Genetic variation in Drosophila melanogaster resistance to infection: A comparison across bacteria

Genetics

Volumn 174, Issue 3, 2006, Pages 1539-1554

  Lazzaro, Brian P ^a,b   Sackton, Timothy B ^b   Clark, Andrew G ^b  

^a Plant Breeding and Genetics Section in the School of Integrative Plant Science   (United States)

^b Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; ENTEROCOCCUS FAECALIS; GENETIC VARIABILITY; GENOTYPE PHENOTYPE CORRELATION; IMMUNE RESPONSE; IMMUNOCOMPETENCE; INFECTION RESISTANCE; LACTOCOCCUS LACTIS; NONHUMAN; PRIORITY JOURNAL; SERRATIA MARCESCENS; SINGLE NUCLEOTIDE POLYMORPHISM;

ANIMALS; BACTERIA; BACTERIAL INFECTIONS; DROSOPHILA MELANOGASTER; ENTEROCOCCUS FAECALIS; EPISTASIS, GENETIC; GENES, INSECT; GENETIC MARKERS; HAPLOTYPES; HEMOLYMPH; IMMUNITY, NATURAL; IMMUNOCOMPETENCE; LACTOCOCCUS LACTIS; POLYMORPHISM, SINGLE NUCLEOTIDE; PROVIDENCIA; SERRATIA MARCESCENS; VARIATION (GENETICS);

BACTERIA (MICROORGANISMS); DROSOPHILA MELANOGASTER; ENTEROCOCCUS FAECALIS; HEXAPODA; LACTOCOCCUS LACTIS; NEGIBACTERIA; POSIBACTERIA; PROVIDENCIA; SERRATIA MARCESCENS;

EID: 33751326790     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.105.054593     Document Type: Article

References (48)

1. ADAMS, M. D., S. E. CELNIKER, R. A. HOLT, C. A. EVANS, J. D. GOCAYNE et al., 2000 The genome sequence of Drosophila melanogaster. Science 287: 2185-2195.
2. AZAMBUJA, P., E. S. GARCIA, C. B. MELLO and D. FEDER, 1997 Immune responses in Rhodnius prolixus: influence of nutrition and ecdysone. J. Insect Physiol. 43: 513-519.
3. BEGUN, D. J., and P. WHITLEY, 2000 Adaptive evolution of relish, a Drosophila NF-κB/IκB protein. Genetics 154: 1231-1238.
4. CHOE, K. M., H. LEE and K. V. ANDERSON, 2005 Drosophila peptidoglycan recognition protein LC (PGRP-LC) acts as a signal-transducing innate immune receptor. Proc. Natl. Acad. Sci. USA 102: 1122-1126.
5. CLARK, A. G., and L. WANG, 1997 Molecular population genetics of Drosophila immune system genes. Genetics 147: 713-724.
6. DATE, A., Y. SATTA, N. TAKAHATA and S. I. CHIGUSA, 1998 Evolutionary history and mechanism of the Drosophila cecropin gene family. Immunogenetics 47: 417-429.
7. CHURCHILL, G. A., and R. W. DOERGE, 1994 Empirical threshold values for quantitative trait mapping. Genetics 138: 963-971.
8. ENGSTRÖM, Y., 1999 Induction and regulation of antimicrobial peptides in Drosophila. Dev. Comp. Immunol. 23: 345-358.
9. FILIPE, S. R., A. TOMASZ and P. LIGOXYGAKIS, 2005 Requirements of peptidoglycan structure that allow detection by the Drosophila Toll pathway. EMBO Rep. 6: 327-333.
10. GENISSEL, A., T. PASTINEN, A. DOWELL, T. F. MACKAY and A. D. LONG, 2004 No evidence for an association between common nonsynonymous polymorphisms in delta and bristle number variation in natural and laboratory populations of Drosophila melanogaster. Genetics 166: 291-306.
11. GOBERT, V., M. GOTTAR, A. A. MATSKEVICH, S. RUTSCHMANN, J. ROYET et al., 2003 Dual activation of the Drosophila toll pathway by two pattern recognition receptors. Science 302: 2126-2130.
12. HEDENGREN, M., K. BORGE and D. HULTMARK, 2000 Expression and evolution of the Drosophila/Diptericin gene family. Biochem. Biophys. Res. Commun. 279: 574-581.
13. HEDENGREN-OLCOTT, M., M. C. OLCOTT, D. T. MOONEY, S. EKENGREN, B. L. GELLER et al., 2004 Differential activation of the NF-kappaB-like factors Relish and Dif in Drosophila melanogaster by fungi and Gram-positive bacteria. J. Biol. Chem. 279: 21121-21127.
14. IMLER, J.-L., and P. BULET, 2005 Antimicrobial peptides in Drosophila: structures, activities and gene regulation. Chem. Immunol. Allergy 86: 1-21.
15. JIGGINS, F. M., and G. D. HURST, 2003 The evolution of parasite recognition genes in the innate immune system: purifying selection on Drosophila melanogaster peptidoglycan recognition proteins. J. Mol. Evol. 57: 598-605.
16. KOELLA, J. C., and F. L. SORENSE, 2002 Effect of adult nutrition on the melanization immune response of the malaria vector Anopheles stephensi. Med. Vet. Entomol. 16: 316-320.
17. KRAAIJEVELD, A. R., and H. C. GODFRAY, 1997 Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Nature 389: 278-280.
18. KUMAR, S., G. K. CHRISTOPHIDES, R. CANTERA, B. CHARLES, Y. S. HAN et al., 2003 The role of reactive oxygen species on Plasmodium melanotic encapsulation in Anopheles gambiae. Proc. Natl. Acad. Sci. USA 100: 14139-14144.
19. LAZZARO, B. P., 2002 A population and quantitative genetic analysis of the Drosophila melanogaster antibacterial immune response. Ph.D. Thesis, Pennsylvania State University, University Park, PA.
20. LAZZARO, B. P., 2005 Elevated polymorphism and divergence in the class C scavenger receptors of Drosophila melanogaster and D. simulans. Genetics 169: 2023-2034.
21. LAZZARO, B. P., and A. G. CLARK, 2001 Evidence for recurrent paralogous gene conversion and exceptional allelic divergence in the Attacin genes of Drosophila melanogaster. Genetics 159: 659-671.
22. LAZZARO, B. P., and A. G. CLARK, 2003 Molecular population genetics of inducible antibacterial peptide genes in Drosophila melanogaster. Mol. Biol. Evol. 20: 914-923.
23. LAZZARO, B. P., B. K. SCEURMAN and A. G. CLARK, 2004 Genetic basis of natural variation in D. melanogaster antibacterial immunity. Science 303: 1873-1876.
24. LECLERC, V., and J.-M. REICHHART, 2004 The immune response of Drosophila melanogaster. Immunol. Rev. 198: 59-71.
25. LIGOXYGAKIS, P., P. BULET and J.-M. REICHHART, 2002 Critical evaluation of the role of the Toll-like receptor 18-Wheeler in the host defense of Drosophila. EMBO Rep. 3: 666-673.
26. LUO, C., B. SHEN, J. L. MANLEY and L. ZHENG, 2001 Tehao functions in the Toll pathway in Drosophila melanogaster: possible roles in development and innate immunity. Insect Mol. Biol. 10: 457-464.
27. LEMAITRE, B., E. NICOLAS, L. MICHAUT, J.-M. REICHHART and J. A. HOFFMANN, 1996 The dorsoventral regulatory gene cassette spatzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 86: 973-983.
28. LEMAITRE, B., J.-M. REICHHART and J. A. HOFFMANN, 1997 Drosophila host defense: differential induction of antimicrobial peptide genes after infection by various classes of microorganisms. Proc. Natl. Acad. Sci. USA 94: 14614-14619.
29. MACDONALD, S. J., and A. D. LONG, 2004 A potential regulatory polymorphism upstream of hairy is not associated with bristle number variation in wild-caught Drosophila. Genetics 167: 2127-2131.
30. MACDONALD, S. J., T. PASTINEN and A. D. LONG, 2005 The effect of polymorphisms in the enhancer of split gene complex on bristle number variation in a large wild-caught cohort of Drosophila melanogaster. Genetics 171: 1741-1756.
31. MACKAY, T. F., and R. F. LYMAN, 2005 Drosophila bristles and the nature of quantitative genetic variation. Philos. Trans. R. Soc. Lond. B Biol. Sci. 360: 1513-1527.
32. MCKEAN, K. A., and L. NUNNEY, 2001 Increased sexual activity reduces male immune function in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 98: 7904-7909.
33. MCKEAN, K. A., and L. NUNNEY, 2005 Bateman's principle and immunity: phenotypically plastic reproductive strategies predict changes in immunological sex differences. Evolution 59: 1510-1517.
34. NETER, J., M. H. KUTNER, C. J. NACHTSHEIM and W. WASSERMAN, 1990 Applied Linear Statistical Models, Ed. 4. McGraw-Hill, Chicago.
35. PALSSON, A., J. DODGSON, I. DWORKIN and G. GIBSON, 2005 Tests for the replication of an association between Egfr and natural variation in Drosophila melanogaster wing morphology. BMC Genet. 6: 44.
36. PILI-FLOURY, S., F. LEULIER, K. TAKAHASHI, K. SAIGO, E. SAMAIN et al., 2004 In vivo RNA interference analysis reveals an unexpected role for GNBP1 in the defense against Gram-positive bacterial infection in Drosophila adults. J. Biol. Chem. 279: 12848-12853.
37. RÄMET, M., A. PEARSON, P. MANFRUELLI, X. LI, H. KOZIEL et al., 2001 Drosophila scavenger receptor CI is a pattern recognition receptor for bacteria. Immunity 15: 1027-1038.
38. RAMOS-ONSINS, S., and M. AGUADÉ, 1998 Molecular evolution of the Cecropin multigene family in Drosophila. functional genes vs. pseudogenes. Genetics 150: 157-171.
39. SCHLENKE, T. A., and D. J. BEGUN, 2003 Natural selection drives Drosophila immune system evolution. Genetics 164: 1471-1480.
40. STENBAK, C. R., J. H. RYU, F. LEULIER, S. PILI-FLOURY, C. PARQUET et al., 2004 Peptidoglycan molecular requirements allowing detection by the Drosophila immune deficiency pathway. J. Immunol. 173: 7339-7348.
41. STOREY, J. D., 2002 A direct approach to false discovery rates. J. R. Stat. Soc. B 64: 479-498.
42. STOREY, J. D., and R. TIBSHIRANI, 2003 Statistical significance for genome-wide experiments. Proc. Natl. Acad. Sci. USA 100: 9440-9445.
43. SUWANCHAICHINDA, C., and S. M. PASKEWITZ, 1998 Effects of larval nutrition, adult body size, and adult temperature on the ability of Anopheles gambiae (Diptera: Culicidae) to melanize sephadex beads. J. Med. Entomol. 35: 157-161.
44. TAUSZIG, S., E. JOUANGUY, J. A. HOFFMANN and J.-L. IMLER, 2000 Toll-related receptors and the control of antimicrobial peptide expression in Drosophila. Proc. Natl. Acad. Sci. USA 97: 10520-10525.
45. TAKEHANA, A., T. YANO, S. MITA, A. KOTANI, Y. OSHIMA et al., 2004 Peptidoglycan recognition protein (PGRP)-LE and PGRP-LC act synergistically in Drosophila immunity. EMBO J. 23: 4690-4700.
46. VASS, E., and A. J. NAPPI, 1998 The effects of dietary yeast on the cellular immune response of Drosophila melanogaster against the larval parasitoid, Leptopilina boulardi. J. Parasitol. 84: 870-872.
47. WERNER, T., K. BORGE-RENBERG, P. MELLROTH, H. STEINER and D. HULTMARK, 2003 Functional diversity of the Drosophila PGRP-LC gene cluster in the response to lipopolysaccharide and peptidoglycan. J. Biol. Chem. 278: 26319-26322.
48. WILLIAMS, M. J., A. RODRIGUEZ, D. A. KIMBRELL and E. D. ELDON, 1997 The 18-wheeler mutation reveals complex antibacterial gene regulation in Drosophila host defense. EMBO J. 16: 6120-6130.