Efficient multivariate linear mixed model algorithms for genome-wide association studies.
paper
Cited
Public
- Authors
- Zhou, Xiang; Stephens, Matthew
- Year
- 2014
- Journal
- Nature methods
- PMID
- 24531419
- DOI
- 10.1038/nmeth.2848
- PMCID
- PMC4211878
Multivariate linear mixed models (mvLMMs) are powerful tools for testing associations between single-nucleotide polymorphisms and multiple correlated phenotypes while controlling for population stratification in genome-wide association studies. We present efficient algorithms in the genome-wide efficient mixed model association (GEMMA) software for fitting mvLMMs and computing likelihood ratio tests. These algorithms offer improved computation speed, power and P-value calibration over existing methods, and can deal with more than two phenotypes.
Illustration of the statistical benefits of our new algorithms implemented in GEMMA. (a) A QQ-plot showing the improved calibration of GEMMA p values compared with those from MTMM for simulated null data. Gray shaded area indicates 0.025 and 0.975 point-wise quantiles of the ordered p values under the null distribution. (b) GEMMA p values are consistently more significant than MTMM p values for the HMDP data. (c) Gain in power for GEMMA compared with MTMM in four different simulation scenarios based on the HMDP data. x-axis in shows the proportion of phenotypic variance in the first phenotype explained (PVE) by the SNP, while the point symbol and line type indicate the SNP effect direction (compared with its effect on the first phenotype) and size (quantified by PVE) on the second phenotype (+: opposite direction, 0.8PVE; Γ: opposite direction, 0.2PVE; o: same direction, 0.8PVE; Ξ: same direction, 0.2PVE). (d) Simulation results illustrating the potential gain in power from four-phenotype vs two-phenotype analyses.
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| Functional phenomics and genetics of the root economics space in winter wheat using high-throughput phenotyping of respiration and architecture. | Guo H et al. | β | 2021 | β |
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| Genome-Wide Association Analysis Reveals Genetic Loci and Candidate Genes for Chest, Abdominal, and Waist Circumferences in Two Duroc Pig Populations. | Zhou S et al. | β | 2021 | β |
| Genome-wide association analysis reveals that EDNRB2 causes a dose-dependent loss of pigmentation in ducks. | Xi Y et al. | β | 2021 | β |
| Genome-wide association mapping for grain manganese in rice (Oryza sativa L.) using a multi-experiment approach. | Ruang-Areerate P et al. | β | 2021 | β |
| Genome-wide association studies for mottled eggs in chickens using a high-density single-nucleotide polymorphism array. | Qu L et al. | β | 2021 | β |
| Genome-Wide Association Study Candidate Genes on Mammary System-Related Teat-Shape Conformation Traits in Chinese Holstein Cattle. | Nazar M et al. | β | 2021 | β |
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| Genome-Wide Association Study (GWAS) of dental caries in diverse populations. | Alotaibi RN et al. | β | 2021 | β |
| Genome-Wide Association Study Identifies Candidate Genes Associated with Feet and Leg Conformation Traits in Chinese Holstein Cattle. | Abdalla IM et al. | β | 2021 | β |
| Genome-wide association study suggests an independent genetic basis of zinc and cadmium concentrations in fresh sweet corn kernels. | Baseggio M et al. | β | 2021 | β |
| Genomic association with pathogen carriage in bighorn sheep (<i>Ovis canadensis</i>). | Martin AM et al. | β | 2021 | β |
| Genomic diversity and genome-wide association analysis related to yield and fatty acid composition of wild American oil palm. | Ithnin M et al. | β | 2021 | β |
| GWAS for genetics of complex quantitative traits: Genome to pangenome and SNPs to SVs and k-mers. | Gupta PK | β | 2021 | β |
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| Integrating genomics and multivariate evolutionary quantitative genetics: a case study of constraints on sexual selection in <i>Drosophila serrata</i>. | Reddiex AJ et al. | β | 2021 | β |
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| Phenotyping stomatal closure by thermal imaging for GWAS and TWAS of water use efficiency-related genes. | Pignon CP et al. | β | 2021 | β |
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| Pleiotropic Loci Associated With Foot Disorders and Common Periparturient Diseases in Holstein Cattle. | Lai E et al. | β | 2021 | β |
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| Sarcoptic mange severity is associated with reduced genomic variation and evidence of selection in Yellowstone National Park wolves (<i>Canis lupus</i>). | DeCandia AL et al. | β | 2021 | β |
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| Three pleiotropic loci associated with bone mineral density and lean body mass. | Zhang YX et al. | β | 2021 | β |
| Transcriptome-wide association analysis of brain structures yields insights into pleiotropy with complex neuropsychiatric traits. | Zhao B et al. | β | 2021 | β |
| Using Breeding Populations With a Dual Purpose: Cultivar Development and Gene Mapping-A Case Study Using Resistance to Common Bacterial Blight in Dry Bean (<i>Phaseolus vulgaris</i> L.). | Simons KJ et al. | β | 2021 | β |
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| A framework for transcriptome-wide association studies in breast cancer in diverse study populations. | Bhattacharya A et al. | β | 2020 | β |
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| A genome resource for green millet Setaria viridis enables discovery of agronomically valuable loci. | Mamidi S et al. | β | 2020 | β |
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| An evolutionary population structure model reveals pleiotropic effects of GmPDAT for traits related to seed size and oil content in soybean. | Liu JY et al. | β | 2020 | β |
| A positively selected FBN1 missense variant reduces height in Peruvian individuals. | Asgari S et al. | β | 2020 | β |
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| Exploring natural diversity of Medicago truncatula reveals physiotypes and loci associated with the response of seedling performance to nitrate supply. | Ben Hdech D et al. | β | 2020 | β |
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| Integrating Genetic and Genomic Analyses of Combined Health Data Across Ecotypes to Improve Disease Resistance in Indigenous African Chickens. | Banos G et al. | β | 2020 | β |
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| Leaf shape in <i>Populus tremula</i> is a complex, omnigenic trait. | MΓ€hler N et al. | β | 2020 | β |
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| Natural variation for carotenoids in fresh kernels is controlled by uncommon variants in sweet corn. | Baseggio M et al. | β | 2020 | β |
| New Insights From Imputed Whole-Genome Sequence-Based Genome-Wide Association Analysis and Transcriptome Analysis: The Genetic Mechanisms Underlying Residual Feed Intake in Chickens. | Ye S et al. | β | 2020 | β |
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| simplePHENOTYPES: SIMulation of pleiotropic, linked and epistatic phenotypes. | Fernandes SB et al. | β | 2020 | β |
| Tissue alarmins and adaptive cytokine induce dynamic and distinct transcriptional responses in tissue-resident intraepithelial cytotoxic T lymphocytes. | Zorro MM et al. | β | 2020 | β |
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| A Fast and Powerful Empirical Bayes Method for Genome-Wide Association Studies. | Chang T et al. | β | 2019 | β |
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| A Geometric Perspective on the Power of Principal Component Association Tests in Multiple Phenotype Studies. | Liu Z et al. | β | 2019 | β |
| A GWAS in Latin Americans highlights the convergent evolution of lighter skin pigmentation in Eurasia. | Adhikari K et al. | β | 2019 | β |
| A Multivariate Genome-Wide Association Study of Wing Shape in <i>Drosophila melanogaster</i>. | Pitchers W et al. | β | 2019 | β |
| Analysis of the genetic architecture of energy balance and its major determinants dry matter intake and energy-corrected milk yield in primiparous Holstein cows. | Krattenmacher N et al. | β | 2019 | β |
| A new regulator of seed size control in Arabidopsis identified by a genome-wide association study. | Ren D et al. | β | 2019 | β |
| Association mapping in plants in the post-GWAS genomics era. | Gupta PK et al. | β | 2019 | β |
| Clinical and Genetic Predictors of Priapism in Sickle Cell Disease: Results from the Recipient Epidemiology and Donor Evaluation Study III Brazil Cohort Study. | Cintho Ozahata M et al. | β | 2019 | β |
| Common Variants in the Glycerol Kinase Gene Reduce Tuberculosis Drug Efficacy. | Bellerose MM et al. | β | 2019 | β |
| Comparison of <i>F</i>-tests for Univariate and Multivariate Mixed-Effect Models in Genome-Wide Association Mapping. | Onogi A | β | 2019 | β |
| Complimentary Methods for Multivariate Genome-Wide Association Study Identify New Susceptibility Genes for Blood Cell Traits. | Fatumo S et al. | β | 2019 | β |
| Defining the genetic control of human blood plasma N-glycome using genome-wide association study. | Sharapov SZ et al. | β | 2019 | β |
| Detecting potential pleiotropy across cardiovascular and neurological diseases using univariate, bivariate, and multivariate methods on 43,870 individuals from the eMERGE network. | Zhang X et al. | β | 2019 | β |
| Early progression to active tuberculosis is a highly heritable trait driven by 3q23 in Peruvians. | Luo Y et al. | β | 2019 | β |
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| Flexible statistical methods for estimating and testing effects in genomic studies with multiple conditions. | Urbut SM et al. | β | 2019 | β |
| Genetic and genomic analyses underpin the feasibility of concomitant genetic improvement of milk yield and mastitis resistance in dairy sheep. | Banos G et al. | β | 2019 | β |
| Genetic Dissection of Femoral and Tibial Microarchitecture. | Lu L et al. | β | 2019 | β |
| Genome-wide association and genotype by environment interactions for growth traits in U.S. Gelbvieh cattle. | Smith JL et al. | β | 2019 | β |
| Genome-wide association multi-locus and multi-variate linear mixed models reveal two linked loci with major effects on partial resistance of apricot to bacterial canker. | Omrani M et al. | β | 2019 | β |
| Genome-wide association studies on the phyllosphere microbiome: Embracing complexity in host-microbe interactions. | Beilsmith K et al. | β | 2019 | β |
| Genome-wide association study for salinity tolerance at the flowering stage in a panel of rice accessions from Thailand. | Lekklar C et al. | β | 2019 | β |
| Genome-wide association study of alcohol consumption and use disorder in 274,424 individuals from multiple populations. | Kranzler HR et al. | β | 2019 | β |
| Genome-Wide Association Study of Growth and Feeding Traits in Pekin Ducks. | Zhu F et al. | β | 2019 | β |
| Genome-wide association study reveals novel loci associated with body size and carcass yields in Pekin ducks. | Deng MT et al. | β | 2019 | β |
| Genomewide Gene-by-Sex Interaction Scans Identify ADGRV1 for Sex Differences in Opioid Dependent African Americans. | Yang BZ et al. | β | 2019 | β |
| Genotypes and Genomic Regions Associated With <i>Rhizoctonia solani</i> Resistance in Common Bean. | Oladzad A et al. | β | 2019 | β |
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| Identification of potential genomic regions and candidate genes for egg albumen quality by a genome-wide association study. | Qu L et al. | β | 2019 | β |
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| Multitrait genome-wide association analysis of Populus trichocarpa identifies key polymorphisms controlling morphological and physiological traits. | Chhetri HB et al. | β | 2019 | β |
| Multivariate Genome-Wide Association Analyses Reveal the Genetic Basis of Seed Fatty Acid Composition in Oat (<i>Avena sativa</i> L.). | Carlson MO et al. | β | 2019 | β |
| Multivariate Genome-wide Association Analysis of a Cytokine Network Reveals Variants with Widespread Immune, Haematological, and Cardiometabolic Pleiotropy. | Nath AP et al. | β | 2019 | β |
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| QTL Underlying Circadian Clock Parameters Under Seasonally Variable Field Settings in <i>Arabidopsis thaliana</i>. | Rubin MJ et al. | β | 2019 | β |
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| Testing Pleiotropy <i>vs.</i> Separate QTL in Multiparental Populations. | Boehm FJ et al. | β | 2019 | β |
| The Genetic Architecture of Bovine Telomere Length in Early Life and Association With Animal Fitness. | Ilska-Warner JJ et al. | β | 2019 | β |
| The Gut Microbiome Derived From Anorexia Nervosa Patients Impairs Weight Gain and Behavioral Performance in Female Mice. | Hata T et al. | β | 2019 | β |
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| Urban colonization through multiple genetic lenses: The city-fox phenomenon revisited. | DeCandia AL et al. | β | 2019 | β |
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| Bivariate genome-wide association analysis strengthens the role of bitter receptor clusters on chromosomes 7 and 12 in human bitter taste. | Hwang LD et al. | β | 2018 | β |
| Candidate Variants for Additive and Interactive Effects on Bioenergy Traits in Switchgrass (<i>Panicum virgatum</i> L.) Identified by Genome-Wide Association Analyses. | Ramstein GP et al. | β | 2018 | β |
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