Analysis of natural variation reveals neurogenetic networks for Drosophila olfactory behavior

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 3, 2013, Pages 1017-1022

  Swarup, Shilpa ^a,b   Huang, Wen ^a   Mackay, Trudy F C ^a   Anholt, Robert R H ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b MONSANTO COMPANY   (United States)

Author keywords

Behavioral genetics; Chemosensation; Genetic architecture

Indexed keywords

ARTICLE; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; FEMALE; GENE EXPRESSION; GENE REPLICATION; GENE SEQUENCE; GENETIC ASSOCIATION; GENETIC VARIABILITY; INSECT GENETICS; INTRACELLULAR SIGNALING; MALE; NERVE CELL DIFFERENTIATION; NERVE CELL NETWORK; NONHUMAN; OLFACTORY SYSTEM; PRIORITY JOURNAL; QUANTITATIVE TRAIT LOCUS; SINGLE NUCLEOTIDE POLYMORPHISM;

ANIMALS; BEHAVIOR, ANIMAL; DROSOPHILA MELANOGASTER; FEMALE; GENE REGULATORY NETWORKS; GENES, INSECT; GENETIC ASSOCIATION STUDIES; GENETIC VARIATION; GENETICS, BEHAVIORAL; GENOME-WIDE ASSOCIATION STUDY; HUMANS; MALE; MODELS, GENETIC; MODELS, NEUROLOGICAL; NEUROGENESIS; POLYMORPHISM, SINGLE NUCLEOTIDE; QUANTITATIVE TRAIT LOCI; SMELL;

DROSOPHILA MELANOGASTER;

EID: 84872591709     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1220168110     Document Type: Article

References (54)

1. Manolio TA, et al. (2009) Finding the missing heritability of complex diseases. Nature 461(7265):747-753.
2. Visscher PM, Brown MA, McCarthy MI, Yang J (2012) Five years of GWAS discovery. Am J Hum Genet 90(1):7-24.
3. Moore JH, Williams SM (2009) Epistasis and its implications for personal genetics. Am J Hum Genet 85(3):309-320.
4. Zuk O, Hechter E, Sunyaev SR, Lander ES (2012) The mystery of missing heritability: Genetic interactions create phantom heritability. Proc Natl Acad Sci USA 109(4):1193-1198.
5. Wang K, Li M, Hakonarson H (2010) Analysing biological pathways in genome-wide association studies. Nat Rev Genet 11(12):843-854.
6. Califano A, Butte AJ, Friend S, Ideker T, Schadt E (2012) Leveraging models of cell regulation and GWAS data in integrative network-based association studies. Nat Genet 44(8):841-847.
7. Jia P, et al.; International Schizophrenia Consortium (2012) Network-assisted investigation of combined causal signals from genome-wide association studies in schizophrenia. PLOS Comput Biol 8(7):e1002587.
8. Pandey A, et al. (2012) Epistasis network centrality analysis yields pathway replication across two GWAS cohorts for bipolar disorder. Transcult Psychiatry 2:e154.
9. Mackay TFC, et al. (2012) The Drosophila melanogaster Genetic Reference Panel. Nature 482(7384):173-178.
10. Venken KJ, Bellen HJ (2012) Genome-wide manipulations of Drosophila melanogaster with transposons, Flp recombinase, and ΦC31 integrase. Methods Mol Biol 859:203-228.
11. Huang W, et al. (2012) Epistasis dominates the genetic architecture of Drosophila quantitative traits. Proc Natl Acad Sci USA 109(39):15553-15559.
12. Su CY, Menuz K, Carlson JR (2009) Olfactory perception: Receptors, cells, and circuits. Cell 139(1):45-59.
13. Clyne PJ, et al. (1999) A novel family of divergent seven-transmembrane proteins: Candidate odorant receptors in Drosophila. Neuron 22(2):327-338. (Pubitemid 29109666)
14. Vosshall LB, Amrein H, Morozov PS, Rzhetsky A, Axel R (1999) A spatial map of olfactory receptor expression in the Drosophila antenna. Cell 96(5):725-736. (Pubitemid 29122814)
15. Gao Q, Chess A (1999) Identification of candidate Drosophila olfactory receptors from genomic DNA sequence. Genomics 60(1):31-39. (Pubitemid 29422811)
16. Hallem EA, Carlson JR (2006) Coding of odors by a receptor repertoire. Cell 125(1):143-160.
17. Benton R, Vannice KS, Gomez-Diaz C, Vosshall LB (2009) Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila. Cell 136(1):149-162.
18. Clyne PJ, Warr CG, Carlson JR (2000) Candidate taste receptors in Drosophila. Science 287(5459):1830-1834.
19. Scott K, et al. (2001) A chemosensory gene family encoding candidate gustatory and olfactory receptors in Drosophila. Cell 104(5):661-673. (Pubitemid 32241017)
20. Hekmat-Scafe DS, Scafe CR, McKinney AJ, Tanouye MA (2002) Genome-wide analysis of the odorant-binding protein gene family in Drosophila melanogaster. Genome Res 12(9):1357-1369.
21. Galindo K, Smith DP (2001) A large family of divergent Drosophila odorant-binding proteins expressed in gustatory and olfactory sensilla. Genetics 159(3):1059-1072. (Pubitemid 34033451)
22. Anholt RRH, Lyman RF, Mackay TFC (1996) Effects of single P-element insertions on olfactory behavior in Drosophila melanogaster. Genetics 143(1):293-301. (Pubitemid 26136992)
23. Sambandan D, Yamamoto A, Fanara JJ, Mackay TFC, Anholt RRH (2006) Dynamic genetic interactions determine odor-guided behavior in Drosophila melanogaster. Genetics 174(3):1349-1363.
24. Fedorowicz GM, Fry JD, Anholt RRH, Mackay TFC (1998) Epistatic interactions between smell-impaired loci in Drosophila melanogaster. Genetics 148(4):1885-1891. (Pubitemid 28180713)
25. Mackay TFC, Hackett JB, Lyman RF, Wayne ML, Anholt RRH (1996) Quantitative genetic variation of odor-guided behavior in a natural population of Drosophila melanogaster. Genetics 144(2):727-735. (Pubitemid 26325863)
26. Wang P, Lyman RF, Shabalina SA, Mackay TFC, Anholt RRH (2007) Association of polymorphisms in odorant-binding protein genes with variation in olfactory response to benzaldehyde in Drosophila. Genetics 177(3):1655-1665. (Pubitemid 350277059)
27. Wang P, Lyman RF, Mackay TFC, Anholt RRH (2010) Natural variation in odorant recognition among odorant-binding proteins in Drosophila melanogaster. Genetics 184(3):759-767.
28. Arya GH, et al. (2010) Natural variation, functional pleiotropy and transcriptional contexts of odorant binding protein genes in Drosophila melanogaster. Genetics 186 (4):1475-1485.
29. Rollmann SM, et al. (2010) Odorant receptor polymorphisms and natural variation in olfactory behavior in Drosophila melanogaster. Genetics 186(2):687-697.
30. Ehrenreich IM, et al. (2010) Dissection of genetically complex traits with extremely large pools of yeast segregants. Nature 464(7291):1039-1042.
31. Paré G, Cook NR, Ridker PM, Chasman DI (2010) On the use of variance per genotype as a tool to identify quantitative trait interaction effects: A report from the Women's Genome Health Study. PLoS Genet 6(6):e1000981.
32. Struchalin MV, Dehghan A, Witteman JC, van Duijn C, Aulchenko YS (2010) Variance heterogeneity analysis for detection of potentially interacting genetic loci: Method and its limitations. BMC Genet 11:92.
33. Swarup S, et al. (2012) Extensive epistasis for olfactory behaviour, sleep and waking activity in Drosophila melanogaster. Genet Res (Camb) 94(1):9-20.
34. Swarup S, Williams TI, Anholt RRH (2011) Functional dissection of Odorant binding protein genes in Drosophila melanogaster. Genes Brain Behav 10(6):648-657.
35. Weber AL, et al. (2012) Genome-wide association analysis of oxidative stress resistance in Drosophila melanogaster. PLoS ONE 7(4):e34745.
36. Jordan KW, et al. (2012) Genome-wide association for sensitivity to chronic oxidative stress in Drosophila melanogaster. PLoS ONE 7(6):e38722.
37. Liu L, et al. (2003) Contribution of Drosophila DEG/ENaC genes to salt taste. Neuron 39(1):133-146. (Pubitemid 36830954)
38. Edwards AC, Zwarts L, Yamamoto A, Callaerts P, Mackay TFC (2009) Mutations in many genes affect aggressive behavior in Drosophila melanogaster. BMC Biol 7:29.
39. Bellen HJ, et al. (2011) The Drosophila gene disruption project: Progress using transposons with distinctive site specificities. Genetics 188(3):731-743.
40. Antonov AV, Schmidt EE, Dietmann S, Krestyaninova M, Hermjakob H (2010) R spider: A network-based analysis of gene lists by combining signaling and metabolic pathways from Reactome and KEGG databases. Nucleic Acids Res 38(Web Server issue):W78-83.
41. Koizumi K, et al. (2007) RNA interference screen to identify genes required for Drosophila embryonic nervous system development. Proc Natl Acad Sci USA 104(13):5626-5631. (Pubitemid 47175731)
42. Pipes GC, Lin Q, Riley SE, Goodman CS (2001) The Beat generation: A multigene family encoding IgSF proteins related to the Beat axon guidance molecule in Drosophila. Development 128(22):4545-4552. (Pubitemid 33130434)
43. Moehring AJ, Mackay TFC (2004) The quantitative genetic basis of male mating behavior in Drosophila melanogaster. Genetics 167(3):1249-1263. (Pubitemid 39045633)
44. Zhu S, et al. (2006) Gradients of the Drosophila Chinmo BTB-zinc finger protein govern neuronal temporal identity. Cell 127(2):409-422. (Pubitemid 44572379)
45. Dekanty A, Lavista-Llanos S, Irisarri M, Oldham S, Wappner P (2005) The insulin-PI3K/TOR pathway induces a HIF-dependent transcriptional response in Drosophila by promoting nuclear localization of HIF-alpha/Sima. J Cell Sci 118(Pt 23):5431-5441. (Pubitemid 43079285)
46. Levene H (1960) Contributions to Probability and Statistics: Essays in Honor of Harold Hotelling, eds Olkin I, et al. (Stanford Univ Press, Stanford, CA), pp 278-292.
47. Wang Y, et al. (2001) Genetic manipulation of the odor-evoked distributed neural activity in the Drosophila mushroom body. Neuron 29(1):267-276. (Pubitemid 32108738)
48. Honegger KS, Campbell RA, Turner GC (2011) Cellular-resolution population imaging reveals robust sparse coding in the Drosophila mushroom body. J Neurosci 31(33):11772-11785.
49. Xia S, Tully T (2007) Segregation of odor identity and intensity during odor discrimination in Drosophila mushroom body. PLoS Biol 5(10):e264.
50. Wong AM, Wang JW, Axel R (2002) Spatial representation of the glomerular map in the Drosophila protocerebrum. Cell 109(2):229-241. (Pubitemid 34518261)
51. Kauffman S (1993) The Origins of Order: Self-Organization and Selection in Evolution (Oxford Univ Press, Oxford, UK).
52. Greene CS, Penrod NM, Williams SM, Moore JH (2009) Failure to replicate a genetic association may provide important clues about genetic architecture. PLoS ONE 4(6):e5639.
53. McQuilton P, St Pierre SE, Thurmond J; FlyBase Consortium (2012) FlyBase 101 - the basics of navigating FlyBase. Nucleic Acids Res 40(Database issue):D706-D714.
54. McKenna A, et al. (2010) The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20(9):1297-1303.