Cited by 1,836Genetic Associations and EpidemiologyGenetic Mapping and Diversity in Plants and AnimalsGenetic and phenotypic traits in livestock

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GenABEL: an R library for genome-wide association analysis

Aulchenko, Yurii S., Ripke, Stephan, Isaacs, Aaron, van Duijn, Cornelia M.·2007·Bioinformatics

DOI 10.1093/bioinformatics/btm108

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Abstract

Here we describe an R library for genome-wide association (GWA) analysis. It implements effective storage and handling of GWA data, fast procedures for genetic data quality control, testing of association of single nucleotide polymorphisms with binary or quantitative traits, visualization of results and also provides easy interfaces to standard statistical and graphical procedures implemented in base R and special R libraries for genetic analysis. We evaluated GenABEL using one simulated and two real data sets. We conclude that GenABEL enables the analysis of GWA data on desktop computers. Availability: http://cran.r-project.org Contact: i.aoultchenko@erasmusmc.nl

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Method
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Method
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Method
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Method
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Method
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Method
Linkage disequilibrium patterns and persistence of phase in purebred and crossbred pig (Sus scrofa) populations
Veroneze, R., Bastiaansen, J. W. M., Knol, E. F., Guimarães, S. E. F., Silva, F. F. E., Harlizius, B., Lopes, M. S., & Lopes, P. S. (2014) · BMC Genetics · doi:10.1186/s12863-014-0126-3 · Cited by 44
“The R software [33] was used for within population marker quality control, using the package GenABLE [34].”
Method
A Photoreceptor Contributes to the Natural Variation of Diapause Induction inDaphnia magna
Roulin, A. C., Bourgeois, Y., Stiefel, U., Walser, J., & Ebert, D. (2016) · Molecular Biology and Evolution · doi:10.1093/molbev/msw200 · Cited by 46
“We performed an association mapping between the SNPs in our region of interest on scaffold 1036 and resting stage production using the R package GenAbel.”
MethodInfluential
Gene set based association analyses for the WSSV resistance of Pacific white shrimp Litopenaeus vannamei
Yu, Y., Liu, J., Li, F., Zhang, X., Zhang, C., & Xiang, J. (2017) · Scientific Reports · doi:10.1038/srep40549 · Cited by 43
Genome-wide haplotype analysis improves trait predictions in Brassica napus hybrids
Jan, H. U., Guan, M., Yao, M., Liu, W., Wei, D., Abbadi, A., Zheng, M., He, X., Chen, H., Guan, C., et al. (2019) · Plant Science · doi:10.1016/j.plantsci.2019.02.007 · Cited by 44
Meta-analysis of genome-wide association studies for litter size in sheep
Gholizadeh, M., & Esmaeili-Fard, S. M. (2021) · Theriogenology · doi:10.1016/j.theriogenology.2021.12.025 · Cited by 44
A genomewide association mapping study using ultrasound‐scanned information identifies potential genomic regions and candidate genes affecting carcass traits in Nellore cattle
Santana, M. H. D. A., Ventura, R. V., Utsunomiya, Y. T., Neves, H. H. D. R., Alexandre, P. A., Oliveira, G. A., Gomes, R. D. C., Bonin, M. N., Coutinho, L. L., Garcia, J. F., et al. (2015) · Journal of Animal Breeding and Genetics · doi:10.1111/jbg.12167 · Cited by 44
Genetic diversity in an indigenous horse breed - implications for mating strategies and the control of future inbreeding
Signer‐Hasler, H., Flury, C., Menet, S., Haase, B., Leeb, T., Simianer, H., Poncet, P. A., & Rieder, S. (2011) · Journal of Animal Breeding and Genetics · doi:10.1111/j.1439-0388.2011.00932.x · Cited by 45
Genomics and metabolomics of muscular mass in a community-based sample of UK females
Korostishevsky, M., Steves, C. J., Malkin, I., Spector, T. D., Williams, F. M. K., & Livshits, G. (2015) · European Journal of Human Genetics · doi:10.1038/ejhg.2015.85 · Cited by 45
A COL11A2 Mutation in Labrador Retrievers with Mild Disproportionate Dwarfism
Frischknecht, M., Niehof-Oellers, H., Jagannathan, V., Owczarek‐Lipska, M., Drögemüller, C., Dietschi, E., Dolf, G., Tellhelm, B., Lang, J., Tiira, K., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0060149 · Cited by 48
“We used GenABEL [31] to perform a GWAS with correction for the population stratification.”
Method
A genome-wide association study reveals a novel candidate gene for sperm motility in pigs
Diniz, D. B., Lopes, M. S., Broekhuijse, M. L. W. J., Lopes, P. S., Harlizius, B., Guimarães, S. E. F., Duijvesteijn, N., Knol, E. F., & Silva, F. F. (2014) · Animal Reproduction Science · doi:10.1016/j.anireprosci.2014.10.014 · Cited by 44
Meta‐analysis of genome‐wide association from genomic prediction models
Rubio, Y. L. B., Duarte, J. L. G., Bates, R. O., Ernst, C. W., Nonneman, D., Rohrer, G. A., King, A. H., Shackelford, T. K., WHEELER, T. L., Cantet, R. J. C., et al. (2015) · Animal Genetics · doi:10.1111/age.12378 · Cited by 44
“Moreover, as a legacy to the widespread use of MA in human GWA, there are a number of programs available to perform these types of analysis that share common features (METAQTL, Veyrieras et al. 2007; METAL, Willer et al. 2010; METABEL, Aulchenko et al. 2007; GWAMA, M€agi & Morris 2010).”
Method
Identification of Candidate Genes for Reactivity in Guzerat (Bos indicus) Cattle: A Genome-Wide Association Study
Santos, F. C. D., Peixoto, M. G. C. D., Fonseca, P. A. D. S., Pires, M. D. F. Á., Ventura, R. V., Rosse, I. C., Bruneli, F. Â. T., Machado, M. A., & Carvalho, M. R. S. (2017) · PLoS ONE · doi:10.1371/journal.pone.0169163 · Cited by 45
Systemic and specific effects of antihypertensive and lipid-lowering medication on plasma protein biomarkers for cardiovascular diseases
Enroth, S., Maturi, V., Berggrund, M., Enroth, S. B., Moustakas, A., Johansson, Å., & Gyllensten, U. (2018) · Scientific Reports · doi:10.1038/s41598-018-23860-y · Cited by 45
A Polygenic Genetic Architecture of Flowering Time in the WorldwideArabidopsis thalianaPopulation
Zan, Y., & Carlborg, Ö. (2018) · Molecular Biology and Evolution · doi:10.1093/molbev/msy203 · Cited by 44
Genome-wide association study of Mycobacterium avium subspecies Paratuberculosis infection in Chinese Holstein
Gao, Y., Jiang, J., Yang, S., Cao, J., Han, B., Wang, Y., Zhang, Y., Yu, Y., Zhang, S., Zhang, Q., et al. (2018) · BMC Genomics · doi:10.1186/s12864-018-5385-3 · Cited by 44
Seasonal Effects on Gene Expression
Goldinger, A., Shakhbazov, K., Henders, A. K., McRae, A. F., Montgomery, G. W., & Powell, J. E. (2015) · PLoS ONE · doi:10.1371/journal.pone.0126995 · Cited by 44
“The normalization was done using the R package GenABEL [38].”
Method
Genome-wide association study of aggressive behaviour in chicken
Li, Z., Zheng, M., Abdalla, B. A., Zhang, Z., Xu, Z., Ye, Q., Xu, H., Luo, W. F., Nie, Q., & Zhang, X. (2016) · Scientific Reports · doi:10.1038/srep30981 · Cited by 45
Identification and validation of a regulatory mutation upstream of the BMP2 gene associated with carcass length in pigs
Li, J., Peng, S., Zhong, L., Zhou, L., Yan, G., Xiao, S., Ma, J., & Huang, L. (2021) · Genetics Selection Evolution · doi:10.1186/s12711-021-00689-0 · Cited by 43
“GWAS analysis Genome-wide association analyses of body size were conducted using the GenABEL package in the R software [27].”
Method
Genetic Parameters and Genomic Regions Underlying Growth and Linear Type Traits in Akkaraman Sheep
Kızılaslan, M., Arzık, Y., White, S. N., Piel, L. M. W., & Çınar, M. U. (2022) · Genes · doi:10.3390/genes13081414 · Cited by 43
“Correspondingly, the ‘GenABEL’ R package [32] was used to remove SNPs with a minor allele frequency (MAF) <0.”
Method
Parent-of-Origin inference for biobanks
Hofmeister, R. J., Rubinacci, S., Ribeiro, D. M., Buil, A., Kutalik, Z., & Delaneau, O. (2022) · Nature Communications · doi:10.1038/s41467-022-34383-6 · Cited by 42
A Genome-Wide Association Analysis Reveals Epistatic Cancellation of Additive Genetic Variance for Root Length in Arabidopsis thaliana
Lachowiec, J., Shen, X., Queitsch, C., & Carlborg, Ö. (2015) · PLoS Genetics · doi:10.1371/journal.pgen.1005541 · Cited by 42
“For the standard additive GWA analysis with population structure controlled, we used the function egscore() from R/GenABEL [38].”
MethodInfluential
Gene-alcohol interactions identify several novel blood pressure loci including a promising locus near SLC16A9
Simino, J. M., Sung, Y. J., Kume, R., Schwander, K., & Rao, D. C. (2013) · Frontiers in Genetics · doi:10.3389/fgene.2013.00277 · Cited by 44
“We used the ABEL suite of packages to perform a two-step score test of the interaction between each SNP and alcohol measure on each BP trait (Aulchenko et al., 2007).”
BackgroundMethodInfluential
Genetic variants in ABCG 1 are associated with survival of nonsmall‐cell lung cancer patients
Wang, Y., Liu, H., Ready, N., Su, L., Wei, Y., Christiani, D. C., & Wei, Q. (2016) · International Journal of Cancer · doi:10.1002/ijc.29991 · Cited by 43
“Associations between SNPs and OS (in additive models) were obtained by both univariate and multivariable Cox regression analyses performed with GenABEL package of R software with adjustment for age, sex, smoking status, histology, tumor stage, chemotherapy, radiotherapy and surgery.(28) For multiple testing correction…”
Method
The chromosome 6q22.33 region is associated with age at diagnosis of type 1 diabetes and disease risk in those diagnosed under 5 years of age
Inshaw, J. R. J., Walker, N. M., Wallace, C., Bottolo, L., & Todd, J. A. (2017) · Diabetologia · doi:10.1007/s00125-017-4440-y · Cited by 41
“We called this approach the ‘residual-based model’, and it has been proposed by Aulchenko et al [21] to make genomewide analysis for related individuals possible.”
Method
Genomewide Meta‐Analysis Validates a Role for S1PR1 in Microtubule Targeting Agent‐Induced Sensory Peripheral Neuropathy
Chua, K. C., Xiong, C., Ho, C., Mushiroda, T., Chen, J., Mulkey, F. A., Lai, D., Schneider, B. P., Rashkin, S. R., Witte, J. S., et al. (2020) · Clinical Pharmacology & Therapeutics · doi:10.1002/cpt.1958 · Cited by 39
Genetic and microbiome analysis of feed efficiency in laying hens
Zhou, Q., Lan, F., Gu, S., Li, G., Wu, G., Yan, Y., Li, X., Jin, J., Wen, C., Sun, C., et al. (2022) · Poultry Science · doi:10.1016/j.psj.2022.102393 · Cited by 42
“inverse normal transformations using the GenABEL package in R (Aulchenko et al., 2007).”
Method
Genome-Wide Genotyping Demonstrates a Polygenic Risk Score Associated With White Matter Hyperintensity Volume in CADASIL
Opherk, C., Gonik, M., Duering, M., Malik, R., Jouvent, É., Hervé, D., Adib‐Samii, P., Bevan, S., Pianese, L., Silvestri, S., et al. (2014) · Stroke · doi:10.1161/strokeaha.113.004461 · Cited by 42
“The mmscore function within GenABEL was used to implement a powerful family-based association test with control for stratification in admixed samples by providing the estimates of ancestry of each individual as covariates.(14) Results were corrected for possible genomic inflation.”
Method
Genome‐wide associations for investigating time‐dependent genetic effects for milk production traits in dairy cattle
Strucken, E. M., Bortfeldt, R. H., de Koning, D., & Brockmann, G. A. (2011) · Animal Genetics · doi:10.1111/j.1365-2052.2011.02278.x · Cited by 42
MGAS: a powerful tool for multivariate gene-based genome-wide association analysis
van der Sluis, S., Dolan, C. V., Li, J., Song, Y., Sham, P. C., Danielle Posthuma, B., & Li, M. (2014) · Bioinformatics · doi:10.1093/bioinformatics/btu783 · Cited by 42
“Standard genome-wide association studies (GWAS) involve the univariate regression of one trait on a large number of genetic variants (single nucleotide polymorphisms, i.e. SNPs), while adapting the nominal a criterion level for the extensive multiple testing (typically a¼5 10 8).”
BackgroundMethod
Haplotype reference consortium panel: Practical implications of imputations with large reference panels
Iglesias, A. I., van der Lee, S. J., Bonnemaijer, P. W. M., Höhn, R., Nag, A., Gharahkhani, P., Khawaja, A. P., Broer, L., Foster, P. J., Hammond, C. J., et al. (2017) · Human Mutation · doi:10.1002/humu.23247 · Cited by 45
Taking advantage from phenotype variability in a local animal genetic resource: identification of genomic regions associated with the hairless phenotype in Casertana pigs
Schiavo, G., Bertolini, F., Utzeri, V. J., Ribani, A., Geraci, C., Santoro, L., Óvilo, C., Fernández, A. I., Gallo, M., & Fontanesi, L. (2018) · Animal Genetics · doi:10.1111/age.12665 · Cited by 42
A role for the OsHKT 2;1 sodium transporter in potassium use efficiency in rice
Hartley, T. N., Thomas, A., & Maathuis, F. J. M. (2019) · Journal of Experimental Botany · doi:10.1093/jxb/erz113 · Cited by 42
“3 and the GenABEL R package (Aulchenko et al., 2007) for KUE metrics, RGR, and tissue cation concentrations.”
Method
A novel analytical method, Birth Date Selection Mapping, detects response of the Angus (Bos taurus) genome to selection on complex traits
Decker, J. E., Vasco, D. A., McKay, S., McClure, M. C., Rolf, M. M., Kim, J., Northcutt, S. L., Bauck, S. W., Woodward, B. W., Schnabel, R. D., et al. (2012) · BMC Genomics · doi:10.1186/1471-2164-13-606 · Cited by 46
“Test statistic p-values for each SNP produced by EMMAX were adjusted to q-values using the method of Benjamini and Hochberg [62] as implemented by the GenABEL package in R [63].”
Method
A nonsense mutation in B3GALNT2 is concordant with hydrocephalus in Friesian horses
Ducro, B. J., Schurink, A., Bastiaansen, J. W. M., Boegheim, I. J. M., van Steenbeek, F. G., Vos‐Loohuis, M., Nijman, I. J., Monroe, G. R., Hellinga, I., Dibbits, B. W., et al. (2015) · BMC Genomics · doi:10.1186/s12864-015-1936-z · Cited by 41
“The significance level of differences in genotype frequencies between cases and controls per SNP was determined with a χ(2)-test from 2 × 3 (genotypic) tables using the ccfast function in the GenABEL package in R [23].”
Method
Genome-Wide Association Mapping in Dogs Enables Identification of the Homeobox Gene, NKX2-8, as a Genetic Component of Neural Tube Defects in Humans
Safra, N., Bassuk, A. G., Ferguson, P. J., Aguilar, M., Coulson, R. L., Thomas, N. C., Hitchens, P. L., Dickinson, P. J., Vernau, K. M., Wolf, Z. T., et al. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003646 · Cited by 41
Genetic Variants Associated with Serum Thyroid Stimulating Hormone (TSH) Levels in European Americans and African Americans from the eMERGE Network
Malinowski, J. R., Denny, J. C., Bielinski, S. J., Basford, M., Bradford, Y., Peissig, P. L., Carrell, D., Crosslin, D. R., Pathak, J., Rasmussen, L. V., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0111301 · Cited by 41
“Control for population stratification was evaluated with Q-Q plots and calculation of the lambda statistic using R packages qqman and GenABEL [33].”
Method
Association of breast cancer risk with genetic variants showing differential allelic expression: Identification of a novel breast cancer susceptibility locus at 4q21
Hamdi, Y., Collaborators, N., Soucy, P., Adoue, V., Michailidou, K., Canisius, S., Lemaçon, A., Droit, A., Andrulis, I. L., Anton‐Culver, H., et al. (2016) · Oncotarget · doi:10.18632/oncotarget.12818 · Cited by 39
“Identity by state was computed using the R GenABEL package [90], and closely related samples with IBS > 0.”
Genetic Architecture of Flooding Tolerance in the Dry Bean Middle-American Diversity Panel
Soltani, A., MafiMoghaddam, S., Walter, K. A., Restrepo-Montoya, D., Mamidi, S., Schroder, S., Lee, R., McClean, P. E., & Osorno, J. M. (2017) · Frontiers in Plant Science · doi:10.3389/fpls.2017.01183 · Cited by 41
“The phenotypic variation explained by most significant markers (which was defined as the markers with highest LOD) in the best model was calculated based on the likelihood-ratio-based R2 (R2LR) (Sun et al., 2010) using the genABLE package in R (Aulchenko et al., 2007).”
Method
Genome-wide association studies of inflammatory bowel disease in German shepherd dogs
Peiravan, A., Bertolini, F., Rothschild, M. F., Simpson, K. W., Jergens, A. E., Allenspach, K., & Werling, D. (2018) · PLoS ONE · doi:10.1371/journal.pone.0200685 · Cited by 41
A role for SPEECHLESS in the integration of leaf stomatal patterning with the growth vs disease trade‐off in poplar
McKown, A. D., Klápště, J., Guy, R. D., Corea, O. R. A., Fritsche, S., Ehlting, J., El-Kassaby, Y. A., & Mansfield, S. D. (2019) · New Phytologist · doi:10.1111/nph.15911 · Cited by 41
“The association analysis was performed using the ‘qtscore’ function implemented in the GENABEL R package (Aulchenko et al., 2007).”
Method
Identification of Growth-Associated Genes by Genome-Wide Association Study and Their Potential Application in the Breeding of Pacific White Shrimp (Litopenaeus vannamei)
Lyu, D., Yu, Y., Wang, Q., Luo, Z., Zhang, Q., Zhang, X., Xiang, J., & Li, F. (2021) · Frontiers in Genetics · doi:10.3389/fgene.2021.611570 · Cited by 43
“Considering a possible stratification due to multiple origins of the shrimp, GWAS was performed using the egscore function in GenABEL package implemented in R environment (Aulchenko et al., 2007).”
Method

Authors: Aulchenko, Y. S., Ripke, S., Isaacs, A., & van Duijn, C. M.
Affiliations: Erasmus MC (NL)
1 Department of Epidemiology and Biostatistics, Erasmus MC Rotterdam, Postbus 2040, 3000 CA Rotterdam, The Netherlands and 2Statistical Genetics Group, Max-Planck-Institute of Psychiatry, Kraepelinstr. 10, D-80804 Munich, Germany
Corresponding author: Aulchenko, Yurii S.
ORCID: Aulchenko, Yurii S.
Ripke, Stephan
Isaacs, Aaron
Venue: Bioinformatics
Publisher: Oxford University Press (OUP)
Published: 2007-03-23
Volume: 23
Issue: 10
Pages: 1294-1296
ISSN: 1367-4803 (ISSN-L)
1367-4811
DOI: 10.1093/bioinformatics/btm108
OpenAlex: W2161245845
Cited by: 1,836
References: 4
Citations by year: 2026: 22 · 2025: 39 · 2024: 91 · 2023: 72 · 2022: 65 · 2021: 129 · 2020: 113 · 2019: 161 · 2018: 178 · 2017: 153 · 2016: 139 · 2015: 143 · 2014: 140 · 2013: 116 · 2012: 89
FWCI: 19.99
Type: journal article
Language: en
Open access: closed
Locations: Bioinformatics (publishedVersion)
PubMed (publishedVersion)
EUR Research Repository (Erasmus University Rotterdam) (publishedVersion)
EUR Research Repository (Erasmus University Rotterdam) (submittedVersion)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Associations and Epidemiology
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Mapping and Diversity in Plants and Animals
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic and phenotypic traits in livestock
Keywords: genome-wide association study, R library, single nucleotide polymorphisms, association testing, binary traits, quantitative traits, statistical software
MeSH terms: Computer Simulation, Haplotypes, Humans, Software, Gene Library, Genome, Human, Information Storage and Retrieval, Genome, Computational Biology, Oligonucleotide Array Sequence Analysis, Polymorphism, Single Nucleotide

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GenABEL: an R library for genome-wide association analysis

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