapped cDNA alignments to improve de novo gene finding. Bioinformatics. 2008;24(5):637–44. doi: 10.1093/bioinformatics/btn013 18218656
79. Cantarel BL, Korf I, Robb SM, Parra G, Ross E, Moore B, et al. MAKER: an easy-to-use annotation pipeline designed for emerging model organism genomes. Genome Res. 2008;18(1):188–96. doi: 10.1101/gr.6743907 18025269
80. Boeckmann B, Bairoch A, Apweiler R, Blatter MC, Estreicher A, Gasteiger E, et al. The SWISS-PROT protein knowledgebase and its supplement TrEMBL in 2003. Nucleic Acids Res. 2003;31(1):365–70. 12520024
81. Finn RD, Mistry J, Schuster-Böckler B, Griffiths-Jones S, Hollich V, Lassmann T, et al. Pfam: clans, web tools and services. Nucleic Acids Res. 2006;34(Database issue):D247–51. doi: 10.1093/nar/gkj149 16381856
82. Marchler-Bauer A, Lu S, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese-Scott C, et al. CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res. 2011;39(Database issue):D225–9. doi: 10.1093/nar/gkq1189 21109532
83. Kanehisa M, Goto S, Sato Y, Furumichi M, Tanabe M, KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res. 2012;40(Database issue):D109–14. doi: 10.1093/nar/gkr988 22080510
84. Zdobnov EM, Apweiler R, InterProScan—an integration platform for the signature-recognition methods in InterPro. Bioinformatics. 2001;17(9):847–8. 11590104
85. Kall L, Krogh A, Sonnhammer EL, A combined transmembrane topology and signal peptide prediction method. Journal of molecular biology. 2004;338(5):1027–36. doi: 10.1016/j.jmb.2004.03.016 15111065
86. Bendtsen JD, Jensen LJ, Blom N, Von Heijne G, Brunak S, Feature-based prediction of non-classical and leaderless protein secretion. Protein Eng Des Sel. 2004;17(4):349–56. doi: 10.1093/protein/gzh037 15115854
87. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S, MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol. 2013;30(12):2725–9. doi: 10.1093/molbev/mst197 24132122
88. Wang Z, Abubucker S, Martin J, Wilson RK, Hawdon J, Mitreva M, Characterizing Ancylostoma caninum transcriptome and exploring nematode parasitic adaptation. BMC Genomics. 2010;11:307. doi: 10.1186/1471-2164-11-307 20470405
89. Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 2013;29(1):15–21. doi: 10.1093/bioinformatics/bts635 23104886
90. Engstrom PG, Steijger T, Sipos B, Grant GR, Kahles A, Consortium R, et al. Systematic evaluation of spliced alignment programs for RNA-seq data. Nature methods. 2013;10(12):1185–91. doi: 10.1038/nmeth.2722 24185836
91. Feng J, Meyer CA, Wang Q, Liu JS, Shirley Liu X, Zhang Y, GFOLD: a generalized fold change for ranking differentially expressed genes from RNA-seq data. Bioinformatics. 2012;28(21):2782–8. doi: 10.1093/bioinformatics/bts515 22923299
92. Bolger AM, Lohse M, Usadel B, Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30(15):2114–20. doi: 10.1093/bioinformatics/btu170 24695404
93. Li H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv:13033997v2 [q-bioGN]. 2013.
94. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 2010;20(9):1297–303. doi: 10.1101/gr.107524.110 20644199
95. Kofler R, Pandey RV, Schlotterer C, PoPoolation2: identifying differentiation between populations using sequencing of pooled DNA samples (Pool-Seq). Bioinformatics. 2011;27(24):3435–6. doi: 10.1093/bioinformatics/btr589 22025480
96. Gasser T, Kneip A, Kohler W, A Flexible and Fast Method for Automatic Smoothing. J Am Stat Assoc. 1991;86(415):643–52.
97. Herrmann E, Local bandwidth choice in kernel regression estimation. J Comput Graph Stat. 1997;6(1):35–54.
98. Beissbarth T, Speed TP, GOstat: find statistically overrepresented Gene Ontologies within a group of genes. Bioinformatics. 2004;20(9):1464–5. doi: 10.1093/bioinformatics/bth088 14962934
99. Nijveen H, van Kaauwen M, Esselink DG, Hoegen B, Vosman B, QualitySNPng: a user-friendly SNP detection and visualization tool. Nucleic Acids Res. 2013;41(Web Server issue):W587–90. doi: 10.1093/nar/gkt333 23632165
100. Tang J, Vosman B, Voorrips RE, van der Linden CG, Leunissen JA, QualitySNP: a pipeline for detecting single nucleotide polymorphisms and insertions/deletions in EST data from diploid and polyploid species. BMC Bioinformatics. 2006;7:438. doi: 10.1186/1471-2105-7-438 17029635
101. Li H, FermiKit: assembly-based variant calling for Illumina resequencing data. Bioinformatics. 2015;31(22):3694–6. doi: 10.1093/bioinformatics/btv440 26220959
102. Xie C, Tammi MT, CNV-seq, a new method to detect copy number variation using high-throughput sequencing. BMC Bioinformatics. 2009;10:80. doi: 10.1186/1471-2105-10-80 19267900
103. Kofler R, Orozco-terWengel P, De Maio N, Pandey RV, Nolte V, Futschik A, et al. PoPoolation: a toolbox for population genetic analysis of next generation sequencing data from pooled individuals. PLoS One. 2011;6(1):e15925. doi: 10.1371/journal.pone.0015925 21253599
104. Lennon NJ, Lintner RE, Anderson S, Alvarez P, Barry A, Brockman W, et al. A scalable, fully automated process for construction of sequence-ready barcoded libraries for 454. Genome Biol. 2010;11(2):R15. doi: 10.1186/gb-2010-11-2-r15 20137071
105. Catchen J, Hohenlohe PA, Bassham S, Amores A, Cresko WA, Stacks: an analysis tool set for population genomics. Mol Ecol. 2013;22(11):3124–40. doi: 10.1111/mec.12354 23701397
106. Weir BS, Cockerham CC, Estimating F-Statistics for the Analysis of Population Structure. Evolution. 1984;38(6):1358–70. doi: 10.1111/j.1558-5646.1984.tb05657.x 28563791
107. Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, et al. The variant call format and VCFtools. Bioinformatics. 2011;27(15):2156–8. doi: 10.1093/bioinformatics/btr330 21653522
108. Humbert J-F, Elard L, A simple PCR method for rapidly detecting defined point mutations. Technical Tips Online. 1997;2(1):48–9.