Proteomic Characterization of Inbreeding-Related Cold Sensitivity in Drosophila melanogaster

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Vermeulen, Cornelis J ^a,b   Pedersen, Kamilla S ^c,g   Beck, Hans C ^d   Petersen, Jørgen ^e   Gagalova, Kristina Kirilova ^b,f   Loeschcke, Volker ^a  

^a AARHUS UNIVERSITY   (Denmark)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

^c DANISH INSTITUTE OF AGRICULTURAL SCIENCES   (Denmark)

^d ODENSE UNIVERSITY HOSPITAL   (Denmark)

^e UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^f UNIVERSITY OF BOLOGNA   (Italy)

^g DANISH TECHNOLOGICAL INSTITUTE   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

HEXOSE; LIPID; MESSENGER RNA; PYRUVIC ACID;

ARTICLE; CARBOHYDRATE METABOLISM; CG18067 GENE; COLD SENSITIVITY; COLD TOLERANCE; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; FEMALE; GENE; GENE EXPRESSION; INBREEDING; LETHALITY; MALE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEOMICS; UPREGULATION;

ANIMALS; COLD TEMPERATURE; COLD-SHOCK RESPONSE; DROSOPHILA MELANOGASTER; FEMALE; GENE ONTOLOGY; GLUCONEOGENESIS; HEXOSES; INBREEDING; INSECT PROTEINS; MALE; PRINCIPAL COMPONENT ANALYSIS; PROTEOMICS; TRANSCRIPTOME;

DROSOPHILA MELANOGASTER;

EID: 84877080451     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0062680     Document Type: Article

References (52)

1. Charlesworth D, Willis JH, (2009) The genetics of inbreeding depression. Nat Rev Genet 10: 783-796.
2. Charlesworth B, Charlesworth D, (1999) The genetic basis of inbreeding depression. Genet Res 74(3): 329-40.
3. Bijlsma R, Bundgaard J, Boerema AC, (2000) Does inbreeding affect the extinction risk of small populations? predictions from Drosophila. J Evol Biol 13: 502-514.
4. Armbruster P, Reed D, (2005) Inbreeding depression in benign and stressful environments. Heredity 95: 235-242.
5. Kristensen TN, Sørensen P, Pedersen KS, Kruhøffer M, Loeschcke V, (2006) Inbreeding by environment interactions affect gene expression in Drosophila melanogaster. Genetics 173: 1329-1336.
6. Kristensen TN, Barker JSF, Pedersen KS, Loeschcke V, (2008) Extreme temperatures increase the deleterious consequences of inbreeding under laboratory and semi-natural conditions. Proc Roy Soc B Biol Sci 275: 2055-2061.
7. Ouborg NJ, Pertoldi C, Loeschcke V, Bijlsma RK, Hedrick PW, (2010) Conservation genetics in transition to conservation genomics. Trends Genet 26(4): 177-187.
8. Kristensen TN, Pedersen KS, Vermeulen CJ, Loeschcke V, (2010) Research on inbreeding in the 'omic' era. Trends Ecol Evol 25(1): 44-52.
9. Paige KN, (2010) The functional genomics of inbreeding depression: A new approach to an old problem. Bioscience 60(4): 267-277.
10. Chevalier F, Martin O, Rofidal V, Devauchelle AD, Barteau S, et al. (2004) Proteomic analyzation of natural variation between Arabidopsis ecotypes. Proteomics 4: 1372-1381.
11. Kültz D, (2005) Molecular and evolutionary basis of the cellular stress response. Annu Rev Physiol 67: 225-257.
12. Biron DG, Loxhale HD, Ponton F, Moura H, Marche L, et al. (2006) Population proteomics: an emerging discipline to study metapopulation ecology. Proteomics 6: 1712-1715.
13. Pedersen KS, Codrea MC, Vermeulen CJ, Loeschcke V, Bendixen E, (2010) Proteomic characterization of a temperature-sensitive conditional lethal in Drosophila melanogaster. Heredity 104(2): 125-134.
14. Kristensen TN, Sørensen P, Kruhøffer M, Pedersen KS, Loeschcke V, (2005) Genome-wide analysis on inbreeding effects on gene expression in Drosophila melanogaster. Genetics 171(1): 157-167.
15. Pedersen KS, Kristensen TN, Loeschcke V, Petersen BO, Duus JØ, et al. (2008) Metabolomic signatures of inbreeding at benign and stressful temperatures in Drosophila melanogaster. Genetics 180(2): 1233-1243.
16. Ayroles JF, Hughes KA, Rowe KC, Reedy MM, Rodriguez-Zas SL, et al. (2009) A genomewide assessment of inbreeding depression: gene number, function and mode of action. Conserv Biol 23: 920-930.
17. Vermeulen CJ, Bijlsma R, Loeschcke V, (2008) QTL mapping of inbreeding related cold sensitivity and conditional lethality in Drosophila melanogaster. J Evol Biol 21: 1236-1244.
18. Partridge L, (2010) The new biology of ageing. Phil Trans R Soc B 365: 147-154.
19. Vermeulen CJ, Bijlsma R, (2004) Changes in mortality patterns and temperature dependence of life span in Drosophila melanogaster caused by inbreeding. Heredity 92: 275-281.
20. Flybase. Available: http://flybase.org/. Accessed 2013 April 2.
21. Tweedie S, Ashburner M, Falls K, Leyland P, McQuilton P, et al. (2009) FlyBase: enhancing Drosophila Gene Ontology annotations. Nucleic Acids Res 37: D555-D559.
22. DAVID: Database for Annotation, Visualization and Integrated Discovery. Available: http://david.abcc.ncifcrf.gov/. Accessed 2013 April 2.
23. Dennis G Jr, Sherman BT, Hosack DA, Yang J, Gao W, et al. (2003) DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol 4(5): P3.
24. Huang DW, Sherman BT, Lempicki RA, (2009) Systematic and integrative analysis of large gene lists using DAVID Bioinformatics Resources. Nature Protoc 4(1): 44-57.
25. Li A, Denlinger DL, (2008) Rapid cold hardening elicits changes in brain protein profiles of the flesh fly, Sarcophaga crassipalpis. Insect Mol Biol 17(5): 565-572.
26. Colinet H, Nguyen TTA, Cloutier C, Michaud D, Hance T, (2007) Proteomic profiling of a parasitic wasp exposed to constant and fluctuating cold exposure. Insect Biochem Mol Biol 37(11): 1177-1188.
27. Beller M, Riedel D, Jänsch L, Dieterich G, Wehland J, et al. (2006) Characterization of the Drosophila lipid droplet subproteome. Mol Cell Proteomics 5(6): 1082-1094.
28. Rogers S, Girolami M, Kolch W, Waters KM, Liu T, et al. (2008) Investigating the correspondence between transcriptomic and proteomic expression profiles using coupled cluster models. Bioinformatics 24(24): 2894-2900.
29. Sørensen JG, Nielsen MM, Loeschcke V, (2007) Gene expression profile analysis of Drosophila melanogaster selected for resistance to environmental stressors. J Evol Biol 20: 1624-1636.
30. Telonis-Scott M, Hallas R, McKechnie SW, Wee CW, Hoffmann AA, (2009) Selection for cold resistance alters gene transcript levels in Drosophila melanogaster. J Insect Physiol 55: 549-555.
31. Sarup P, Sørensen JG, Kristensen TN, Hoffmann AA, Loeschcke V, et al. (2011) Candidate Genes Detected in Transcriptome Studies Are Strongly Dependent on Genetic Background. PLoS ONE 6(1): e15644.
32. Zhang J, Marshall KE, Westwood JT, Clark MS, Sinclair BJ, (2011) Divergent transcriptomic responses to repeated and single cold exposures in Drosophila melanogaster. J Exp Biol 214(23): 4021-4029.
33. Mackay TFC, (2009) Mutations and quantitative genetic variation: lessons from Drosophila. Phil Trans R Soc B 365: 1229-1239.
34. Sawyer SA, Parsch J, Zhang Z, Hartl DL, (2007) Prevalence of positive selection among nearly neutral amino acid replacements in Drosophila. Proc Natl Acad Sci USA 104(16): 6504-6510.
35. Doucet D, Walker VK, Qin W, (2009) The bugs that came in from the cold: Molecular adaptations to low temperatures in insects. Cell Mol Life Sci 66(8): 1404-1418.
36. Overgaard J, Sørensen JG, Petersen SO, Loeschcke V, Holmstrup M, (2005) Changes in membrane lipid composition following rapid cold hardening in Drosophila melanogaster. J Insect Physiol 51(11): 1173-1182.
37. Overgaard J, Malmendal A, Sørensen JG, Bundy JG, Loeschcke V, et al. (2007) Metabolomic profiling of rapid cold hardening and cold shock in Drosophila melanogaster. J Insect Physiol 53(12): 1218-1232.
38. Teets NM, Peyton JT, Ragland GJ, Colinet H, Renault D, et al. (2012) Combined transcriptomic and metabolomic approach uncovers molecular mechanisms of cold tolerance in a temperate flesh fly. Physiol Genomics 44(15): 764-777.
39. García C, Ávila V, Quesada H, Caballero A, (2012) Gene-expression changes caused by inbreeding protect against inbreeding depression in Drosophila. Genetics 192(1): 161-172.
40. Fox CW, Reed DH, (2011) Inbreeding depression increases with environmental stress: an experimental study and meta-analysis. Evolution 65(1): 246-258.
41. Mikkelsen K, Loeschcke V, Kristensen TN, (2011) Trait specific consequences of fast and slow inbreeding: lessons from captive populations of Drosophila melanogaster. Conserv Genet 11(2): 479-488.
42. Dierks A, Hoffmann B, Bauerfeind SS, Fisher K, (2012) Effects of inbreeding on life history and thermal performance in the tropical butterfly Bicyclus anynana. Pop Ecol 54(1): 83-90.
43. Reed DH, Fox CW, Enders LS, Kristensen TN, (2012) Inbreeding-stress interactions: evolutionary and conservation consequences. Ann NY Acad Sci 1256: 33-48.
44. Vermeulen CJ, Bijlsma R, (2004) Characterization of conditionally expressed mutants affecting age-specific survival in inbred lines of Drosophila melanogaster: lethal conditions and temperature sensitive periods. Genetics 167: 1241-1248.
45. Candiano G, Bruschi M, Musante L, Santucci L, Ghiggeri GM, et al. (2004) Blue silver: a very sensitive colloidal Coomassie G-250 staining for proteome analysis. Electrophoresis 25: 1327-1333.
46. R Development Core Team (2009) R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria. ISBN 3-900051-07-0. Available: http://www.R-project.org. Accessed 2013 April 2.
47. Troyanskaya O, Cantor M, Sherlock G, Brown P, Hastie T, et al. (2001) Missing value estimation methods for DNA microarrays. Bioinformatics 17(6): 520-525.
48. Smyth GK (2004) Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3(1):Article 3.
49. Smyth GK (2005) Limma: linear models for microarray data. In: Gentleman R, Carey V, Dudoit S, Irizarry R, Huber W, editors. Bioinformatics and Computational Biology Solutions using R and Bioconductor. Springer New York. 397-420.
50. Ritz C, Spiess AN, (2008) qpcR: An R package for sigmoidal model selection in quantitative real-time polymerase chain reaction analysis. Bioinformatics 24(13): 1549-1551.
51. Ramakers C, Ruijter JM, Lekanne Deprez RH, Moorman AFM, (2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett 339(1): 62-66.
52. Ruijter JM, Ramakers C, Hoogaars WMH, Karlen Y, Bakker O, et al. (2009) Amplification efficiency: Linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Res 37(6): e45.