The utility of PacBio circular consensus sequencing for characterizing complex gene families in non-model organisms

BMC Genomics

Volumn 15, Issue 1, 2014, Pages

  Larsen, Peter A ^a   Heilman, Amy M ^a,b   Yoder, Anne D ^a  

^a DUKE UNIVERSITY   (United States)

^b MAX PLANCK INSTITUTE FOR EVOLUTIONARY ANTHROPOLOGY   (Germany)

Author keywords

Chemosensory genes; Microcebus murinus; Multigene family; Pacific Biosciences; Pheromone detection; Single molecule real time sequencing

Indexed keywords

ARTICLE; CIRCULAR CONSENSUS SEQUENCING; CLUSTER ANALYSIS; CONSENSUS SEQUENCE; DNA SEQUENCE; MICROCEBUS MURINUS; MOUSE LEMUR; MULTIGENE FAMILY; NONHUMAN; NUCLEOTIDE SEQUENCE; SEQUENCE HOMOLOGY; V1R GENE; V2R GENE; ANIMAL; CHEIROGALEIDAE; GENETIC POLYMORPHISM; GENETICS; MOLECULAR GENETICS; OLFACTORY RECEPTOR; PHYLOGENY; PHYSIOLOGY; PROCEDURES; VOMERONASAL ORGAN;

MICROCEBUS MURINUS;

OLFACTORY RECEPTOR;

ANIMALS; BASE SEQUENCE; CHEIROGALEIDAE; CLUSTER ANALYSIS; MOLECULAR SEQUENCE DATA; PHYLOGENY; POLYMORPHISM, GENETIC; RECEPTORS, ODORANT; SEQUENCE ANALYSIS, DNA; VOMERONASAL ORGAN;

EID: 84906842527     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-15-720     Document Type: Article

References (51)

1. Nei M, Rooney AP. Concerted and birth-and-death evolution of multigene families. Annu Rev Genet 2005, 39:121. 10.1146/annurev.genet.39.073003.112240, 1464479, 16285855.
2. Holland PW, Garcia-Ferna`ndez J, Williams NA, Sidow A. Gene duplications and the origins of vertebrate development. Development 1994, 1994:125-133.
3. Amores A, Force A, Yan Y-L, Joly L, Amemiya C, Fritz A, Ho RK, Langeland J, Prince V, Wang Y-L. Zebrafish hox clusters and vertebrate genome evolution. Science 1998, 282:1711-1714.
4. Iwabe N, Kuma K-I, Miyata T. Evolution of gene families and relationship with organismal evolution: rapid divergence of tissue-specific genes in the early evolution of chordates. Mol Biol Evol 1996, 13:483-493. 10.1093/oxfordjournals.molbev.a025609, 8742637.
5. Lundin LG. Evolution of the vertebrate genome as reflected in paralogous chromosomal regions in man and the house mouse. Genomics 1993, 16:1-19. 10.1006/geno.1993.1133, 8486346.
6. Alkan C, Sajjadian S, Eichler EE. Limitations of next-generation genome sequence assembly. Nat Methods 2010, 8:61-65. 3115693, 21102452.
7. Hirsch CN, Robin Buell C. Tapping the Promise of Genomics in Species with Complex, Nonmodel Genomes. Annu Rev Plant Biol 2013, 64:89-110. 10.1146/annurev-arplant-050312-120237, 23451780.
8. Cheung J, Estivill X, Khaja R, MacDonald JR, Lau K, Tsui L-C, Scherer SW. Genome-wide detection of segmental duplications and potential assembly errors in the human genome sequence. Genome Biol 2003, 4:R25. 10.1186/gb-2003-4-4-r25, 154576, 12702206.
9. Strand T, Wang B, Meyer-Lucht Y, Ho¨glund J. Evolutionary history of black grouse major histocompatibility complex class IIB genes revealed through single locus sequence-based genotyping. BMC Genet 2013, 14:29. 3652749, 23617616.
10. Klein J. Natural History of the Major Histocompatibility Complex 1986, New York: Wiley.
11. Garrigan D, Hedrick PW. Perspective: detecting adaptive molecular polymorphism: lessons from the MHC. Evolution 2003, 57:1707-1722. 10.1111/j.0014-3820.2003.tb00580.x, 14503614.
12. Ilmonen P, Penn DJ, Damjanovich K, Morrison L, Ghotbi L, Potts WK. Major histocompatibility complex heterozygosity reduces fitness in experimentally infected mice. Genetics 2007, 176:2501-2508. 10.1534/genetics.107.074815, 1950649, 17603099.
13. Brouwer L, Barr I, Van De POL M, Burke T, Komdeur J, Richardson DS. MHC-dependent survival in a wild population: evidence for hidden genetic benefits gained through extra-pair fertilizations. Mol Ecol 2010, 19:3444-3455. 10.1111/j.1365-294X.2010.04750.x, 20670363.
14. Zhang X, Goodsell J, Norgren RB. Limitations of the rhesus macaque draft genome assembly and annotation. BMC Genomics 2012, 13:206. 10.1186/1471-2164-13-206, 3426473, 22646658.
15. Roberts RJ, Carneiro MO, Schatz MC. The advantages of SMRT sequencing. Genome Biol 2013, 14:405. 10.1186/gb-2013-14-6-405, 3953343, 23822731.
16. Eid J, Fehr A, Gray J, Luong K, Lyle J, Otto G, Peluso P, Rank D, Baybayan P, Bettman B. Real-time DNA sequencing from single polymerase molecules. Science 2009, 323:133-138. 10.1126/science.1162986, 19023044.
17. Travers KJ, Chin C-S, Rank DR, Eid JS, Turner SW. A flexible and efficient template format for circular consensus sequencing and SNP detection. Nucleic Acids Res 2010, 38:e159-e159. 10.1093/nar/gkq543, 2926623, 20571086.
18. Young JM, Massa HF, Hsu L, Trask BJ. Extreme variability among mammalian V1R gene families. Genome Res 2010, 20:10-18. 10.1101/gr.098913.109, 2798821, 19952141.
19. Yang H, Shi P, Zhang Y-P, Zhang J. Composition and evolution of the V2r vomeronasal receptor gene repertoire in mice and rats. Genomics 2005, 86:306-315. 10.1016/j.ygeno.2005.05.012, 16024217.
20. Grus WE, Zhang J. Origin and evolution of the vertebrate vomeronasal system viewed through system-specific genes. Bioessays 2006, 28:709-718. 10.1002/bies.20432, 16850401.
21. Dulac C, Axel R. A novel family of genes encoding putative pheromone receptors in mammals. Cell 1995, 83:195-206. 10.1016/0092-8674(95)90161-2, 7585937.
22. Young JM, Kambere M, Trask BJ, Lane RP. Divergent V1R repertoires in five species: Amplification in rodents, decimation in primates, and a surprisingly small repertoire in dogs. Genome Res 2005, 15:231-240. 10.1101/gr.3339905, 546524, 15653832.
23. Grus WE, Shi P, Zhang Y-P, Zhang J. Dramatic variation of the vomeronasal pheromone receptor gene repertoire among five orders of placental and marsupial mammals. Proc Natl Acad Sci USA 2005, 102:5767-5772. 10.1073/pnas.0501589102, 556306, 15790682.
24. Shi P, Bielawski JP, Yang H, Zhang Y. Adaptive diversification of vomeronasal receptor 1 genes in rodents. J Mol Evol 2005, 60:566-576. 10.1007/s00239-004-0172-y, 15983866.
25. Grus WE, Zhang J. Rapid turnover and species-specificity of vomeronasal pheromone receptor genes in mice and rats. Gene 2004, 340:303-312. 10.1016/j.gene.2004.07.037, 15475172.
26. Delbarco-Trillo J, Burkert B, Goodwin T, Drea C. Night and day: the comparative study of strepsirrhine primates reveals socioecological and phylogenetic patterns in olfactory signals. J Evol Biol 2011, 24:82-98. 10.1111/j.1420-9101.2010.02145.x, 21091564.
27. Irwin MT, Samonds KE, Raharison J-L, Wright PC. Lemur latrines: observations of latrine behavior in wild primates and possible ecological significance. J Mammal 2004, 85:420-427.
28. Andrew RJ, Klopman RB. Urine washing: comparative notes. Prosimian Biology 1974, 303-312. London: Duckworth, Martin RD, Doyle GA, Walker AC.
29. Yoder A, Chan L, dos Reis M, Larsen P, Campbell C, Rasolarison R, Barrett M, Roos C, Kappeler P, Bielawski J, Yang Z. Molecular evolutionary characterization of a novel V1R subfamily in strepsirrhine primates. Genome Biol Evol 2014, 6:213-227. 10.1093/gbe/evu006, 3914689, 24398377.
30. Hohenbrink P, Radespiel U, Mundy NI. Pervasive and ongoing positive selection in the vomeronasal-1 receptor (V1R) repertoire of mouse lemurs. Mol Biol Evol 2012, 29:3807-3816. 10.1093/molbev/mss188, 22821010.
31. Dulac C, Torello AT. Molecular detection of pheromone signals in mammals: from genes to behaviour. Nat Rev Neurosci 2003, 4:551-562. 10.1038/nrn1140, 12838330.
32. Zhang J, Webb DM. Evolutionary deterioration of the vomeronasal pheromone transduction pathway in catarrhine primates. Proc Natl Acad Sci USA 2003, 100:8337-8341. 10.1073/pnas.1331721100, 166230, 12826614.
33. Isogai Y, Si S, Pont-Lezica L, Tan T, Kapoor V, Murthy VN, Dulac C. Molecular organization of vomeronasal chemoreception. Nature 2011, 478:241-245. 10.1038/nature10437, 3192931, 21937988.
34. Steiger SS, Fidler AE, Valcu M, Kempenaers B. Avian olfactory receptor gene repertoires: evidence for a well-developed sense of smell in birds?. Proc R Soc Lond B Biol Sci 2008, 275:2309-2317.
35. Del Punta K, Rothman A, Rodriguez I, Mombaerts P. Sequence diversity and genomic organization of vomeronasal receptor genes in the mouse. Genome Res 2000, 10:1958-1967. 10.1101/gr.10.12.1958, 313053, 11116090.
36. Go Y, Satta Y, Kawamoto Y, Rakotoarisoa G, Randrianjafy A, Koyama N, Hirai H. Frequent segmental sequence exchanges and rapid gene duplication characterize the MHC class I genes in lemurs. Immunogenetics 2003, 55:450-461. 10.1007/s00251-003-0613-6, 14530885.
37. Liang B, Luo M, Scott-Herridge J, Semeniuk C, Mendoza M, Capina R, Sheardown B, Ji H, Kimani J, Ball BT. A comparison of parallel pyrosequencing and sanger clone-based sequencing and its impact on the characterization of the genetic diversity of HIV-1. PLoS ONE 2011, 6:e26745. 10.1371/journal.pone.0026745, 3198814, 22039546.
38. Hughes GM, Gang L, Murphy WJ, Higgins DG, Teeling EC. Using Illumina Next Generation Sequencing technologies to sequence multigene families in de novo species. Mol Ecol Res 2013, 13:510-521.
39. Larsen P, Smith T. Application of circular consensus sequencing and network analysis to characterize the bovine IgG repertoire. BMC Immunol 2012, 13:52. 10.1186/1471-2172-13-52, 3500647, 22978666.
40. Neves LG, Davis JM, Barbazuk WB, Kirst M. Whole-exome targeted sequencing of the uncharacterized pine genome. Plant J 2013, 75:146-156. 10.1111/tpj.12193, 23551702.
41. Sommer S, Courtiol A, Mazzoni CJ. MHC genotyping of non-model organisms using next-generation sequencing: a new methodology to deal with artefacts and allelic dropout. BMC Genomics 2013, 14:1-17. 10.1186/1471-2164-14-1, 3722126, 23323973.
42. Goecks J, Nekrutenko A, Taylor J, Team TG. Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biol 2010, 11:R86. 10.1186/gb-2010-11-8-r86, 2945788, 20738864.
43. Blankenberg D, Kuster GV, Coraor N, Ananda G, Lazarus R, Mangan M, Nekrutenko A, Taylor J. Galaxy: A Web-Based Genome Analysis Tool for Experimentalists. Curr Protoc Mol Biol 2010, 19(10):11-19.10. 21.
44. Giardine B, Riemer C, Hardison RC, Burhans R, Elnitski L, Shah P, Zhang Y, Blankenberg D, Albert I, Taylor J. Galaxy: a platform for interactive large-scale genome analysis. Genome Res 2005, 15:1451-1455. 10.1101/gr.4086505, 1240089, 16169926.
45. Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 2010, 26:2460-2461. 10.1093/bioinformatics/btq461, 20709691.
46. Rodriguez I, Del Punta K, Rothman A, Ishii T, Mombaerts P. Multiple new and isolated families within the mouse superfamily of V1r vomeronasal receptors. Nat Neurosci 2002, 5:134-140. 10.1038/nn795, 11802169.
47. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Ho¨hna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 2012, 61:539-542. 10.1093/sysbio/sys029, 3329765, 22357727.
48. Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2006, 22:2688-2690. 10.1093/bioinformatics/btl446, 16928733.
49. Krzywinski M, Birol I, Jones SJ, Marra MA. Hive plots-rational approach to visualizing networks. Brief Bioinform 2012, 13:627-644. 10.1093/bib/bbr069, 22155641.
50. Librado P, Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 2009, 25:1451-1452. 10.1093/bioinformatics/btp187, 19346325.
51. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28:2731-2739. 10.1093/molbev/msr121, 3203626, 21546353.