Genomic analysis of the causative agents of coccidiosis in domestic chickens

Genome Research

Volumn 24, Issue 10, 2014, Pages 1676-1685

  Reid, Adam J ^a   Blake, Damer P ^b,c   Ansari, Hifzur R ^d   Billington, Karen ^c   Browne, Hilary P ^a   Bryant, Josephine ^a   Dunn, Matt ^a   Hung, Stacy S ^e   Kawahara, Fumiya ^f   Miranda Saavedra, Diego ^g   Malas, Tareq B ^d   Mourier, Tobias ^h   Naghra, Hardeep ^a,i   Nair, Mridul ^d   Otto, Thomas D ^a   Rawlings, Neil D ^j   Rivailler, Pierre ^c,k   Sanchez Flores, Alejandro ^l   Sanders, Mandy ^a   Subramaniam, Chandra ^c   Tay, Yea Ling ^m,n   Woo, Yong ^d   Wu, Xikun ^c,o   Barrell, Bart ^a   Dear, Paul H ^p   Doerig, Christian ^q   Gruber, Arthur ^r   Ivens, Alasdair C ^s   Parkinson, John ^e   Rajandream, Marie Adéle ^a   Shirley, Martin W ^c   Wan, Kiew Lian ^m,n   Berriman, Matthew ^a   Tomley, Fiona M ^b,c   Pain, Arnab ^d   more..

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^b ROYAL VETERINARY COLLEGE   (United Kingdom)

^c INSTITUTE FOR ANIMAL HEALTH   (United Kingdom)

^d KING ABDULLAH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Saudi Arabia)

^e HOSPITAL FOR SICK CHILDREN   (Canada)

^f NIPPON INSTITUTE FOR BIOLOGICAL SCIENCE   (Japan)

^g NEWCASTLE UNIVERSITY   (United Kingdom)

^h UNIVERSITY OF COPENHAGEN   (Denmark)

ⁱ UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^j EUROPEAN BIOINFORMATICS INSTITUTE   (United Kingdom)

^k CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^l INSTITUTO DE BIOTECNOLOGÍA   (Mexico)

^m UNIVERSITI KEBANGSAAN MALAYSIA   (Malaysia)

ⁿ MALAYSIA GENOME INSTITUTE   (Malaysia)

^o AMGEN LTD   (United Kingdom)

^p MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^q MONASH UNIVERSITY   (Australia)

^r UNIVERSITY OF SÃO PAULO   (Brazil)

^s UNIVERSITY OF EDINBURGH   (United Kingdom)

more..

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; PROTEOME; PROTOZOAL PROTEIN;

ADAPTATION; APICOMPLEXAN LIFE CYCLE STAGE; ARTICLE; CHICKEN; COCCIDIOSIS; CONTROLLED STUDY; DOMESTIC ANIMAL; EIMERIA; GENE SEQUENCE; GENOMICS; HOST CELL; HOST PARASITE INTERACTION; NONHUMAN; RETROPOSON; ANIMAL; BIRD DISEASE; CELL LINE; CHROMOSOMAL MAPPING; CLASSIFICATION; GENE EXPRESSION PROFILING; GENETICS; GENOME; PARASITOLOGY; PHYLOGENY; SYNTENY; VETERINARY;

ANIMALS; CELL LINE; CHICKENS; CHROMOSOME MAPPING; COCCIDIOSIS; EIMERIA; GENE EXPRESSION PROFILING; GENOME, PROTOZOAN; PHYLOGENY; POULTRY DISEASES; PROTEOME; PROTOZOAN PROTEINS; SYNTENY;

EID: 84907481921     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.168955.113     Document Type: Article

References (60)

1. Allen PC, Jenkins MC. 2010. Observations on the gross pathology of Eimeria praecox infections in chickens. Avian Dis 54: 834-840.
2. Anamika, Srinivasan N, Krupa A. 2005. A genomic perspective of protein kinases in Plasmodium falciparum. Proteins 58: 180-189.
3. Arredondo SA, CaiM, Takayama Y, MacDonald NJ, Anderson DE, Aravind L, Clore GM, Miller LH. 2012. Structure of the Plasmodium 6-cysteine s48/45 domain. Proc Natl Acad Sci 109: 6692-6697.
4. Balaji S, Babu MM, Iyer LM, Aravind L. 2005. Discovery of the principal specific transcription factors of Apicomplexa and their implication for the evolution of the AP2-integrase DNA binding domains. Nucleic Acids Res 33: 3994-4006.
5. Batzoglou S, Jaffe DB, Stanley K, Butler J, Gnerre S, Mauceli E, Berger B, Mesirov JP, Lander ES. 2002. ARACHNE: a whole-genome shotgun assembler. Genome Res 12: 177-189.
6. Benson G. 1999. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 27: 573-580.
7. Blake DP, Billington KJ, Copestake SL, Oakes RD, Quail MA, Wan KL, Shirley MW, Smith AL. 2011. Genetic mapping identifies novel highly protective antigens for an apicomplexan parasite. PLoS Pathog 7: e1001279.
8. Boetzer M, Henkel CV, Jansen HJ, Butler D, Pirovano W. 2011. Scaffolding pre-assembled contigs using SSPACE. Bioinformatics 27: 578-579.
9. Campbell TL, De Silva EK, Olszewski KL, Elemento O, Llinas M. 2010. Identification and genome-wide prediction of DNA binding specificities for the ApiAP2 family of regulators from the malaria parasite. PLoS Pathog 6: e1001165.
10. Capella-Gutierrez S, Silla-Martinez JM, Gabaldon T. 2009. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25: 1972-1973.
11. Chalmers IW, Hoffmann KF. 2012. Platyhelminth Venom Allergen-Like (VAL) proteins: revealing structural diversity, class-specific features and biological associations across the phylum. Parasitology 139: 1231-1245.
12. Chapman HD, Barta JR, Blake D, Gruber A, Jenkins M, Smith NC, Suo X, Tomley FM. 2013. A selective review of advances in coccidiosis research. Adv Parasitol 83: 93-171.
13. Chow YP, Wan KL, Blake DP, Tomley F, Nathan S. 2011. Immunogenic Eimeria tenella glycosylphosphatidylinositol-anchored surface antigens (SAGs) induce inflammatory responses in avianmacrophages. PLoS ONE 6: e25233.
14. Clark JD, Billington K, Bumstead JM, Oakes RD, Soon PE, Sopp P, Tomley FM, Blake DP. 2008. A toolbox facilitating stable transfection of Eimeria species. Mol Biochem Parasitol 162: 77-86.
15. Coulson RM, Hall N, Ouzounis CA. 2004. Comparative genomics of transcriptional control in the human malaria parasite Plasmodium falciparum. Genome Res 14: 1548-1554.
16. del Cacho E, Pages M, Gallego M, Monteagudo L, Sanchez-Acedo C. 2005. Synaptonemal complex karyotype of Eimeria tenella. Int J Parasitol 35: 1445-1451.
17. Fentress SJ, Behnke MS, Dunay IR, Mashayekhi M, Rommereim LM, Fox BA, Bzik DJ, Taylor GA, Turk BE, Lichti CF, et al. 2010. Phosphorylation of immunity-related GTPases by a Toxoplasma gondii-secreted kinase promotesmacrophage survival and virulence.CellHostMicrobe 8: 484-495.
18. Gibbs GM, Roelants K, O'Bryan MK. 2008. The CAP superfamily: cysteinerich secretory proteins, antigen 5, and pathogenesis-related 1 proteins- roles in reproduction, cancer, and immune defense. Endocr Rev 29: 865-897.
19. He CY, Shaw MK, Pletcher CH, Striepen B, Tilney LG, Roos DS. 2001. A plastid segregation defect in the protozoan parasite Toxoplasma gondii. EMBO J 20: 330-339.
20. Jahn D, Matros A, Bakulina AY, Tiedemann J, Schubert U, Giersberg M, Haehnel S, Zoufal K, Mock HP, Kipriyanov SM. 2009. Model structure of the immunodominant surface antigen of Eimeria tenella identified as a target for sporozoite-neutralizing monoclonal antibody. Parasitol Res 105: 655-668.
21. Katoh K, Standley DM. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30: 772-780.
22. Kordis D. 2005. A genomic perspective on the chromodomain-containing retrotransposons: chromoviruses. Gene 347: 161-173.
23. Kozarewa I, Ning Z, Quail MA, Sanders MJ, Berriman M, Turner DJ. 2009. Amplification-free Illumina sequencing-library preparation facilitates improvedmapping and assembly of (G+C)-biased genomes. Nat Methods 6: 291-295.
24. Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA. 2009. Circos: an information aesthetic for comparative genomics. Genome Res 19: 1639-1645.
25. Kuck P, Meusemann K. 2010. FASconCAT: convenient handling of data matrices. Mol Phylogenet Evol 56: 1115-1118.
26. Le SQ, Dang CC, Gascuel O. 2012. Modeling protein evolution with several amino acid replacement matrices depending on site rates. Mol Biol Evol 29: 2921-2936.
27. Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754-1760.
28. Li L, Stoeckert CJ Jr, Roos DS. 2003. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 13: 2178-2189.
29. Liberator P, Anderson J, Feiglin M, Sardana M, Griffin P, Schmatz D, Myers RW. 1998. Molecular cloning and functional expression of mannitol-1-phosphatase from the apicomplexan parasite Eimeria tenella. J Biol Chem 273: 4237-4244.
30. Lim L, McFadden GI. 2010. The evolution, metabolism and functions of the apicoplast. Philos Trans R Soc Lond B Biol Sci 365: 749-763.
31. Ling KH, Rajandream MA, Rivailler P, Ivens A, Yap SJ, Madeira AM, Mungall K, Billington K, YeeWY, Bankier AT, et al. 2007. Sequencing and analysis of chromosome 1 of Eimeria tenella reveals a unique segmental organization. Genome Res 17: 311-319.
32. Long PL, Millard BJ, Joyner LP, Norton CC. 1976. A guide to laboratory techniques used in the study and diagnosis of avian coccidiosis. Folia Vet Lat 6: 201-217.
33. McDonald V, Shirley MW. 1987. The endogenous development of virulent strains and attenuated precocious lines of Eimeria tenella and E. necatrix. J Parasitol 73: 993-997.
34. McDougald LR, Jeffers TK. 1976. Eimeria tenella (Sporozoa, Coccidia): Gametogony following a single asexual generation. Science 192: 258-259.
35. Miranda-Saavedra D, Gabaldon T, Barton GJ, Langsley G, Doerig C. 2012. The kinomes of apicomplexan parasites. Microbes Infect 14: 796-810.
36. Novaes J, Rangel LT, Ferro M, Abe RY, Manha AP, de Mello JC, Varuzza L, Durham AM, Madeira AM, Gruber A. 2012. A comparative transcriptome analysis reveals expression profiles conserved across three Eimeria spp. of domestic fowl and associated with multiple developmental stages. Int J Parasitol 42: 39-48.
37. Ogedengbe JD, Hanner RH, Barta JR. 2011. DNA barcoding identifies Eimeria species and contributes to the phylogenetics of coccidian parasites (Eimeriorina, Apicomplexa, Alveolata). Int J Parasitol 41: 843-850.
38. Otto TD, Sanders M, Berriman M, Newbold C. 2010. Iterative Correction of Reference Nucleotides (iCORN) using second generation sequencing technology. Bioinformatics 26: 1704-1707.
39. Parra G, BradnamK, Korf I. 2007. CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes. Bioinformatics 23: 1061-1067.
40. Peixoto L, Chen F, HarbOS, Davis PH, Beiting DP, Brownback CS,Ouloguem D, Roos DS. 2010. Integrative genomic approaches highlight a family of parasite-specific kinases that regulate host responses. Cell HostMicrobe 8: 208-218.
41. PerutzMF, Pope BJ,Owen D,Wanker EE, Scherzinger E. 2002. Aggregation of proteins with expanded glutamine and alanine repeats of the glutamine-rich and asparagine-rich domains of Sup35 and of the amyloid b-peptide of amyloid plaques. Proc Natl Acad Sci 99: 5596-5600.
42. Reid AJ, Vermont SJ, Cotton JA, Harris D, Hill-Cawthorne GA, Konen-Waisman S, Latham SM, Mourier T, Norton R, Quail MA, et al. 2012. Comparative genomics of the apicomplexan parasites Toxoplasma gondii and Neospora caninum:Coccidia differing in host range and transmission strategy. PLoS Pathog 8: e1002567.
43. Saeij JP, Coller S, Boyle JP, Jerome ME, White MW, Boothroyd JC. 2007. Toxoplasma co-opts host gene expression by injection of a polymorphic kinase homologue. Nature 445: 324-327.
44. Schmatz DM, Baginsky WF, Turner MJ. 1989. Evidence for and characterization of a mannitol cycle in Eimeria tenella. Mol Biochem Parasitol 32: 263-270.
45. ShirleyMW, Smith AL, Tomley FM. 2005. The biology of avian Eimeria with an emphasis on their control by vaccination. Adv Parasitol 60: 285-330.
46. Si Y, Liu P, Li P, Brutnell TP. 2014. Model-based clustering for RNA-seq data. Bioinformatics 30: 197-205.
47. Sobreira TJ, Durham AM, Gruber A. 2006. TRAP: automated classification, quantification and annotation of tandemly repeated sequences. Bioinformatics 22: 361-362.
48. Spence PJ, Jarra W, Levy P, Reid AJ, Chappell L, Brugat T, Sanders M, Berriman M, Langhorne J. 2013. Vector transmission regulates immune control of Plasmodium virulence. Nature 498: 228-231.
49. Stamatakis A, Ludwig T, Meier H. 2005. RAxML-III: a fast program for maximum likelihood-based inference of large phylogenetic trees. Bioinformatics 21: 456-463.
50. Su H, Liu X, Yan W, Shi T, Zhao X, Blake DP, Tomley FM, Suo X. 2012. piggyBac transposon-mediated transgenesis in the apicomplexan parasite Eimeria tenella. PLoS ONE 7: e40075.
51. Tabares E, Ferguson D, Clark J, Soon PE, Wan KL, Tomley F. 2004. Eimeria tenella sporozoites and merozoites differentially express glycosylphosphatidylinositol-anchored variant surface proteins. Mol Biochem Parasitol 135: 123-132.
52. Talevich E, Kannan N. 2013. Structural and evolutionary adaptation of rhoptry kinases and pseudokinases, a family of coccidian virulence factors. BMC Evol Biol 13: 117.
53. Talevich E, Mirza A, Kannan N. 2011. Structural and evolutionary divergence of eukaryotic protein kinases in Apicomplexa. BMC Evol Biol 11: 321.
54. Tsai IJ, Otto TD, Berriman M. 2010. Improving draft assemblies by iterative mapping and assembly of short reads to eliminate gaps. Genome Biol 11: R41.
55. van Dooren GG, Tomova C, Agrawal S, Humbel BM, Striepen B. 2008. Toxoplasma gondii Tic20 is essential for apicoplast protein import. Proc Natl Acad Sci 105: 13574-13579.
56. Wang Y, Tang H, Debarry JD, Tan X, Li J, Wang X, Lee TH, Jin H, Marler B, Guo H, et al. 2012. MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res 40: e49.
57. Ward P, Equinet L, Packer J, Doerig C. 2004. Protein kinases of the human malaria parasite Plasmodium falciparum: the kinome of a divergent eukaryote. BMC Genomics 5: 79.
58. Williams RB. 1998. Epidemiological aspects of the use of live anticoccidial vaccines for chickens. Int J Parasitol 28: 1089-1098.
59. Wootton JC, Federhen S. 1996. Analysis of compositionally biased regions in sequence databases. Methods Enzymol 266: 554-571.
60. Zerbino DR, Birney E. 2008. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18: 821-829.