Using next-generation sequencing to isolate mutant genes from forward genetic screens

Nature Reviews Genetics

Volumn 15, Issue 10, 2014, Pages 662-676

  Schneeberger, Korbinian ^a  

^a MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS THALIANA; CAENORHABDITIS ELEGANS; GENE EXPRESSION; GENE FREQUENCY; GENE MAPPING; GENE MUTATION; GENETIC CROSS; GENETIC DIFFERENCE; GENETIC LINKAGE; GENETIC SCREENING; GENETIC VARIABILITY; HOMOZYGOSITY; MUTAGENESIS; NEUROSPORA CRASSA; NEXT GENERATION SEQUENCING; NONHUMAN; PRIORITY JOURNAL; REVIEW; SACCHAROMYCES CEREVISIAE; SINGLE NUCLEOTIDE POLYMORPHISM; SPONTANEOUS MUTATION; ANIMAL; CHROMOSOME MAP; GENETIC ASSOCIATION; HIGH THROUGHPUT SEQUENCING; HUMAN; MUTATION; NUCLEOTIDE SEQUENCE; PROCEDURES; TRENDS;

ANIMALS; CHROMOSOME MAPPING; DNA MUTATIONAL ANALYSIS; GENETIC LINKAGE; GENETIC TESTING; GENOME-WIDE ASSOCIATION STUDY; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; MUTATION;

EID: 84922264677     PISSN: 14710056     EISSN: 14710064     Source Type: Journal    
DOI: 10.1038/nrg3745     Document Type: Review

References (120)

1. Patton, E. E. & Zon, L. I. The art and design of genetic screens: zebrafish. Nature Rev. Genet. 2, 956-966 (2001
2. Forsburg, S. L. The art and design of genetic screens: yeast. Nature Rev. Genet. 2, 659-668 (2001
3. Casselton, L. & Zolan, M. The art and design of genetic screens: filamentous fungi. Nature Rev. Genet. 3, 683-697 (2002
4. Jorgensen, E. M. & Mango, S. E. The art and design of genetic screens: Caenorhabditis elegans. Nature Rev. Genet. 3, 356-369 (2002
5. St Johnston, D. The art and design of genetic screens: Drosophila melanogaster. Nature Rev. Genet. 3, 176-188 (2002
6. Page, D. R. & Grossniklaus, U. The art and design of genetic screens: Arabidopsis thaliana. Nature Rev. Genet. 3, 124-136 (2002
7. Shuman, H. A. & Silhavy, T. J. The art and design of genetic screens: Escherichia coli. Nature Rev. Genet. 4, 419-431 (2003
8. Kile, B. T. & Hilton, D. J. The art and design of genetic screens: mouse. Nature Rev. Genet. 6, 557-567 (2005
9. Candela, H. & Hake, S. The art and design of genetic screens: maize. Nature Rev. Genet. 9, 192-203 (2008
10. Michelmore, R. W., Paran, I. & Kesseli, R. V. Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. Proc. Natl Acad. Sci. USA 88, 9828-9832 (1991
11. Darvasi, A. & Soller, M. Selective DNA pooling for determination of linkage between a molecular marker and a quantitative trait locus. Genetics 138, 1365-1373 (1994
12. Winzeler, E. A. et al. Direct allelic variation scanning of the yeast genome. Science 281, 1194-1197 (1998
13. Lindblad-Toh, K. et al. Large-scale discovery and genotyping of single-nucleotide polymorphisms in the mouse. Nature Genet. 24, 381-386 (2000
14. Wicks, S. R., Yeh, R. T., Gish, W. R., Waterston, R. H. & Plasterk, R. H. Rapid gene mapping in Caenorhabditis elegans using a high density polymorphism map. Nature Genet. 28, 160-164 (2001
15. Stickney, H. L. et al. Rapid mapping of zebrafish mutations with SNPs and oligonucleotide microarrays. Genome Res. 12, 1929-1934 (2002
16. Borevitz, J. O. et al. Large-scale identification of single-feature polymorphisms in complex genomes. Genome Res. 13, 513-523 (2003
17. Hazen, S. P. et al. Rapid array mapping of circadian clock and developmental mutations in Arabidopsis. Plant Physiol. 138, 990-997 (2005
18. Brauer, M. J., Christianson, C. M., Pai, D. A. & Dunham, M. J. Mapping novel traits by array-Assisted bulk segregant analysis in Saccharomyces cerevisiae. Genetics 173, 1813-1816 (2006
19. Lai, C. Q. et al. Speed-mapping quantitative trait loci using microarrays. Nature Methods 4, 839-841 (2007
20. Liu, S. et al. High-Throughput genetic mapping of mutants via quantitative single nucleotide polymorphism typing. Genetics 184, 19-26 (2010
21. Wolyn, D. J. et al. Light-response quantitative trait loci identified with composite interval and eXtreme array mapping in Arabidopsis thaliana. Genetics 167, 907-917 (2004
22. Schneeberger, K. et al. SHOREmap: simultaneous mapping and mutation identification by deep sequencing. Nature Methods 6, 550-551 (2009
23. Davey, J. W. et al. Genome-wide genetic marker discovery and genotyping using next-generation sequencing. Nature Rev. Genet. 12, 499-510 (2011
24. Lister, R., Gregory, B. D. & Ecker, J. R. Next is now: new technologies for sequencing of genomes, transcriptomes, and beyond. Curr. Opin. Plant Biol. 12, 107-118 (2009
25. Cuperus, J. T. et al. Identification of MIR390a precursor processing-defective mutants in Arabidopsis by direct genome sequencing. Proc. Natl Acad. Sci. USA 107, 466-471 (2010
26. Austin, R. S. et al. Next-generation mapping of Arabidopsis genes. Plant J. 67, 715-725 (2011
27. Manavella, P. A. et al. Fast-forward genetics identifies plant CPL phosphatases as regulators of miRNA processing factor HYL1. Cell 151, 859-870 (2012
28. Uchida, N., Sakamoto, T., Kurata, T. & Tasaka, M. Identification of EMS-induced causal mutations in a non-reference Arabidopsis thaliana accession by whole genome sequencing. Plant Cell Physiol. 52, 716-722 (2011
29. Wenger, J. W., Schwartz, K. & Sherlock, G. Bulk segregant analysis by high-Throughput sequencing reveals a novel xylose utilization gene from Saccharomyces cerevisiae. PLoS Genet. 6, e1000942 (2010
30. Doitsidou, M., Poole, R. J., Sarin, S., Bigelow, H. & Hobert, O. C. elegans mutant identification with a one-step whole-genome-sequencing and SNP mapping strategy. PLoS ONE 5, e15435 (2010
31. Pomraning, K. R., Smith, K. M. & Freitag, M. Bulk segregant analysis followed by high-Throughput sequencing reveals the Neurospora cell cycle gene, ndc 1, to be allelic with the gene for ornithine decarboxylase, spe 1. Eukaryot. Cell 10, 724-733 (2011
32. Leshchiner, I. et al. Mutation mapping and identification by whole genome sequencing. Genome Res. 22, 1541-1548 (2012
33. Voz, M. L. et al. Fast homozygosity mapping and identification of a zebrafish ENU-induced mutation by whole-genome sequencing. PLoS ONE 7, e34671 (2012
34. Bowen, M. E., Henke, K., Siegfried, K. R., Warman, M. L. & Harris, M. P. Efficient mapping and cloning of mutations in zebrafish by low-coverage whole-genome sequencing. Genetics 190, 1017-1024 (2012
35. Obholzer, N. et al. Rapid positional cloning of zebrafish mutations by linkage and homozygosity mapping using whole-genome sequencing. Development 139, 4280-4290 (2012
36. Lindner, H. et al. SNP-Ratio Mapping (SRM): identifying lethal alleles and mutations in complex genetic backgrounds by next-generation sequencing. Genetics 191, 1381-1386 (2012
37. Galvão, V. C. et al. Synteny-based mapping-by mequencing enabled by targeted enrichment. Plant J. 71, 517-526 (2012
38. Greenberg, M. V. et al. Identification of genes required for de novo DNA methylation in Arabidopsis. Epigenetics 6, 344-354 (2011
39. Abe, A. et al. Genome sequencing reveals agronomically important loci in rice using MutMap. Nature Biotech. 30, 174-178 (2012
40. Hartwig, B., James, G. V., Konrad, K., Schneeberger, K. & Turck, F. Fast isogenic mapping-by sequencing of ethyl methanesulfonate-induced mutant bulks. Plant Physiol. 160, 591-600 (2012
41. Birkeland, S. R. et al. Discovery of mutations in Saccharomyces cerevisiae by pooled linkage analysis and whole-genome sequencing. Genetics 186, 1127-1137 (2010
42. Nowrousian, M., Teichert, I., Masloff, S & Kück, U. Whole-genome Sequencing of Sordaria Macrospora Mutants Identifies Developmental Genes. G3 (Bethesda) 2, 261-270 (2012
43. Zhu, Y. et al. Gene discovery using mutagen-induced polymorphisms and deep sequencing: application to plant disease resistance. Genetics 192, 139-146 (2012
44. Nordström, K. J. et al. Mutation identification by direct comparison of whole-genome sequencing data from mutant and wild-Type individuals using k mers. Nature Biotech. 31, 325-330 (2013
45. Allen, R. S., Nakasugi, K., Doran, R. L., Millar, A. A. & Waterhouse, P. M. Facile mutant identification via a single parental backcross method and application of whole genome sequencing based mapping pipelines. Front. Plant Sci. 4, 362 (2013
46. Zuryn, S., Le Gras, S., Jamet, K. & Jarriault, S. A. Strategy for direct mapping and identification of mutations by whole genome sequencing. Genetics 186, 427-430 (2010
47. Velikkakam James, G. et al. User guide for mapping-by sequencing in Arabidopsis. Genome Biol. 14, R61 (2013
48. Fekih, R. et al. MutMap+: genetic mapping and mutant identification without crossing in rice. PLoS ONE 8, e68529 (2013
49. Lander, E. S. & Botstein, D. Homozygosity mapping: a way to map human recessive traits with the DNA of inbred children. Science 236, 1567-1570 (1987
50. Hildebrandt, F. et al. A systematic approach to mapping recessive disease genes in individuals from outbred populations. PLoS Genet. 5, e1000353 (2009
51. Singh, R. et al. The oil palm SHELL gene controls oil yield and encodes a homologue of SEEDSTICK. Nature 500, 340-344 (2013
52. del Viso, F., Bhattacharya, D., Kong, Y., Gilchrist, M. J. & Khokha, M. K. Exon capture and bulk segregant analysis: rapid discovery of causative mutations using high-Throughput sequencing. BMC Genomics 13, 649 (2012
53. Smith, D. R. et al. Rapid whole-genome mutational profiling using next-generation sequencing technologies. Genome Res. 18, 1638-1642 (2008
54. Srivatsan, A. et al. High-precision, whole-genome sequencing of laboratory strains facilitates genetic studies. PLoS Genet. 4, e1000139 (2008
55. Irvine, D. V. et al. Mapping epigenetic mutations in fission yeast using whole-genome next-generation sequencing. Genome Res. 19, 1077-1083 (2009
56. Ashelford, K. et al. Full genome re sequencing reveals a novel circadian clock mutation in Arabidopsis. Genome Biol. 12, R28 (2011
57. Sarin, S., Prabhu, S., O'Meara, M. M., Pe'er, I. & Hobert, O. Caenorhabditis elegans mutant allele identification by whole-genome sequencing. Nature Methods 5, 865-867 (2008
58. Blumenstiel, J. P. et al. Identification of EMS-induced mutations in Drosophila melanogaster by whole-genome sequencing. Genetics 182, 25-32 (2009
59. Sobreira, N. L. et al. Whole-genome sequencing of a single proband together with linkage analysis identifies a Mendelian disease gene. PLoS Genet. 6, e1000991 (2010
60. McCluskey, K Et Al. Rediscovery by Whole Genome Sequencing: Classical Mutations and Genome Polymorphisms in Neurospora Crassa. G3 (Bethesda) 1, 303-316 (2011
61. Arnold, C. N. et al. Rapid identification of a disease allele in mouse through whole genome sequencing and bulk segregation analysis. Genetics 187, 633-641 (2011
62. Dutcher, S K. et Al. Whole-genome Sequencing to Identify Mutants and Polymorphisms in Chlamydomonas Reinhardtii. G3 (Bethesda) 2, 15-22 (2012
63. Krothapalli, K. et al. Forward genetics by genome sequencing reveals that rapid cyanide release deters insect herbivory of Sorghum bicolor. Genetics 195, 309-318 (2013
64. Lin, H., Miller, M. L., Granas, D. M. & Dutcher, S. K. Whole genome sequencing identifies a deletion in protein phosphatase 2A that affects its stability and localization in Chlamydomonas reinhardtii. PLoS Genet. 9, e1003841 (2013
65. Schneeberger, K. & Weigel, D. Fast-forward genetics enabled by new sequencing technologies. Trends Plant Sci. 16, 282-288 (2011
66. Gerhold, A. R., Richter, D. J., Yu, A. S. & Hariharan, I. K. Identification and characterization of genes required for compensatory growth in Drosophila. Genetics 189, 1309-1326 (2011
67. Belfield, E. J. et al. Genome-wide analysis of mutations in mutant lineages selected following fast-neutron irradiation mutagenesis of Arabidopsis thaliana. Genome Res. 22, 1306-1315 (2012
68. Hill, J. T. et al. MMAPPR: mutation mapping analysis pipeline for pooled RNA-seq. Genome Res. 23, 687-697 (2013
69. Minevich, G., Park, D. S., Blankenberg, D., Poole, R. J. & Hobert, O. CloudMap: a cloud-based pipeline for analysis of mutant genome sequences. Genetics 192, 1249-1269 (2012
70. Edwards, M. D. & Gifford, D. K. High-resolution genetic mapping with pooled sequencing. BMC Bioinformatics 13 (Suppl. 6), S8 (2012
71. Magwene, P. M., Willis, J. H. & Kelly, J. K. The statistics of bulk segregant analysis using next generation sequencing. PLoS Comput. Biol. 7, e1002255 (2011
72. Henke, K., Bowen, M. E. & Harris, M. P. Perspectives for identification of mutations in the zebrafish: making use of next-generation sequencing technologies for forward genetic approaches. Methods 62, 185-196 (2013
73. Zuryn, S. & Jarriault, S. Deep sequencing strategies for mapping and identifying mutations from genetic screens. Worm 2, e25081 (2013
74. Wijnker, E. et al. The genomic landscape of meiotic crossovers and gene conversions in Arabidopsis thaliana. Elife 2, e01426 (2013
75. Long, Q. et al. Massive genomic variation and strong selection in Arabidopsis thaliana lines from Sweden. Nature Genet 45, 884-890 (2013
76. Fairfield, H. et al. Mutation discovery in mice by whole exome sequencing. Genome Biol. 12, R86 (2011
77. Andrews, T. D. et al. Massively parallel sequencing of the mouse exome to accurately identify rare, induced mutations: an immediate source for thousands of new mouse models. Open Biol. 2, 120061 (2012
78. Gupta, T. et al. Microtubule actin crosslinking factor 1 regulates the Balbiani body and animal-vegetal polarity of the zebrafish oocyte. PLoS Genet. 6, e1001073 (2010
79. Wang, H. et al. Rapid identification of heterozygous mutations in Drosophila melanogaster using genomic capture sequencing. Genome Res. 20, 981-988 (2010
80. Bontems, F. et al. Efficient mutation identification in zebrafish by microarray capturing and next generation sequencing. Biochem. Biophys. Res. Commun. 405, 373-376 (2011
81. O'Rourke, S. M. et al. Rapid mapping and identification of mutations in Caenorhabditis elegans by RAD mapping and genomic interval pull-down sequencing. Genetics 189, 767-778 (2011
82. Sun, M Et Al. Multiplex Chromosomal Exome Sequencing Accelerates Identification of ENU-induced Mutations in the Mouse. G3 (Bethesda) 2, 143-150 (2012
83. Mascher, M. et al. Mapping-by sequencing accelerates forward genetics in barley. Genome Biol. 15, R78 (2014
84. Pankin, A. et al. Mapping-by-sequencing identifies HvPHYTOCHROME C as a candidate gene for the early maturity 5 locus modulating the circadian clock and photoperiodic flowering in barley. Genetics http://dx.doi.org/10.1534/genetics.114.165613 (2014
85. Ryan, S. et al. Rapid identification of kidney cyst mutations by whole exome sequencing in zebrafish. Development 140, 4445-4451 (2013
86. Mokry, M. et al. Identification of factors required for meristem function in Arabidopsis using a novel next generation sequencing fast forward genetics approach. BMC Genomics 12, 256 (2011
87. Lewis, Z. A. et al. High-density detection of restriction-site-Associated DNA markers for rapid mapping of mutated loci in Neurospora. Genetics 177, 1163-1171 (2007
88. Miller, M. R., Dunham, J. P., Amores, A., Cresko, W. A. & Johnson, E. A. Rapid and cost-effective polymorphism identification and genotyping using restriction site associated DNA (RAD) markers. Genome Res. 17, 240-248 (2007
89. Baird, N. A. et al. Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS ONE 3, e3376 (2008
90. Miller, A. C., Obholzer, N. D., Shah, A. N., Megason, S. G. & Moens, C. B. RNA-seq based mapping and candidate identification of mutations from forward genetic screens. Genome Res. 23, 679-686 (2013
91. Liu, S., Yeh, C. T., Tang, H. M., Nettleton, D. & Schnable, P. S. Gene mapping via bulked segregant RNA-seq (BSR-seq). PLoS ONE 7, e36406 (2012
92. Wurtzel, O., Dori-Bachash, M., Pietrokovski, S., Jurkevitch, E. & Sorek, R. Mutation detection with next-generation resequencing through a mediator genome. PLoS ONE 5, e15628 (2010
93. Livaja, M. et al. BSTA: a targeted approach combines bulked segregant analysis with next-generation sequencing and de novo transcriptome assembly for SNP discovery in sunflower. BMC Genomics 14, 628 (2013
94. Ratan, A., Zhang, Y., Hayes, V. M., Schuster, S. C. & Miller, W. Calling SNPs without a reference sequence. BMC Bioinformatics 11, 130 (2010
95. Peterlongo, P., Schnel, N., Pisanti, N., Sagot, M. F. & Lacroix, V. in String Processing and Information Retrieval 147-158 (Springer, 2010
96. Iqbal, Z., Caccamo, M., Turner, I., Flicek, P. & McVean, G. De novo assembly and genotyping of variants using colored de Bruijn graphs. Nature Genet. 44, 226-232 (2012
97. Huang, X. et al. High-Throughput genotyping by whole-genome resequencing. Genome Res. 19, 1068-1076 (2009
98. Sturtevant, A. H. The linear arrangement of six sex-linked factors in Drosophila, as shown by their mode of association. J. Exp. Zool. 14, 43-59 (1913
99. Harper, M. A. et al. Phenotype sequencing: identifying the genes that cause a phenotype directly from pooled sequencing of independent mutants. PLoS ONE 6, e16517 (2011
100. Jiménez-Gómez, J. M. Next generation quantitative genetics in plants. Front. Plant Sci. 2, 77 (2011
101. Lebowitz, R. J., Soller, M. & Beckmann, J. S. Trait-based analyses for the detection of linkage between marker loci and quantitative trait loci in crosses between inbred lines. Theor. Appl. Genet. 73, 556-562 (1987
102. Takagi, H. et al. QTL-seq: rapid mapping of quantitative trait loci in rice by whole genome resequencing of DNA from two bulked populations. Plant J. 74, 174-183 (2013
103. Swinnen, S. et al. Identification of novel causative genes determining the complex trait of high ethanol tolerance in yeast using pooled-segregant whole-genome sequence analysis. Genome Res 22, 975-984 (2012
104. Trick, M. et al. Combining SNP discovery from next-generation sequencing data with bulked segregant analysis (BSA) to fine-map genes in polyploid wheat. BMC Plant Biol. 12, 14 (2012
105. Carter, R., Hunt, P. & Cheesman, S. Linkage Group Selection - a fast approach to the genetic analysis of malaria parasites. Int. J. Parasitol. 37, 285-293 (2007
106. Parts, L. et al. Revealing the genetic structure of a trait by sequencing a population under selection. Genome Res. 21, 1131-1138 (2011
107. Van Leeuwen, T. et al. Population bulk segregant mapping uncovers resistance mutations and the mode of action of a chitin synthesis inhibitor in arthropods. Proc. Natl Acad. Sci. USA 109, 4407-4412 (2012
108. Kinga Modrzynska, K. et al. Quantitative genome re sequencing defines multiple mutations conferring chloroquine resistance in rodent malaria. BMC Genomics 13, 106 (2012
109. Ehrenreich, I. M. et al. Dissection of genetically complex traits with extremely large pools of yeast segregants. Nature 464, 1039-1042 (2010
110. Yang, Z. et al. Mapping of quantitative trait loci underlying cold tolerance in rice seedlings via high-Throughput sequencing of pooled extremes. PLoS ONE 8, e68433 (2013
111. Nolte, V., Pandey, R. V., Kofler, R. & Schlötterer, C. Genome-wide patterns of natural variation reveal strong selective sweeps and ongoing genomic conflict in Drosophila mauritiana. Genome Res. 23, 99-110 (2013
112. Turner, T. L., Bourne, E. C., Von Wettberg, E. J., Hu, T. T. & Nuzhdin, S. V. Population resequencing reveals local adaptation of Arabidopsis lyrata to serpentine soils. Nature Genet 42, 260-263 (2010
113. Takagi, H. et al. MutMap-Gap: whole-genome resequencing of mutant F2 progeny bulk combined with de novo assembly of gap regions identifies the rice blast resistance gene Pii. New Phytol. 200, 276-283 (2013
114. Tobler, R. et al. Massive habitat-specific genomic response in D. melanogaster populations during experimental evolution in hot and cold environments. Mol Biol Evol. 31, 364-375 (2014
115. Keightley, P. D. & Bulfield, G. Detection of quantitative trait loci from frequency changes of marker alleles under selection. Genet. Res. 62, 195-203 (1993
116. Burke, M. K. et al. Genome-wide analysis of a long-Term evolution experiment with Drosophila. Nature 467, 587-590 (2010
117. Turner, T. L., Stewart, A. D., Fields, A. T., Rice, W. R. & Tarone, A. M. Population-based resequencing of experimentally evolved populations reveals the genetic basis of body size variation in Drosophila melanogaster. PLoS Genet. 7, e1001336 (2011
118. Sham, P., Bader, J. S., Craig, I., O'Donovan, M. & Owen, M. DNA pooling: a tool for large-scale association studies. Nature Rev. Genet. 3, 862-871 (2002
119. Goecks, J., Nekrutenko, A., Taylor, J. & Galaxy Team. Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biol. 11, R86 (2010
120. Thorvaldsdóttir, H., Robinson, J. T. & Mesirov, J. P. Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform. 14, 178-192 (2013