Recombination Rate Variation, Hitchhiking, and Demographic History Shape Deleterious Load in Poplar

Molecular Biology and Evolution

Volumn 33, Issue 11, 2016, Pages 2899-2910

  Zhang, M ^a   Zhou, L ^a   Bawa, R ^a   Suren, H ^a   Holliday, J A ^a  

^a VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

Author keywords

deleterious alleles; genetic hitchhiking; genetic load; populus trichocarpa; selective sweep

Indexed keywords

DEMOGRAPHY; EFFECTIVE POPULATION SIZE; EXOME; GENE FREQUENCY; GENETIC LOAD; HOMOZYGOSITY; HUMAN; HUMAN EXPERIMENT; NATURAL POPULATION; NONHUMAN; PLANT GROWTH; POPULATION MODEL; POPULUS TRICHOCARPA; PURIFYING SELECTION; SELECTIVE SWEEP; SPECIES; ALLELE; GENETIC RECOMBINATION; GENETIC SELECTION; GENETIC VARIATION; GENETICS; GENOMICS; HOMOZYGOTE; MOLECULAR EVOLUTION; NUCLEIC ACID DATABASE; PLANT GENOME; POPULATION DENSITY; POPULUS; PROCEDURES;

ALLELES; DATABASES, NUCLEIC ACID; DEMOGRAPHY; EVOLUTION, MOLECULAR; GENE FREQUENCY; GENETIC LOAD; GENETIC VARIATION; GENOME, PLANT; GENOMICS; HOMOZYGOTE; POPULATION DENSITY; POPULUS; RECOMBINATION, GENETIC; SELECTION, GENETIC;

EID: 84994530600     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msw169     Document Type: Article

References (83)

1. Agrawal AF, Whitlock MC. 2012. Mutation load: the fitness of individuals in populations where deleterious alleles are abundant. Ann Rev Ecol Evol Syst. 43:115.
2. Bass JD, Swcf AJ, Dabney A, Robinson D. 2015. qvalue: Q-value estimation for false discovery rate control. R package version 2.4.2. Available from: http://github.com/jdstorey/qvalue.
3. Benjamini Y, Hochberg Y. 2000. On the adaptive control of the false discovery rate in multiple testing with independent statistics. J Educ Behav Stat. 25:60-83.
4. Betancourt AJ, Welch JJ, Charlesworth B. 2009. Reduced effectiveness of selection caused by a lack of recombination. Curr Biol. 19:655-660.
5. Bosch M, Mayer CD, Cookson A, Donnison IS. 2011. Identification of genes involved in cell wall biogenesis in grasses by differential gene expression profiling of elongating and non-elongating maize inter-nodes. J Exp Bot. 62:3545-3561.
6. Boyko AR, Williamson SH, Indap AR, Degenhardt JD, Hernandez RD, Lohmueller KE, Adams MD, Schmidt S, Sninsky JJ, Sunyaev SR, et al. 2008. Assessing the evolutionary impact of amino acid mutations in the human genome. Plos Genet. 4:e1000083.
7. Campos JL, Halligan DL, Haddrill PR, Charlesworth B. 2014. The relation between recombination rate and patterns of molecular evolution and variation in Drosophila melanogaster. Mol Biol Evol. 31:1010-1028.
8. Cao J, Schneeberger K, Ossowski S, Gunther T, Bender S, Fitz J, Koenig D, Lanz C, Stegle O, Lippert C, et al. 2011. Whole-genome sequencing of multiple Arabidopsis thaliana populations. Nat Genet. 43:956-963.
9. Charlesworth B. 2007. Mutation-selection balance and the evolutionary advantage of sex and recombination. Genet Res. 89:451-473.
10. Charlesworth B, Charlesworth D. 2000. The degeneration of Y chromosomes. Philos Trans R Soc Lond B Biol Sci. 355:1563-1572.
11. Charlesworth D, Willis JH. 2009. The genetics of inbreeding depression. Nat Rev Genet. 10:783-796.
12. Choi Y, Sims GE, Murphy S, Miller JR, Chan AP. 2012. Predicting the functional effect of amino acid substitutions and indels. Plos One 7. Available from: http://dx.doi.org/10.1371/journal.pone.0046688.
13. Chun S, Fay JC. 2011. Evidence for hitchhiking of deleterious mutations within the human genome. Plos Genet. 7:e1002240.
14. Cirulli ET, Lasseigne BN, Petrovski S, Sapp PC, Dion PA, Leblond CS, Couthouis J, Lu Y-F, Wang Q, Krueger BJ, et al. 2015. Exome sequencing in amyotrophic lateral sclerosis identifies risk genes and pathways. Science 347:1436-1441.
15. Crow JF. 1958. Some possibilities for measuring selection intensities in man. Hum Biol. 30:1-13.
16. Demarsy E, Schepens I, Okajima K, Hersch M, Bergmann S, Christie J, Shimazaki K-i, Tokutomi S, Fankhauser C. 2012. Phytochrome kinase substrate 4 is phosphorylated by the phototropin 1 photoreceptor. EMBO J. 31:3457-3467.
17. DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, Hartl C, Philippakis AA, del Angel G, Rivas MA, Hanna M, et al. 2011. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet. 43:491-498.
18. Dickson SP, Wang K, Krantz I, Hakonarson H, Goldstein DB. 2010. Rare Variants Create Synthetic Genome-Wide Associations. PLoS Biol. 8(1):e1000294
19. Do R, Stitziel NO, Won H-H, Jorgensen AB, Duga S, Merlini PA Kiezun A, Farrall M, Goel A Zuk O, et al. 2015. Exome sequencing identifies rare LDLR and APOA5 alleles conferring risk for myocardial infarction. Nature 518:102.
20. Evans LM, Slavov GT, Rodgers-Melnick E, Martin J, Ranjan P, Muchero W, Brunner AM, Schackwitz W, Gunter L, Chen JG, et al. 2014. Population genomics of Populus Trichocarpa identifies signatures of selection and adaptive trait associations. Nat Genet. 46:1089-1096.
21. Eyre-Walker A Keightley PD. 2007. The distribution of fitness effects of new mutations. Nat Rev Genet. 8:610-618.
22. Fay JC, Wyckoff GJ, Wu CI. 2001. Positive and negative selection on the human genome. Genetics 158:1227-1234
23. Felsenstein J. 1974. The evolutionary advantage of recombination. Genetics 78:737-756.
24. Fu W, Gittelman RM, Bamshad MJ, Akey JM. 2014. Characteristics of neutral and deleterious protein-coding variation among individuals and populations. Am J Hum Genet. 95:421-436.
25. Gossmann TI, Song BH, Windsor AJ, Mitchell-Olds T, Dixon CJ, Kapralov MV, Filatov DA, Eyre-Walker A 2010. Genome wide analyses reveal little evidence for adaptive evolution in many plant species. Mol Biol Evol. 27:1822-1832.
26. Goudet J. 2014. hierfstat Estimation and tests of hierarchical F-statistics: R package version 0.04-14.
27. Gunther T, Schmid KJ. 2010. Deleterious amino acid polymorphisms in Arabidopsis thaliana and rice. Theor Appl Genet. 121:157-168.
28. Henn BM, Botigue LR, Bustamante CD, Clark AG, Gravel S. 2015. Estimating the mutation load in human genomes. Nat Rev Genet. 16:333-343.
29. Henn BM, Botigue LR, Peischl S, Dupanloup I, Lipatov M, Maples BK, Martin AR, Musharoff S, Cann H, Snyder MP, et al. 2016. Distance from sub-Saharan Africa predicts mutational load in diverse human genomes. Proc Natl Acad Sci USA. 113:E440-E449.
30. Holliday JA, Zhou L, Bawa R, Zhang M, Oubida RW. 2016. Evidence for extensive parallelism but divergent genomic architecture of adaptation along altitudinal and latitudinal gradients in Populus trichocarpa. New Phytol. 209:1240-1251.
31. Hussin JG, Hodgkinson A Idaghdour Y, Grenier J-C, Goulet J-P, Gbeha E, Hip-Ki E, Awadalla P. 2015. Recombination affects accumulation of damaging and disease-associated mutations in human populations. Nat Genet. 47:400-U162.
32. Jackson DA 1993. Stopping rules in principal components analysis: a comparison of heuristical and statistical approaches. Ecology 74:2204-2214.
33. Jansson S, Douglas CJ. 2007. Populus: a model system for plant biology. Ann Rev Plant Biol. 58:435-458.
34. Keightley PD. 2012. Rates and fitness consequences of new mutations in humans. Genetics 190:295-304
35. Kimura M, Maruyama T, Crow JF. 1963. The mutation load in small populations. Genetics 48:1303-1312.
36. Lande R. 1994. Risk of population extinction from fixation of new deleterious mutations. Evolution 48:1460-1469.
37. Lange LA Hu Y, Zhang H, Xue C, Schmidt EM, Tang Z-Z, Bizon C, Lange EM, Smith JD, Turner EH, et al. 2014. Whole-exome sequencing identifies rare and low-frequency coding variants associated with LDL cholesterol. Am J Hum Genet. 94:233-245.
38. Leida C, Conesa A Llacer G, Badenes ML, Riios G. 2012. Histone modifications and expression of DAM6 gene in peach are modulated during bud dormancy release in a cultivar-dependent manner. New Phytol. 193:67-80.
39. Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754-1760.
40. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R. 2009. The sequence alignment/map format and SAMtools. Bioinformatics 25:2078-2079.
41. Liscum E, Reed JW. 2002. Genetics of Aux/IAA and ARF action in plant growth and development. Plant Mol Biol. 49:387-400.
42. Loewe L, Hill WG. 2010. The population genetics of mutations: good, bad and indifferent. Philos Trans R Soc Lond B Biol Sci. 365:1153-1167.
43. Lohmueller KE. 2014. The distribution of deleterious genetic variation in human populations. Curr Opin Genet Dev. 29:139-146.
44. Lohmueller KE, Indap AR, Schmidt S, Boyko AR, Hernandez RD, Hubisz MJ, Sninsky JJ, White TJ, Sunyaev SR, Nielsen R, et al. 2008. Proportionally more deleterious genetic variation in European than in African populations. Nature 451:994-997.
45. Lu J, Tang T, Tang H, Huang J, Shi S, Wu CI. 2006. The accumulation of deleterious mutations in rice genomes: a hypothesis on the cost of domestication. Trends Genet. 22:126-131.
46. Lynch M, Conery J, Burger R. 1995. Mutation accumulation and the extinction of small populationS. Am Nat. 146:489-518.
47. Marsden CD, Ortega-Del Vecchyo D, O'Brien DP, Taylor JF, Ramirez O, Vila C, Marques-Bonet T, Schnabel RD, Wayne RK, Lohmueller KE. 2016. Bottlenecks and selective sweeps during domestication have increased deleterious genetic variation in dogs. Proc Natl Acad Sci U S A. 113:152-157.
48. McKown AD, Guy RD, Klapste J, Geraldes A, Friedmann M, Cronk QC, El-Kassaby YA, Mansfield SD, Douglas CJ. 2014. Geographical and environmental gradients shape phenotypic trait variation and genetic structure in Populus trichocarpa. New Phytol. 201:1263-1276.
49. McEvoy BP, Powell JE, Goddard ME, Visscher PM. 2011. Human population dispersal "out of Africa" estimated from linkage disequilibrium and allele frequencies of SNPs. Genome Res. 21(6): 821-829.
50. Mezmouk S, Ross-Ibarra J. 2014. The pattern and distribution of deleterious mutations in maize. G3 (Bethesda) 4:163-171.
51. Ng PC, Henikoff S. 2001. Predicting deleterious amino acid substitutions. Genome Res. 11:863-874.
52. Ng PC, Henikoff S. 2003. SIFT: predicting amino acid changes that affect protein function. Nucleic Acids Res. 31:3812-3814.
53. Ng PC, Henikoff S. 2006. Predicting the effects of amino acid substitutions on protein function. Annu Rev Genomics Hum Genet. 7:61-80.
54. Oubida RW, Gantulga D, Zhang M, Zhou L, Bawa R, Holliday JA. 2015. Partitioning of multivariate phenotypes using regression trees reveals complex patterns of adaptation to climate across the range of black cottonwood (Populus trichocarpa). Front Plant Sci. 6:181.
55. Paige KN. 2010. The functional genomics of inbreeding depression: a new approach to an old problem. BioScience 60:267-277.
56. Pang X, Halaly T, Crane O, Keilin T, Keren-Keiserman A, Ogrodovitch A, Galbraith D, Or E. 2007. Involvement of calcium signalling in dormancy release of grape buds. J Exp Bot. 58:3249-3262.
57. Peng G, Luo L, Siu H, Zhu Y, Hu P, Hong S, Zhao J, Zhou X, Reveille JD, Jin L, et al. 2009. Gene and pathway-based second-wave analysis of genome-wide association studies. Eur J Hum Genet. 18:111-117.
58. Petit RJ, Hampe A. 2006. Some evolutionary consequences of being a tree. Annu Rev Ecol Evol Syst. 187-214. In.
59. Pounds S, Cheng C. 2006. Robust estimation of the false discovery rate. Bioinformatics 22:1979-1987.
60. R Core Team. 2016. R: A language and environment for statistical computing. Vienna (Austria): R Foundation for Statistical Computing. Available from: https://www.R-project.org/.
61. Renaut S, Rieseberg LH. 2015. The accumulation of deleterious mutations as a consequence of domestication and improvement in sunflowers and other compositae crops. Mol Biol Evol. 32:2273-2283.
62. Rinne PL, Welling A, Vahala J, Ripel L, Ruonala R, Kangasjarvi J, van der Schoot C. 2011. Chilling of dormant buds hyperinduces FLOWERING LOCUS T and recruits GA-inducible 1,3-beta-gluca-nases to reopen signal conduits and release dormancy in Populus. Plant Cell 23:130-146.
63. Rodgers-Melnick E, Bradbury PJ, Elshire RJ, Glaubitz JC, Acharya CB, Mitchell SE, Li CH, Li YX, Buckler ES. 2015. Recombination in diverse maize is stable, predictable, and associated with genetic load. Proc Natl Acad Sci U S A. 112:3823-3828.
64. Sellaro R, Yanovsky MJ, Casal JJ. 2011. Repression of shade-avoidance reactions by sunfleck induction of HY5 expression in Arabidopsis. Plant J. 68:919-928.
65. Simons YB, Turchin MC, Pritchard JK, Sella G. 2014. The deleterious mutation load is insensitive to recent population history. Nat Genet. 46:220.
66. Slavov GT, DiFazio SP, Martin J, Schackwitz W, Muchero W, Rodgers-Melnick E, Lipphardt MF, Pennacchio CP, Hellsten U, Pennacchio LA, et al. 2012. Genome resequencing reveals multiscale geographic structure and extensive linkage disequilibrium in the forest treePopulus trichocarpa. New Phytol. 196:713-725.
67. Smithson M, Verkuilen J. 2006. A better lemon squeezer? Maximum-likelihood regression with beta-distributed dependent variables. Psychol Methods. 11:54-71.
68. Stephens M, Donnelly P. 2003. A comparison of bayesian methods for haplotype reconstruction from population genotype data. Am J Hum Genet. 73:1162-1169.
69. Stephens M, Scheet P. 2005. Accounting for decay of linkage disequilibrium in haplotype inference and missing-data imputation. Am J Hum Genet. 76:449-462.
70. Stephens M, Smith NJ, Donnelly P. 2001. A new statistical method for haplotype reconstruction from population data. Am J Hum Genet. 68:978-989.
71. Sunyaev S, Ramensky V, Koch I, Lathe W, 3rd, Kondrashov AS, Bork P. 2001. Prediction of deleterious human alleles. Hum Mol Genet. 10:591-597.
72. Vaser R, Adusumalli S, Leng SN, Sikic M, Ng PC. 2016. SIFT missense predictions for genomes. Nat Protoc. 11:1-9.
73. Voight BF, Kudaravalli S, Wen X, Pritchard JK. 2006. A map of recent positive selection in the human genome. PLoS Biol. 4:e72.
74. Walter K, Min JL, Huang J, Crooks L, Memari Y, McCarthy S, Perry JRB, Xu C, Futema M, Lawson D, et al. 2015. The UK10K project identifies rare variants in health and disease. Nature 526:82.
75. Whitlock MC. 2000. Fixation of new alleles and the extinction of small populations: drift load, beneficial alleles, and sexual selection. Evolution 54:1855-1861.
76. Whitlock MC, Bürger R. 2004. Fixation of new mutations in small populations. In: Ferrière R, Dieckmann U, Couvet D, editors. Evolutionary conservation biology. Cambridge (United Kingdom): Cambridge University Press. p. 155-170.
77. Whitlock MC, Griswold CK, Peters AD. 2003. Compensating for the meltdown: the critical effective size of a population with deleterious and compensatory mutations. Ann Zoo Fenn. 40:169-183.
78. Wojcik GL, Kao WHL, Duggal P. 2015. Relative performance of gene- and pathway-level methods as secondary analyses for genome-wide association studies. BMC Genetics 16
79. Wong GK, Yang Z, Passey DA, Kibukawa M, Paddock M, Liu CR, Bolund L, Yu J. 2003. A population threshold for functional polymorphisms. Genome Res. 13:1873-1879.
80. Xie Q, Wang P, Liu X, Yuan L, Wang L, Zhang C, Li Y, Xing H, Zhi L, Yue Z, et al. 2014. LNK1 and LNK2 are transcriptional coactivators in the Arabidopsis circadian oscillator. Plant Cell 26: 2843-2857.
81. Xue Y, Chen Y, Ayub Q, Huang N, Ball EV, Mort M, Phillips AD, Shaw K, Stenson PD, Cooper DN, et al. 2012. Deleterious- and disease-allele prevalence in healthy individuals: insights from current predictions, mutation databases, and population-scale resequencing. Am J Hum Genet. 91:1022-1032.
82. Zhou L, Bawa R, Holliday JA. 2014. Exome resequencing reveals signatures of demographic and adaptive processes across the genome and range of black cottonwood (Populus trichocarpa). Mol Ecol. 23:2486-2499.
83. Zhou L, Holliday JA. 2012. Targeted enrichment of the black cottonwood (Populus trichocarpa) gene space using sequence capture. Bmc Genomics 13:703.