Genome-wide variations in a natural isolate of the nematode Caenorhabditis elegans

BMC Genomics

Volumn 15, Issue 1, 2014, Pages

  Vergara, Ismael A ^a   Tarailo Graovac, Maja ^a   Frech, Christian ^a   Wang, Jun ^a   Qin, Zhaozhao ^a   Zhang, Ting ^a   She, Rong ^a   Chu, Jeffrey S C ^a   Wang, Ke ^a   Chen, Nansheng ^a  

^a SIMON FRASER UNIVERSITY   (Canada)

Author keywords

C. elegans; Compound variation; Genomic variation; Large insertion; Loss of function; Natural isolate strain; Next generation DNA sequencing

Indexed keywords

ARTICLE; CAENORHABDITIS ELEGANS; CODON; DNA SEQUENCE; GENE DELETION; GENE IDENTIFICATION; GENE INSERTION; GENE LOCATION; GENETIC CODE; GENETIC DIFFERENCE; GENETIC DISTANCE; GENETIC VARIABILITY; GENOME ANALYSIS; LOSS OF FUNCTION MUTATION; NONHUMAN; OPEN READING FRAME; PHENOTYPE; RNA INTERFERENCE;

CAENORHABDITIS ELEGANS;

ANIMALS; BASE COMPOSITION; CAENORHABDITIS ELEGANS; CHROMOSOME MAPPING; CODON; COMPARATIVE GENOMIC HYBRIDIZATION; COMPUTATIONAL BIOLOGY; DNA TRANSPOSABLE ELEMENTS; DRUG RESISTANCE; GENETIC ASSOCIATION STUDIES; GENETIC VARIATION; GENOME, HELMINTH; GENOTYPE; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; INDEL MUTATION; MULTIGENE FAMILY; MUTAGENESIS, INSERTIONAL; OPEN READING FRAMES; PHENOTYPE; POLYMORPHISM, SINGLE NUCLEOTIDE; SEQUENCE DELETION;

EID: 84897568721     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-15-255     Document Type: Article

References (90)

1. Link CD. C. elegans models of age-associated neurodegenerative diseases: lessons from transgenic worm models of Alzheimer's disease. Exp Gerontol 2006, 41:1007-1013. 10.1016/j.exger.2006.06.059, 16930903.
2. Poulin G, Nandakumar R, Ahringer J. Genome-wide RNAi screens in Caenorhabditis elegans: impact on cancer research. Oncogene 2004, 23:8340-8345. 10.1038/sj.onc.1208010, 15517014.
3. C. elegans Genome Sequencing Consortium Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 1998, 282:2012-2018. C. elegans Genome Sequencing Consortium.
4. Riddle DL, Blumenthal T, Meyer BJ, Priess JR. Introduction to C. Elegans - Origins of the Model. C Elegans II 1997,
5. Kiontke K, Sudhaus W. Ecology of Caenorhabditis species. WormBook 2006, 1-14.
6. Barriere A, Felix MA. Natural variation and population genetics of Caenorhabditis elegans. WormBook 2005, 1-19.
7. Kammenga JE, Phillips PC, De Bono M, Doroszuk A. Beyond induced mutants: using worms to study natural variation in genetic pathways. Trends Genet 2008, 24:178-185. 10.1016/j.tig.2008.01.001, 18325626.
8. Barriere A, Felix MA. High local genetic diversity and low outcrossing rate in Caenorhabditis elegans natural populations. Curr Biol 2005, 15:1176-1184. 10.1016/j.cub.2005.06.022, 16005289.
9. Haber M, Schungel M, Putz A, Muller S, Hasert B, Schulenburg H. Evolutionary history of Caenorhabditis elegans inferred from microsatellites: evidence for spatial and temporal genetic differentiation and the occurrence of outbreeding. Mol Biol Evol 2005, 22:160-173.
10. Sivasundar A, Hey J. Sampling from natural populations with RNAI reveals high outcrossing and population structure in Caenorhabditis elegans. Curr Biol 2005, 15:1598-1602. 10.1016/j.cub.2005.08.034, 16139217.
11. Sivasundar A, Hey J. Population genetics of Caenorhabditis elegans: the paradox of low polymorphism in a widespread species. Genetics 2003, 163:147-157. 1462423, 12586703.
12. Graustein A, Gaspar JM, Walters JR, Palopoli MF. Levels of DNA polymorphism vary with mating system in the nematode genus caenorhabditis. Genetics 2002, 161:99-107. 1462083, 12019226.
13. Barriere A, Felix MA. Temporal dynamics and linkage disequilibrium in natural Caenorhabditis elegans populations. Genetics 2007, 176:999-1011. 1894625, 17409084.
14. Cutter AD. Molecular evolution inferences from the C. elegans genome. WormBook 2010, 1-14.
15. Koch R, van Luenen HG, van der Horst M, Thijssen KL, Plasterk RH. Single nucleotide polymorphisms in wild isolates of Caenorhabditis elegans. Genome Res 2000, 10:1690-1696. 10.1101/gr.GR-1471R, 310957, 11076854.
16. Andersen EC, Gerke JP, Shapiro JA, Crissman JR, Ghosh R, Bloom JS, Felix MA, Kruglyak L. Chromosome-scale selective sweeps shape Caenorhabditis elegans genomic diversity. Nat Genet 2012, 44:285-290. 10.1038/ng.1050, 3365839, 22286215.
17. Hodgkin J, Doniach T. Natural variation and copulatory plug formation in Caenorhabditis elegans. Genetics 1997, 146:149-164. 1207933, 9136008.
18. Solorzano E, Okamoto K, Datla P, Sung W, Bergeron RD, Thomas WK. Shifting patterns of natural variation in the nuclear genome of caenorhabditis elegans. BMC Evol Biol 2011, 11:168. 10.1186/1471-2148-11-168, 3151237, 21679441.
19. Volkers RJ, Snoek LB, Hubar CJ, Coopman R, Chen W, Yang W, Sterken MG, Schulenburg H, Braeckman BP, Kammenga JE. Gene-environment and protein-degradation signatures characterize genomic and phenotypic diversity in wild Caenorhabditis elegans populations. BMC Biol 2013, 11:93. 10.1186/1741-7007-11-93, 3846632, 23957880.
20. Swan KA, Curtis DE, McKusick KB, Voinov AV, Mapa FA, Cancilla MR. High-throughput gene mapping in Caenorhabditis elegans. Genome Res 2002, 12:1100-1105. 186621, 12097347.
21. Wicks SR, Yeh RT, Gish WR, Waterston RH, Plasterk RH. Rapid gene mapping in Caenorhabditis elegans using a high density polymorphism map. Nat Genet 2001, 28:160-164. 10.1038/88878, 11381264.
22. Minevich G, Park DS, Blankenberg D, Poole RJ, Hobert O. CloudMap: a cloud-based pipeline for analysis of mutant genome sequences. Genetics 2012, 192:1249-1269. 10.1534/genetics.112.144204, 3512137, 23051646.
23. Flibotte S, Edgley ML, Maydan J, Taylor J, Zapf R, Waterston R, Moerman DG. Rapid high resolution single nucleotide polymorphism-comparative genome hybridization mapping in Caenorhabditis elegans. Genetics 2009, 181:33-37. 2621182, 18957702.
24. Johnson TE, Wood WB. Genetic analysis of life-span in Caenorhabditis elegans. Proc Natl Acad Sci USA 1982, 79:6603-6607. 10.1073/pnas.79.21.6603, 347176, 6959141.
25. Li Y, Alvarez OA, Gutteling EW, Tijsterman M, Fu J, Riksen JA, Hazendonk E, Prins P, Plasterk RH, Jansen RC, Breitling R, Kammenga JE. Mapping determinants of gene expression plasticity by genetical genomics in C. elegans. PLoS Genet 2006, 2:e222. 10.1371/journal.pgen.0020222, 1756913, 17196041.
26. Seidel HS, Rockman MV, Kruglyak L. Widespread genetic incompatibility in C. elegans maintained by balancing selection. Science 2008, 319:589-594. 10.1126/science.1151107, 2421010, 18187622.
27. Doroszuk A, Snoek LB, Fradin E, Riksen J, Kammenga J. A genome-wide library of CB4856/N2 introgression lines of Caenorhabditis elegans. Nucleic Acids Res 2009, 37:e110. 10.1093/nar/gkp528, 2760803, 19542186.
28. Palopoli MF, Rockman MV, TinMaung A, Ramsay C, Curwen S, Aduna A, Laurita J, Kruglyak L. Molecular basis of the copulatory plug polymorphism in Caenorhabditis elegans. Nature 2008, 454:1019-1022. 10.1038/nature07171, 2597896, 18633349.
29. McGrath PT, Rockman MV, Zimmer M, Jang H, Macosko EZ, Kruglyak L, Bargmann CI. Quantitative mapping of a digenic behavioral trait implicates globin variation in C. elegans sensory behaviors. Neuron 2009, 61:692-699. 10.1016/j.neuron.2009.02.012, 2772867, 19285466.
30. Persson A, Gross E, Laurent P, Busch KE, Bretes H, de Bono M. Natural variation in a neural globin tunes oxygen sensing in wild Caenorhabditis elegans. Nature 2009, 458:1030-1033. 10.1038/nature07820, 19262507.
31. Hallem EA, Sternberg PW. Acute carbon dioxide avoidance in Caenorhabditis elegans. Proc Natl Acad Sci USA 2008, 105:8038-8043. 10.1073/pnas.0707469105, 2430355, 18524955.
32. Kammenga JE, Doroszuk A, Riksen JA, Hazendonk E, Spiridon L, Petrescu AJ, Tijsterman M, Plasterk RH, Bakker J. A Caenorhabditis elegans wild type defies the temperature-size rule owing to a single nucleotide polymorphism in tra-3. PLoS Genet 2007, 3:e34. 10.1371/journal.pgen.0030034, 1808073, 17335351.
33. Tijsterman M, Okihara KL, Thijssen K, Plasterk RH. PPW-1, a PAZ/PIWI protein required for efficient germline RNAi, is defective in a natural isolate of C. elegans. Curr Biol 2002, 12:1535-1540. 10.1016/S0960-9822(02)01110-7, 12225671.
34. Atkinson-Leadbeater K, Nuttley WM, van der Kooy D. A genetic dissociation of learning and recall in Caenorhabditis elegans. Behav Neurosci 2004, 118:1206-1213.
35. Jurado P, Kodama E, Tanizawa Y, Mori I. Distinct thermal migration behaviors in response to different thermal gradients in Caenorhabditis elegans. Genes Brain Behav 2010, 9:120-127. 10.1111/j.1601-183X.2009.00549.x, 20002199.
36. Reddy KC, Andersen EC, Kruglyak L, Kim DH. A polymorphism in npr-1 is a behavioral determinant of pathogen susceptibility in C. elegans. Science 2009, 323:382-384. 10.1126/science.1166527, 2748219, 19150845.
37. Darby C, Chakraborti A, Politz SM, Daniels CC, Tan L, Drace K. Caenorhabditis elegans mutants resistant to attachment of Yersinia biofilms. Genetics 2007, 176:221-230. 10.1534/genetics.106.067496, 1893055, 17339204.
38. de Bono M, Bargmann CI. Natural variation in a Neuropeptide Y receptor homolog modifies social behavior and food response in C. elegans. Cell 1998, 94:679-689. 10.1016/S0092-8674(00)81609-8, 9741632.
39. Gloria-Soria A, Azevedo RB. npr-1 Regulates foraging and dispersal strategies in Caenorhabditis elegans. Curr Biol 2008, 18:1694-1699. 10.1016/j.cub.2008.09.043, 18993077.
40. 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.
41. Weber KP, De S, Kozarewa I, Turner DJ, Babu MM, de Bono M. Whole genome sequencing highlights genetic changes associated with laboratory domestication of C. elegans. PLoS One 2010, 5:e13922. 10.1371/journal.pone.0013922, 2978686, 21085631.
42. 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.
43. Rose AM, O'Neil NJ, Bilenky M, Butterfield YS, Malhis N, Flibotte S, Jones MR, Marra M, Baillie DL, Jones SJ. Genomic sequence of a mutant strain of Caenorhabditis elegans with an altered recombination pattern. BMC Genomics 2010, 11:131. 10.1186/1471-2164-11-131, 2837035, 20178641.
44. 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.
45. 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.
46. Denver DR, Dolan PC, Wilhelm LJ, Sung W, Lucas-Lledo JI, Howe DK, Lewis SC, Okamoto K, Thomas WK, Lynch M, Baer CF. A genome-wide view of Caenorhabditis elegans base-substitution mutation processes. Proc Natl Acad Sci USA 2009, 106:16310-16314. 10.1073/pnas.0904895106, 2752564, 19805298.
47. Denver DR, Howe DK, Wilhelm LJ, Palmer CA, Anderson JL, Stein KC, Phillips PC, Estes S. Selective sweeps and parallel mutation in the adaptive recovery from deleterious mutation in Caenorhabditis elegans. Genome Res 2010, 20:1663-1671. 10.1101/gr.108191.110, 2989992, 21036923.
48. Maydan JS, Flibotte S, Edgley ML, Lau J, Selzer RR, Richmond TA, Pofahl NJ, Thomas JH, Moerman DG. Efficient high-resolution deletion discovery in Caenorhabditis elegans by array comparative genomic hybridization. Genome Res 2007, 17:337-347. 10.1101/gr.5690307, 1800925, 17267812.
49. Maydan JS, Lorch A, Edgley ML, Flibotte S, Moerman DG. Copy number variation in the genomes of twelve natural isolates of Caenorhabditis elegans. BMC Genomics 2010, 11:62. 10.1186/1471-2164-11-62, 2822765, 20100350.
50. Denver DR, Morris K, Thomas WK. Phylogenetics in Caenorhabditis elegans: an analysis of divergence and outcrossing. Mol Biol Evol 2003, 20:393-400. 10.1093/molbev/msg044, 12644560.
51. Chen N, Harris TW, Antoshechkin I, Bastiani C, Bieri T, Blasiar D, Bradnam K, Canaran P, Chan J, Chen CK, Chen WJ, Cunningham F, Davis P, Kenny E, Kishore R, Lawson D, Lee R, Muller HM, Nakamura C, Pai S, Ozersky P, Petcherski A, Rogers A, Sabo A, Schwarz EM, Van Auken K, Wang Q, Durbin R, Spieth J, Sternberg PW, Stein LD. WormBase: a comprehensive data resource for Caenorhabditis biology and genomics. Nucleic Acids Res 2005, 33:D383-D389. 540020, 15608221.
52. Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, Bemben LA, Berka J, Braverman MS, Chen YJ, Chen Z, Dewell SB, Du L, Fierro JM, Gomes XV, Godwin BC, He W, Helgesen S, Ho CH, Irzyk GP, Jando SC, Alenquer ML, Jarvie TP, Jirage KB, Kim JB, Knight JR, Lanza JR, Leamon JH, Lefkowitz SM, Lei M, Li J, et al. Genome sequencing in microfabricated high-density picolitre reactors. Nature 2005, 437:376-380. 1464427, 16056220.
53. Ning Z, Cox AJ, Mullikin JC. SSAHA: a fast search method for large DNA databases. Genome Res 2001, 11:1725-1729. 10.1101/gr.194201, 311141, 11591649.
54. Koboldt DC, Chen K, Wylie T, Larson DE, McLellan MD, Mardis ER, Weinstock GM, Wilson RK, Ding L. VarScan: variant detection in massively parallel sequencing of individual and pooled samples. Bioinformatics 2009, 25:2283-2285. 10.1093/bioinformatics/btp373, 2734323, 19542151.
55. Collins DW, Jukes TH. Rates of transition and transversion in coding sequences since the human-rodent divergence. Genomics 1994, 20:386-396. 10.1006/geno.1994.1192, 8034311.
56. Wheeler DA, Srinivasan M, Egholm M, Shen Y, Chen L, McGuire A, He W, Chen YJ, Makhijani V, Roth GT, Gomes X, Tartaro K, Niazi F, Turcotte CL, Irzyk GP, Lupski JR, Chinault C, Song XZ, Liu Y, Yuan Y, Nazareth L, Qin X, Muzny DM, Margulies M, Weinstock GM, Gibbs RA, Rothberg JM. The complete genome of an individual by massively parallel DNA sequencing. Nature 2008, 452:872-876. 10.1038/nature06884, 18421352.
57. 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.
58. Coghlan A, Wolfe KH. Fourfold faster rate of genome rearrangement in nematodes than in Drosophila. Genome Res 2002, 12:857-867. 10.1101/gr.172702, 1383740, 12045140.
59. Hillier LW, Miller RD, Baird SE, Chinwalla A, Fulton LA, Koboldt DC, Waterston RH. Comparison of C. elegans and C. briggsae genome sequences reveals extensive conservation of chromosome organization and synteny. PLoS Biol 2007, 5:e167. 10.1371/journal.pbio.0050167, 1914384, 17608563.
60. Stein LD, Bao Z, Blasiar D, Blumenthal T, Brent MR, Chen N, Chinwalla A, Clarke L, Clee C, Coghlan A, Coulson A, D'Eustachio P, Fitch DH, Fulton LA, Fulton RE, Griffiths-Jones S, Harris TW, Hillier LW, Kamath R, Kuwabara PE, Mardis ER, Marra MA, Miner TL, Minx P, Mullikin JC, Plumb RW, Rogers J, Schein JE, Sohrmann M, Spieth J, et al. The genome sequence of Caenorhabditis briggsae: a platform for comparative genomics. PLoS Biol 2003, 1:E45. 261899, 14624247.
61. Vergara IA, Chen N. Large synteny blocks revealed between Caenorhabditis elegans and Caenorhabditis briggsae genomes using OrthoCluster. BMC Genomics 2010, 11:516. 10.1186/1471-2164-11-516, 2997010, 20868500.
62. Stewart MK, Clark NL, Merrihew G, Galloway EM, Thomas JH. High genetic diversity in the chemoreceptor superfamily of Caenorhabditis elegans. Genetics 2005, 169:1985-1996. 10.1534/genetics.104.035329, 1449585, 15520260.
63. Chen N, Pai S, Zhao Z, Mah A, Newbury R, Johnsen RC, Altun Z, Moerman DG, Baillie DL, Stein LD. Identification of a nematode chemosensory gene family. Proc Natl Acad Sci USA 2005, 102:146-151. 10.1073/pnas.0408307102, 539308, 15618405.
64. Frech C, Chen N. Genome-wide comparative gene family classification. PLoS One 2010, 5:e13409. 10.1371/journal.pone.0013409, 2955529, 20976221.
65. Thomas JH, Robertson HM. The Caenorhabditis chemoreceptor gene families. BMC Biol 2008, 6:42. 10.1186/1741-7007-6-42, 2576165, 18837995.
66. Grantham R. Amino acid difference formula to help explain protein evolution. Science 1974, 185:862-864. 10.1126/science.185.4154.862, 4843792.
67. Li WH, Wu CI, Luo CC. Nonrandomness of point mutation as reflected in nucleotide substitutions in pseudogenes and its evolutionary implications. J Mol Evol 1984, 21:58-71. 10.1007/BF02100628, 6442359.
68. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25:3389-3402. 10.1093/nar/25.17.3389, 146917, 9254694.
69. Jurka J. Repbase update: a database and an electronic journal of repetitive elements. Trends Genet 2000, 16:418-420. 10.1016/S0168-9525(00)02093-X, 10973072.
70. Vergara IA, Frech C, Chen N. CooVar: co-occurring variant analyzer. BMC Res Notes 2012, 5:615. 10.1186/1756-0500-5-615, 3532326, 23116482.
71. Bruinsma JJ, Schneider DL, Davis DE, Kornfeld K. Identification of mutations in Caenorhabditis elegans that cause resistance to high levels of dietary zinc and analysis using a genomewide map of single nucleotide polymorphisms scored by pyrosequencing. Genetics 2008, 179:811-828. 10.1534/genetics.107.084384, 2429876, 18505880.
72. Denver DR, Morris K, Kewalramani A, Harris KE, Chow A, Estes S, Lynch M, Thomas WK. Abundance, distribution, and mutation rates of homopolymeric nucleotide runs in the genome of Caenorhabditis elegans. J Mol Evol 2004, 58:584-595. 10.1007/s00239-004-2580-4, 15170261.
73. Barnes TM, Kohara Y, Coulson A, Hekimi S. Meiotic recombination, noncoding DNA and genomic organization in Caenorhabditis elegans. Genetics 1995, 141:159-179. 1206715, 8536965.
74. Fraser AG, Kamath RS, Zipperlen P, Martinez-Campos M, Sohrmann M, Ahringer J. Functional genomic analysis of C. elegans chromosome I by systematic RNA interference. Nature 2000, 408:325-330. 10.1038/35042517, 11099033.
75. Maeda I, Kohara Y, Yamamoto M, Sugimoto A. Large-scale analysis of gene function in Caenorhabditis elegans by high-throughput RNAi. Curr Biol 2001, 11:171-176. 10.1016/S0960-9822(01)00052-5, 11231151.
76. Vergara IA, Mah AK, Huang JC, Tarailo-Graovac M, Johnsen RC, Baillie DL, Chen N. Polymorphic segmental duplication in the nematode Caenorhabditis elegans. BMC Genomics 2009, 10:329. 10.1186/1471-2164-10-329, 2728738, 19622155.
77. Ceron J, Rual JF, Chandra A, Dupuy D, Vidal M, van den Heuvel S. Large-scale RNAi screens identify novel genes that interact with the C. elegans retinoblastoma pathway as well as splicing-related components with synMuv B activity. BMC Dev Biol 2007, 7:30. 10.1186/1471-213X-7-30, 1863419, 17417969.
78. Kamath RS, Fraser AG, Dong Y, Poulin G, Durbin R, Gotta M, Kanapin A, Le Bot N, Moreno S, Sohrmann M, Welchman DP, Zipperlen P, Ahringer J. Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 2003, 421:231-237. 10.1038/nature01278, 12529635.
79. Rual JF, Ceron J, Koreth J, Hao T, Nicot AS, Hirozane-Kishikawa T, Vandenhaute J, Orkin SH, Hill DE, van den Heuvel S, Vidal M. Toward improving Caenorhabditis elegans phenome mapping with an ORFeome-based RNAi library. Genome Res 2004, 14:2162-2168. 10.1101/gr.2505604, 528933, 15489339.
80. Simmer F, Moorman C, van der Linden AM, Kuijk E, van den Berghe PV, Kamath RS, Fraser AG, Ahringer J, Plasterk RH. Genome-wide RNAi of C. elegans using the hypersensitive rrf-3 strain reveals novel gene functions. PLoS Biol 2003, 1:E12. 212692, 14551910.
81. Bendesky A, Tsunozaki M, Rockman MV, Kruglya L, Bargmann CI. Catecholamine receptor polymorphisms affect decision-making in C. elegans. Nature 2011, 472:313-318. 10.1038/nature09821, 3154120, 21412235.
82. Yamada K, Hirotsu T, Matsuki M, Kunitomo H, Iino Y. GPC-1, a G protein gamma-subunit, regulates olfactory adaptation in Caenorhabditis elegans. Genetics 2009, 181:1347-1357. 10.1534/genetics.108.099002, 2666504, 19189947.
83. MacArthur DG, Tyler-Smith C. Loss-of-function variants in the genomes of healthy humans. Hum Mol Genet 2010, 19:R125-R130. 10.1093/hmg/ddq365, 2953739, 20805107.
84. Piano F, Schetter AJ, Morton DG, Gunsalus KC, Reinke V, Kim SK, Kemphues KJ. Gene clustering based on RNAi phenotypes of ovary-enriched genes in C. elegans. Curr Biol 2002, 12:1959-1964. 10.1016/S0960-9822(02)01301-5, 12445391.
85. Waters K, Yang AZ, Reinke V. Genome-wide analysis of germ cell proliferation in C.elegans identifies VRK-1 as a key regulator of CEP-1/p53. Dev Biol 2010, 344:1011-1025. 10.1016/j.ydbio.2010.06.022, 3375680, 20599896.
86. Sonnichsen B, Koski LB, Walsh A, Marschall P, Neumann B, Brehm M, Alleaume AM, Artelt J, Bettencourt P, Cassin E, Hewitson M, Holz C, Khan M, Lazik S, Martin C, Nitzsche B, Ruer M, Stamford J, Winzi M, Heinkel R, Röder M, Finell J, Häntsch H, Jones SJ, Jones M, Piano F, Gunsalus KC, Oegema K, Gönczy P, Coulson A, et al. Full-genome RNAi profiling of early embryogenesis in Caenorhabditis elegans. Nature 2005, 434:462-469. 10.1038/nature03353, 15791247.
87. Croce A, Cassata G, Disanza A, Gagliani MC, Tacchetti C, Malabarba MG, Carlier MF, Scita G, Baumeister R, Di Fiore PP. A novel actin barbed-end-capping activity in EPS-8 regulates apical morphogenesis in intestinal cells of Caenorhabditis elegans. Nat Cell Biol 2004, 6:1173-1179. 10.1038/ncb1198, 15558032.
88. She R, Chu JS, Wang K, Pei J, Chen N. GenBlastA: enabling BLAST to identify homologous gene sequences. Genome Res 2009, 19:143-149. 2612959, 18838612.
89. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994, 22:4673-4680. 10.1093/nar/22.22.4673, 308517, 7984417.
90. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R. The Sequence Alignment/Map format and SAMtools. Bioinformatics 2009, 25:2078-2079. 10.1093/bioinformatics/btp352, 2723002, 19505943.