Whole genome profiling of spontaneous and chemically induced mutations in Toxoplasma gondii

BMC Genomics

Volumn 15, Issue 1, 2014, Pages

  Farrell, Andrew ^a   Coleman, Bradley I ^a   Benenati, Brian ^a   Brown, Kevin M ^b,c   Blader, Ira J ^b,d   Marth, Gabor T ^a   Gubbels, Marc Jan ^a  

^a BOSTON COLLEGE   (United States)

^b UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY AT BUFFALO   (United States)

Author keywords

Apicomplexa; Chemical mutagenesis; In vitro adaptation; SNV calling; Whole genome sequencing

Indexed keywords

ETHYLNITROSOUREA; MESYLIC ACID ETHYL ESTER; ADENOSINE; GLYCOSYLTRANSFERASE; PROTOZOAL PROTEIN; THYMIDINE; URACIL PHOSPHORIBOSYLTRANSFERASE;

AMINO ACID SEQUENCE; ARTICLE; CHEMICAL MUTAGENESIS; EXON; GENE SEQUENCE; GENETIC VARIABILITY; GENOME ANALYSIS; IN VITRO STUDY; MUTATIONAL ANALYSIS; NONHUMAN; TOXOPLASMA GONDII; BASE PAIRING; CELL LINE; DRUG EFFECTS; GENETICS; GENOME; HIGH THROUGHPUT SEQUENCING; HUMAN; METABOLISM; MOLECULAR GENETICS; PHENOTYPE; POINT MUTATION; TOXOPLASMA;

APICOMPLEXA; PLASMODIUM (APICOMPLEXA); PROTOZOA; TOXOPLASMA; TOXOPLASMA GONDII;

ADENOSINE; AMINO ACID SEQUENCE; BASE PAIRING; CELL LINE; ETHYL METHANESULFONATE; ETHYLNITROSOUREA; GENOME; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; MOLECULAR SEQUENCE DATA; PENTOSYLTRANSFERASES; PHENOTYPE; POINT MUTATION; PROTOZOAN PROTEINS; THYMIDINE; TOXOPLASMA;

EID: 84900868097     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-15-354     Document Type: Article

References (74)

1. White NJ, Pukrittayakamee S, Hien TT, Faiz MA, Mokuolu OA, Dondorp AM. Malaria. Lancet 2013, 383:723-735.
2. Montoya JG, Liesenfeld O. Toxoplasmosis. Lancet 2004, 363:1965-1976. 10.1016/S0140-6736(04)16412-X, 15194258.
3. Kim K, Weiss LM. Toxoplasma gondii: the model apicomplexan. Int J Parasitol 2004, 34:423-432. 10.1016/j.ijpara.2003.12.009, 3086386, 15003501.
4. Pfefferkorn ER, Pfefferkorn LC. Arabinosyl nucleosides inhibit Toxoplasma gondii and allow the selection of resistant mutants. J Parasitol 1976, 62:993-999. 10.2307/3279197, 1003290.
5. Pfefferkorn ER, Pfefferkorn LC. Toxoplasma gondii: isolation and preliminary characterization of temperature-sensitive mutants. Exp Parasitol 1976, 39:365-376. 10.1016/0014-4894(76)90040-0, 1269580.
6. Pfefferkorn ER, Schwartzman JD, Kasper LH. Toxoplasma gondii: use of mutants to study the host-parasite relationship. Ciba Found Symp 1983, 99:74-91.
7. Farrell A, Thirugnanam S, Lorestani A, Dvorin JD, Eidell KP, Ferguson DJ, Anderson-White BR, Duraisingh MT, Marth GT, Gubbels MJ. A DOC2 protein identified by mutational profiling is essential for apicomplexan parasite exocytosis. Science 2012, 335:218-221. 10.1126/science.1210829, 3354045, 22246776.
8. Gubbels MJ, Lehmann M, Muthalagi M, Jerome ME, Brooks CF, Szatanek T, Flynn J, Parrot B, Radke J, Striepen B, White MW. Forward genetic analysis of the apicomplexan cell division cycle in Toxoplasma gondii. PLoS Pathog 2008, 4:e36. 10.1371/journal.ppat.0040036, 2242837, 18282098.
9. White MW, Jerome ME, Vaishnava S, Guerini M, Behnke M, Striepen B. Genetic rescue of a Toxoplasma gondii conditional cell cycle mutant. Mol Microbiol 2005, 55:1060-1071.
10. Pfefferkorn ER, Pfefferkorn LC. Toxoplasma gondii: characterization of a mutant resistant to 5-fluorodeoxyuridine. Exp Parasitol 1977, 42:44-55. 10.1016/0014-4894(77)90060-1, 140809.
11. Black MW, Arrizabalaga G, Boothroyd JC. Ionophore-resistant mutants of Toxoplasma gondii reveal host cell permeabilization as an early event in egress. Mol Cell Biol 2000, 20:9399-9408. 10.1128/MCB.20.24.9399-9408.2000, 102196, 11094090.
12. Arrizabalaga G, Ruiz F, Moreno S, Boothroyd JC. Ionophore-resistant mutant of Toxoplasma gondii reveals involvement of a sodium/hydrogen exchanger in calcium regulation. J Cell Biol 2004, 165:653-662. 10.1083/jcb.200309097, 2172388, 15173192.
13. Garrison E, Treeck M, Ehret E, Butz H, Garbuz T, Oswald BP, Settles M, Boothroyd J, Arrizabalaga G. A forward genetic screen reveals that calcium-dependent protein kinase 3 regulates egress in Toxoplasma. PLoS Pathog 2012, 8:e1003049. 10.1371/journal.ppat.1003049, 3510250, 23209419.
14. Uyetake L, Ortega-Barria E, Boothroyd JC. Isolation and characterization of a cold-sensitive attachment/invasion mutant of Toxoplasma gondii. Exp Parasitol 2001, 97:55-59. 10.1006/expr.2000.4577, 11207115.
15. Pfefferkorn ER, Pfefferkorn LC. Quantitative studies of the mutagenesis of Toxoplasma gondii. J Parasitol 1979, 65:364-370. 10.2307/3280274, 158076.
16. Sikora P, Chawade A, Larsson M, Olsson J, Olsson O. Mutagenesis as a Tool in Plant Genetics, Functional Genomics, and Breeding. Int J Plant Genomics 2011, 13.
17. Anderson P. Mutagenesis. Methods Cell Biol 1995, 48:31-58.
18. Flibotte S, Edgley ML, Chaudhry I, Taylor J, Neil SE, Rogula A, Zapf R, Hirst M, Butterfield Y, Jones SJ, Marra MA, Barstead RJ, Moerman DG. Whole-genome profiling of mutagenesis in Caenorhabditis elegans. Genetics 2010, 185:431-441. 10.1534/genetics.110.116616, 2881127, 20439774.
19. Acevedo-Arozena A, Wells S, Potter P, Kelly M, Cox RD, Brown SD. ENU mutagenesis, a way forward to understand gene function. Annu Rev Genomics Hum Genet 2008, 9:49-69. 10.1146/annurev.genom.9.081307.164224, 18949851.
20. Amsterdam A, Hopkins N. Mutagenesis strategies in zebrafish for identifying genes involved in development and disease. Trends Genet 2006, 22:473-478. 10.1016/j.tig.2006.06.011, 16844256.
21. Barbaric I, Wells S, Russ A, Dear TN. Spectrum of ENU-induced mutations in phenotype-driven and gene-driven screens in the mouse. Environ Mol Mutagen 2007, 48:124-142. 10.1002/em.20286, 17295309.
22. Greene EA, Codomo CA, Taylor NE, Henikoff JG, Till BJ, Reynolds SH, Enns LC, Burtner C, Johnson JE, Odden AR, Comai L, Henikoff S. Spectrum of chemically induced mutations from a large-scale reverse-genetic screen in Arabidopsis. Genetics 2003, 164:731-740. 1462604, 12807792.
23. Hanash SM, Boehnke M, Chu EH, Neel JV, Kuick RD. Nonrandom distribution of structural mutants in ethylnitrosourea-treated cultured human lymphoblastoid cells. Proc Natl Acad Sci U S A 1988, 85:165-169. 10.1073/pnas.85.1.165, 279504, 3422414.
24. Hillier LW, Marth GT, Quinlan AR, Dooling D, Fewell G, Barnett D, Fox P, Glasscock JI, Hickenbotham M, Huang W, Magrini VJ, Richt RJ, Sander SN, Stewart DA, Stromberg M, Tsung EF, Wylie T, Schedl T, Wilson RK, Mardis ER. Whole-genome sequencing and variant discovery in C. elegans. Nat Methods 2008, 5:183-188. 10.1038/nmeth.1179, 18204455.
25. Smith DR, Quinlan AR, Peckham HE, Makowsky K, Tao W, Woolf B, Shen L, Donahue WF, Tusneem N, Stromberg MP, Stewart DA, Zhang L, Ranade SS, Warner JB, Lee CC, Coleman BE, Zhang Z, McLaughlin SF, Malek JA, Sorenson JM, Blanchard AP, Chapman J, Hillman D, Chen F, Rokhsar DS, McKernan KJ, Jeffries TW, Marth GT, Richardson PM. Rapid whole-genome mutational profiling using next-generation sequencing technologies. Genome Res 2008, 18:1638-1642. 10.1101/gr.077776.108, 2556265, 18775913.
26. Sarin S, Prabhu S, O'Meara MM, Pe'er I, Hobert O. Caenorhabditis elegans mutant allele identification by whole-genome sequencing. Nat Methods 2008, 5:865-867. 10.1038/nmeth.1249, 2574580, 18677319.
27. Shen Y, Sarin S, Liu Y, Hobert O, Pe'er I. Comparing platforms for C. elegans mutant identification using high-throughput whole-genome sequencing. PLoS One 2008, 3:e4012. 10.1371/journal.pone.0004012, 2603312, 19107202.
28. Sarin S, Bertrand V, Bigelow H, Boyanov A, Doitsidou M, Poole RJ, Narula S, Hobert O. Analysis of multiple ethyl methanesulfonate-mutagenized Caenorhabditis elegans strains by whole-genome sequencing. Genetics 2010, 185:417-430. 10.1534/genetics.110.116319, 2881126, 20439776.
29. Zuryn S, Le Gras S, Jamet K, Jarriault S. A strategy for direct mapping and identification of mutations by whole-genome sequencing. Genetics 2010, 186:427-430. 10.1534/genetics.110.119230, 2940307, 20610404.
30. Voz ML, Coppieters W, Manfroid I, Baudhuin A, Von Berg V, Charlier C, Meyer D, Driever W, Martial JA, Peers B. Fast homozygosity mapping and identification of a zebrafish ENU-induced mutation by whole-genome sequencing. PLoS One 2012, 7:e34671. 10.1371/journal.pone.0034671, 3319596, 22496837.
31. Shiwa Y, Fukushima-Tanaka S, Kasahara K, Horiuchi T, Yoshikawa H. Whole-Genome Profiling of a Novel Mutagenesis Technique Using Proofreading-Deficient DNA Polymerase delta. Int J Evol Biol 2012, 2012:860797. 3364565, 22675654.
32. Hobert O. The impact of whole genome sequencing on model system genetics: get ready for the ride. Genetics 2010, 184:317-319. 10.1534/genetics.109.112938, 2828713, 20103786.
33. Brown KM, Suvorova ES, Farrell A, Wiley GB, Gubbels MJ, Marth GT, Gaffney PM, White M, Blader IJ. Chemical genetic screening identifies a small molecule that blocks Toxoplasma growth by inhibiting both host- and parasite-encoded kinases. PLoS Path 2014, accepted for publication.
34. Sugi T, Kobayashi K, Takamea H, Gong H, Ishiwa A. Identification of mutations in TgMAPK1 of Toxoplasma gondii conferring the resistance to 1NM-PP1. Int J Parasitol Drugs Drug Resist 2013, 3:93-101. 3862444, 24533298.
35. Coleman BI, Gubbels MJ. A genetic screen to isolate Toxoplasma gondii host cell egress mutants. J Vis Exp 2012, 60:e3807.
36. Roos DS, Donald RG, Morrissette NS, Moulton AL. Molecular tools for genetic dissection of the protozoan parasite Toxoplasma gondii. Methods Cell Biol 1994, 45:27-63.
37. Sabin AB. Toxoplasmic encephalitis in children. J Am Med Assoc 1941, 116:801-807.
38. Donald RG, Carter D, Ullman B, Roos DS. Insertional tagging, cloning, and expression of the Toxoplasma gondii hypoxanthine-xanthine-guanine phosphoribosyltransferase gene. Use as a selectable marker for stable transformation. J Biol Chem 1996, 271:14010-14019. 10.1074/jbc.271.24.14010, 8662859.
39. Dobrowolski JM, Sibley LD. Toxoplasma invasion of mammalian cells is powered by the actin cytoskeleton of the parasite. Cell 1996, 84:933-939. 10.1016/S0092-8674(00)81071-5, 8601316.
40. Teo CF, Zhou XW, Bogyo M, Carruthers VB. Cysteine protease inhibitors block Toxoplasma gondii microneme secretion and cell invasion. Antimicrob Agents Chemother 2007, 51:679-688. 10.1128/AAC.01059-06, 1797762, 17145790.
41. Gubbels MJ, Li C, Striepen B. High-throughput growth assay for Toxoplasma gondii using yellow fluorescent protein. Antimicrob Agents Chemother 2003, 47:309-316. 10.1128/AAC.47.1.309-316.2003, 149035, 12499207.
42. Eidell KP, Burke T, Gubbels MJ. Development of a screen to dissect Toxoplasma gondii egress. Mol Biochem Parasitol 2010, 171:97-103. 10.1016/j.molbiopara.2010.03.004, 20227445.
43. Carey KL, Westwood NJ, Mitchison TJ, Ward GE. A small-molecule approach to studying invasive mechanisms of Toxoplasma gondii. Proc Natl Acad Sci U S A 2004, 101:7433-7438. 10.1073/pnas.0307769101, 409936, 15123807.
44. Lee W-P, Stromberg M, Ward A, Stewart C, Garrison E, Marth GT. MOSAIK: A hash-based algorithm for accurate next-generation sequencing short-read mapping. PLoS One 2014, 9:e90581. 10.1371/journal.pone.0090581, 3944147, 24599324.
45. Marth GT, Korf I, Yandell MD, Yeh RT, Gu Z, Zakeri H, Stitziel NO, Hillier L, Kwok PY, Gish WR. A general approach to single-nucleotide polymorphism discovery. Nat Genet 1999, 23:452-456. 10.1038/70570, 10581034.
46. Garrison E, Marth GT. Haplotype-Based Variant Detection from Short-Read Sequencing 2012, http://arxiv.org/abs/1207.3907v2.
47. Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA. Circos: an information aesthetic for comparative genomics. Genome Res 2009, 19:1639-1645. 10.1101/gr.092759.109, 2752132, 19541911.
48. Gajria B, Bahl A, Brestelli J, Dommer J, Fischer S, Gao X, Heiges M, Iodice J, Kissinger JC, Mackey AJ, Pinney DF, Roos DS, Stoeckert CJ, Wang H, Brunk BP. ToxoDB: an integrated Toxoplasma gondii database resource. Nucleic Acids Res 2008, 36:D553-D556. 2238934, 18003657.
49. Sibley LD, Boothroyd JC. Virulent strains of Toxoplasma gondii comprise a single clonal lineage. Nature 1992, 359:82-85. 10.1038/359082a0, 1355855.
50. Martinelli A, Henriques G, Cravo P, Hunt P. Whole genome re-sequencing identifies a mutation in an ABC transporter (mdr2) in a Plasmodium chabaudi clone with altered susceptibility to antifolate drugs. Int J Parasitol 2010, 41:165-171. 3034870, 20858498.
51. Araya CL, Payen C, Dunham MJ, Fields S. Whole-genome sequencing of a laboratory-evolved yeast strain. BMC Genomics 2010, 11:88. 10.1186/1471-2164-11-88, 2829512, 20128923.
52. Le Crom S, Schackwitz W, Pennacchio L, Magnuson JK, Culley DE, Collett JR, Martin J, Druzhinina IS, Mathis H, Monot F, Seiboth B, Cherry B, Rey M, Berka R, Kubicek CP, Baker SE, Margeot A. Tracking the roots of cellulase hyperproduction by the fungus Trichoderma reesei using massively parallel DNA sequencing. Proc Natl Acad Sci U S A 2009, 106:16151-16156. 10.1073/pnas.0905848106, 2752593, 19805272.
53. Yang Z, Yoder AD. Estimation of the transition/transversion rate bias and species sampling. J Mol Evol 1999, 48:274-283. 10.1007/PL00006470, 10093216.
54. Zhang J. Rates of conservative and radical nonsynonymous nucleotide substitutions in mammalian nuclear genes. J Mol Evol 2000, 50:56-68.
55. Khan A, Taylor S, Su C, Sibley LD, Paulsen I, Ajioka JW. Genetics and Genome Organization of Toxoplasma Gondii 2007, Norwich, UK: Horizon Scientific Press.
56. Pfefferkorn ER. Toxoplasma gondii: the enzymic defect of a mutant resistant to 5-fluorodeoxyuridine. Exp Parasitol 1978, 44:26-35. 10.1016/0014-4894(78)90077-2, 146608.
57. Schwartzman JD, Pfefferkorn ER. Pyrimidine synthesis by intracellular Toxoplasma gondii. J Parasitol 1981, 67:150-158. 10.2307/3280627, 7241272.
58. Donald RG, Roos DS. Insertional mutagenesis and marker rescue in a protozoan parasite: cloning of the uracil phosphoribosyltransferase locus from Toxoplasma gondii. Proc Natl Acad Sci U S A 1995, 92:5749-5753. 10.1073/pnas.92.12.5749, 41774, 7777580.
59. Goecks J, Eberhard C, Too T, Nekrutenko A, Taylor J. Web-based visual analysis for high-throughput genomics. BMC Genomics 2013, 14:397. 10.1186/1471-2164-14-397, 3691752, 23758618.
60. Sun YV, Levin AM, Boerwinkle E, Robertson H, Kardia SL. A scan statistic for identifying chromosomal patterns of SNP association. Genet Epidemiol 2006, 30:627-635. 10.1002/gepi.20173, 16858698.
61. Yang N, Farrell A, Niedelman W, Melo M, Lu D, Julien L, Marth GT, Gubbels MJ, Saeij JP. Genetic basis for phenotypic differences between different Toxoplasma gondii type I strains. BMC Genomics 2013, 14:467. 10.1186/1471-2164-14-467, 3710486, 23837824.
62. Martincorena I, Seshasayee AS, Luscombe NM. Evidence of non-random mutation rates suggests an evolutionary risk management strategy. Nature 2012, 485:95-98. 10.1038/nature10995, 22522932.
63. Fox BA, Ristuccia JG, Gigley JP, Bzik DJ. Efficient gene replacements in Toxoplasma gondii strains deficient for nonhomologous end-joining. Eukaryot Cell 2009, 8:520-529. 10.1128/EC.00357-08, 2669201, 19218423.
64. Nordstrom KJ, Albani MC, James GV, Gutjahr C, Hartwig B, Turck F, Paszkowski U, Coupland G, Schneeberger K. Mutation identification by direct comparison of whole-genome sequencing data from mutant and wild-type individuals using k-mers. Nat Biotechnol 2013, 31:325-330. 10.1038/nbt.2515, 23475072.
65. Kohler S, Delwiche CF, Denny PW, Tilney LG, Webster P, Wilson RJ, Palmer JD, Roos DS. A plastid of probable green algal origin in Apicomplexan parasites. Science 1997, 275:1485-1489. 10.1126/science.275.5305.1485, 9045615.
66. Reiff SB, Vaishnava S, Striepen B. The HU protein is important for apicoplast genome maintenance and inheritance in Toxoplasma gondii. Eukaryot Cell 2012, 11:905-915. 10.1128/EC.00029-12, 3416497, 22611021.
67. Matsuzaki M, Kikuchi T, Kita K, Kojima S, Kuroiwa T. Large amounts of apicoplast nucleoid DNA and its segregation in Toxoplasma gondii. Protoplasma 2001, 218:180-191. 10.1007/BF01306607, 11770434.
68. Pastink A, Heemskerk E, Nivard MJ, Van Vliet CJ, Vogel EW. Mutational specificity of ethyl methanesulfonate in excision-repair-proficient and -deficient strains of Drosophila melanogaster. Mol Gen Genet 1991, 229:213-218. 10.1007/BF00272158, 1921971.
69. Klungland A, Laake K, Hoff E, Seeberg E. Spectrum of mutations induced by methyl and ethyl methanesulfonate at the hprt locus of normal and tag expressing Chinese hamster fibroblasts. Carcinogenesis 1995, 16:1281-1285. 10.1093/carcin/16.6.1281, 7788844.
70. Onyango DO, Naguleswaran A, Delaplane S, Reed A, Kelley MR, Georgiadis MM, Sullivan WJ. Base excision repair apurinic/apyrimidinic endonucleases in apicomplexan parasite Toxoplasma gondii. DNA Repair 2011, 10:466-475. 10.1016/j.dnarep.2011.01.011, 3084321, 21353648.
71. Quwailid MM, Hugill A, Dear N, Vizor L, Wells S, Horner E, Fuller S, Weedon J, McMath H, Woodman P, Edwards D, Campbell D, Rodger S, Carey J, Roberts A, Glenister P, Lalanne Z, Parkinson N, Coghill EL, McKeone R, Cox S, Willan J, Greenfield A, Keays D, Brady S, Spurr N, Gray I, Hunter J, Brown SD, Cox RD. A gene-driven ENU-based approach to generating an allelic series in any gene. Mamm Genome 2004, 15:585-591. 10.1007/s00335-004-2379-z, 15457338.
72. Timmermann B, Jarolim S, Russmayer H, Kerick M, Michel S, Kruger A, Bluemlein K, Laun P, Grillari J, Lehrach H, Breitenbach M, Ralser M. A new dominant peroxiredoxin allele identified by whole-genome re-sequencing of random mutagenized yeast causes oxidant-resistance and premature aging. Aging (Albany NY) 2010, 2:475-486. 2954039, 20729566.
73. Schumacher MA, Carter D, Scott DM, Roos DS, Ullman B, Brennan RG. Crystal structures of Toxoplasma gondii uracil phosphoribosyltransferase reveal the atomic basis of pyrimidine discrimination and prodrug binding. EMBO J 1998, 17:3219-3232. 10.1093/emboj/17.12.3219, 1170660, 9628859.
74. Longley DB, Harkin DP, Johnston PG. 5-fluorouracil: mechanisms of action and clinical strategies. Nat Rev Cancer 2003, 3:330-338. 10.1038/nrc1074, 12724731.