Genetic variation in senescence marker protein-30 is associated with natural variation in cold tolerance in Drosophila

Genetics Research

Volumn 92, Issue 2, 2010, Pages 103-113

  Clowers, Katie J ^a,c   Lyman, Richard F ^b   MacKay, Trudy F C ^b   Morgan, Theodore J ^a  

^a KANSAS STATE UNIVERSITY   (United States)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; REGUCALCIN; DROSOPHILA PROTEIN; SIGNAL PEPTIDE;

ARTICLE; COLD STRESS; COLD TOLERANCE; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; FEMALE; GENE LOCUS; GENETIC POLYMORPHISM; GENETIC TRAIT; GENETIC VARIABILITY; HOMEOSTASIS; INBRED STRAIN; MOLECULAR EVOLUTION; NATURAL POPULATION; NONHUMAN; PHENOTYPIC VARIATION; POPULATION; REGULATORY MECHANISM; UNITED STATES; ADAPTATION; ANIMAL; COLD; GENE; GENETICS; PHENOTYPE;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; COLD TEMPERATURE; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EVOLUTION, MOLECULAR; GENES, INSECT; GENETIC VARIATION; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; PHENOTYPE; POLYMORPHISM, GENETIC;

EID: 77954498909     PISSN: 00166723     EISSN: 14695073     Source Type: Journal    
DOI: 10.1017/S0016672310000108     Document Type: Article

References (54)

1. Anderson, A. R., Collinge, J. E., Hoffmann, A. A., Kellett, M. & McKechnie, S. W. (2003). Thermal tolerance tradeoffs associated with the right arm of chromosome 3 and marked by the hsr-omega gene in Drosophila melanogaster. Heredity 90, 195-202.
2. Anderson, A. R., Hoffmann, A. A. & McKechnie, S. W. (2005). Response to selection for rapid chill-coma recovery in Drosophila melanogaster: physiology and life-history traits. Genetical Research 85, 15-22.
3. Ayrinhac, A., Debat, V., Gibert, P., Kister, A. G., Legout, H., Moreteau, B., Vergillno, R. & David, J. R. (2004). Cold adaptation in geographical populations of Drosophila melanogaster: phenotypic plasticity is more important than genetic variability. Functional Ecology 18, 700-706.
4. Ayroles, J. F., Carbone, M. A., Stone, E. A., Jordan, K. W., Lyman, R. F., Magwire, M. M., Rollmann, S. M., Duncan, L. H., Lawrence, F., Anholt, R. R. & MacKay, T. F. (2009). Systems genetics of complex traits in Drosophila melanogaster. Nature Genetics 41, 299-307.
5. Carbone, M. A., Jordan, K. W., Lyman, R. F., Harbison, S. T., Leips, J., Morgan, T. J., DeLuca, M., Awadalla, P. & MacKay, T. F. (2006). Phenotypic variation and natural selection at Catsup, a pleiotropic quantitative trait gene in Drosophila. Current Biology 16, 912-919.
6. Chen, C. P. & Walker, V. K. (1993). Increase in cold-shock tolerance by selection of cold resistant lines in Drosophila melanogaster. Ecological Entomology 18, 184-190.
7. Clarke, A. (1996). The influence of climate change of the distribution and evolution of organisms. In Animals and Temperature: Phenotypic and Evolutionary Adaptation, (ed I. A. Johnston & A. F. Bennett), pp. 377-407. Cambridge: Cambridge University Press.
8. Collinge, J. E., Anderson, A. R., Weeks, A. R., Johnson, T. K. & McKechnie, S. W. (2008). Latitudinal and coldtolerance variation associate with DNA repeat-number variation in the hsr-omega RNA gene of Drosophila melanogaster. Heredity 101, 260-270.
9. Collinge, J. E., Hoffmann, A. A. & McKechnie, S. W. (2006). Altitudinal patterns for latitudinally varying traits and polymorphic markers in Drosophila melanogaster from eastern Australia. Journal of Evolutionary Biology 19, 473-482.
10. Coyne, J. A. & Elwyn, S. (2006). Does the desaturase-2 locus in Drosophila melanogaster cause adaptation and sexual isolation? Evolution 60, 279-291. (Pubitemid 44804554)
11. David, J. R. & Capy, P. (1988). Genetic variation of Drosophila melanogaster natural populations. Trends in Genetics 4, 106-111.
12. David, J. R., Gibert, P., Moreteau, B., Gilchrist, G. W. & Huey, R. B. (2003). The fly that came in from the cold: geographic variation of recovery time from lowtemperature exposure in Drosophila subobscura. Functional Ecology 17, 425-430.
13. Fu, Y.-X. & Li, W.-H. (1993). Statistical tests of neutrality of mutations. Genetics 133, 693-709.
14. Fujita, T., Inoue, H., Kitamura, T., Sato, N., Shimosawa, T. & Maruyama, N. (1998). Senescence marker protein-30 (SMP30) rescues cell death by enhancing plasma membrane Ca2+ pumping activity in Hep G2 cells. Biochemical and Biophysical Research Communications 250, 374-380.
15. Gibert, P. & Huey, R. B. (2001). Chill-coma temperature in Drosophila: effects of developmental temperature, latitude, and phylogeny. Physiological and Biochemical Zoology 74, 429-434.
16. Gibert, P., Moreteau, B., Petavy, D., Karan, D. & David, J. R. (2001). Chill-coma tolerance, a major climatic adaptation among Drosophila species. Evolution 55, 1063-1068.
17. Goto, S. G. (2000). Expression of Drosophila homologue of senescence marker protein-30 during cold acclimation. Journal of Insect Physiology 46, 1111-1120.
18. Goto, S. G. (2001). A novel gene that is up-regulated during recovery from cold shock in Drosophila melanogaster. Gene 270, 259-264.
19. Greenberg, A. J., Moran, J. R., Coyne, J. A. & Wu, C. I. (2003). Ecological adaptation during incipient speciation revealed by precise gene replacement. Science 302, 1754-1757.
20. Hochachka, P. W. (1986). Defense strategies against hypoxia and hypothermia. Science 231, 234-241.
21. Hoekstra, H. E. & Coyne, J. A. (2007). The locus of evolution: evo devo and the genetics of adaptation. Evolution 61, 995-1016.
22. Hoffmann, A. A., Anderson, A. & Hallas, R. (2002). Opposing clines for high and low temperature resistance in Drosophila melanogaster. Ecology Letters 5, 614-618.
23. Hoffmann, A. A. & Parsons, P. (1991). Evolutionary Genetics of Environmental Stress. Oxford: Oxford university press.
24. Hoffmann, A. A., Shirriffs, J. & Scott, M. (2005). Relative importance of plastic vs genetic factors in adaptive differentiation: geographical variation for stress resistance in Drosophila melanogaster from eastern Australia. Functional Ecology 19, 222-227.
25. Hoffmann, A. A., Sorensen, J. G. & Loeschcke, V. (2003). Adaptation of Drosophila to temperature extremes: bringing together quantitative and molecular approaches. Journal of Thermal Biology 28, 175-216.
26. Hoffmann, A. A. & Willi, Y. (2008). Detecting genetic responses to environmental change. Nature Reviews Genetics 9, 421-432.
27. Inoue, H., Fujita, T., Kitamura, T., Shimosawa, T., Nagasawa, R., Inoue, R., Maruyama, N. & Nagasawa, T. (1999). Senescence marker protein-30 (SMP30) enhances the calcium efflux from renal tubular epithelial cells. Clinical and Experimental Nephrology 3, 261-267.
28. Kelty, J. D., Killian, K. A. & Lee, R. E. (1996). Cold shock and rapid cold-hardening of pharate adult flesh flies (Sarcophaga crassipalpis) : effects on behaviour and neuromuscular function following eclosion. Physiological Entomology 21, 283-288.
29. Kennington, W. J., Partridge, L. & Hoffmann, A. A. (2006). Patterns of diversity and linkage disequilibrium within the cosmopolitan inversion In(3R)Payne in Drosophila melanogaster are indicative of coadaptation. Genetics 172, 1655-1663.
30. Kimura, M. T. (2004). Cold and heat tolerance of drosophilid flies with reference to their latitudinal distributions. Oecologia 140, 442-449.
31. Kostal, V., Renault, D., Mehrabianova, A. & Bastl, J. (2007). Insect cold tolerance and repair of chill-injury at fluctuating thermal regimes: role of ion homeostasis. Comparative Biochemistry and Physiology A-Molecular and Integrative Physiology 147, 231-238.
32. Kostal, V., Vambera, J. & Bastl, J. (2004). On the nature of pre-freeze mortality in insects: water balance, ion homeostasis and energy charge in the adults of Pyrrhocoris apterus. Journal of Experimental Biology 207, 1509-1521.
33. Leather, S. R., Walters, K. F. A. & Bale, J. S. (1993). The Ecology of Insect Overwintering. Cambridge [England]; New York, NY, USA: Cambridge University Press.
34. Lewontin, R. C. (1974). The Genetic Basis of Evolutionary Change. New York: Columbia University Press.
35. Librado, P. & Rozas, J. (2009). DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451-1452.
36. Long, A. D., Lyman, R. F., Langley, C. H. & Mackay, T. F. C. (1998). Two sites in the Delta gene region contribute to naturally occurring variation in bristle number in Drosophila melanogaster. Genetics 149, 999-1017.
37. Morgan, T. J. & Mackay, T. F. (2006). Quantitative trait loci for thermotolerance phenotypes in Drosophila melanogaster. Heredity 96, 232-242.
38. Nei, M. & Tajima, F. (1981). DNA polymorphism detectable by restriction endonucleases. Genetics 97, 145-163.
39. Norry, F. M., Gomez, F. H. & Loeschcke, V. (2007). Knockdown resistance to heat stress and slow recovery from chill coma are genetically associated in a quantitative trait locus region of chromosome 2 in Drosophila melanogaster. Molecular Ecology 16, 3274-3284.
40. Norry, F. M., Scannapieco, A. C., Sambucetti, P., Bertoli, C. I. & Loeschcke, V. (2008). QTL for the thermotolerance effect of heat hardening, knockdown resistance to heat and chill-coma recovery in an intercontinental set of recombinant inbred lines of Drosophila melanogaster. Molecular Ecology 17, 4570-4581.
41. Overgaard, J., Sorensen, J. G., Petersen, S. O., Loeschcke, V. & Holmstrup, M. (2005). Changes in membrane lipid composition following rapid cold hardening in Drosophila melanogaster. Journal of Insect Physiology 51, 1173-1182.
42. Pullin, A. S. & Bale, J. S. (1988). Cause and effects of prefreeze mortality in aphids. Cryo-Letters 9, 102-113.
43. Qin, W., Neal, S. J., Robertson, R. M., Westwood, J. T. & Walker, V. K. (2005). Cold hardening and transcriptional change in Drosophila melanogaster. Insect Molecular Biology 14, 607-613.
44. Rako, L., Blacket, M. J., McKechnie, S. W. & Hoffmann, A. A. (2007). Candidate genes and thermal phenotypes: identifying ecologically important genetic variation for thermotolerance in the Australian Drosophila melanogaster cline. Molecular Ecology 16, 2948-2957.
45. Schmidt, P. S. & Paaby, A. B. (2008). Reproductive diapause and life-history clines in North American populations of Drosophila melanogaster. Evolution 62, 1204-1215.
46. Sinclair, B. J., Gibbs, A. G. & Roberts, S. P. (2007). Gene transcription during exposure to, and recovery from, cold and desiccation stress in Drosophila melanogaster. Insect Molecular Biology 16, 435-443.
47. Son, T. G., Kim, S. J., Kim, K., Kim, M., Chung, H. Y. & Lee, J. (2008). Cryoprotective roles of senescence marker protein 30 against intracellular calcium elevation and oxidative stress. Archives of Pharmacal Research 31, 872-877.
48. Tajima, F. (1989). Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585-595.
49. Takeuchi, K., Nakano, Y., Kato, U., Kaneda, M., Aizu, M., Awano, W., Yonemura, S., Kiyonaka, S., Mori, Y., Yamamoto, D. & Umeda, M. (2009). Changes in temperature preferences and energy homeostasis in dystroglycan mutants. Science 323, 1740-1743.
50. Teets, N. M., Elnitsky, M. A., Benoit, J. B., Lopez-Martinez, G., Denlinger, D. L. & Lee, R. E. (2008). Rapid cold-hardening in larvae of the Antarctic midge Belgica antarctica: cellular cold-sensing and a role for calcium. American Journal of Physiology-Regulatory Integrative and Comparative Physiology 294, R1938-R1946.
51. Telonis-Scott, M., Hallas, R., McKechnie, S. W., Wee, C. W. & Hoffmann, A. A. (2009). Selection for cold resistance alters gene transcript levels in Drosophila melanogaster. Journal of Insect Physiology 55, 549-555.
52. Tucic, N. (1979). Genetic capacity for adaptation to cold resistance at different developmental stages of Drosophila melanogaster. Evolution 33, 350-358.
53. Watterson, G. A. (1975). On the number of segregating sites in genetical models without recombination. Theoretical Population Biology 7, 256-276.
54. Zhen, Y. & Ungerer, M. C. (2008). Clinal variation in freezing tolerance among natural accessions of Arabidopsis thaliana. New Phytologist 177, 419-427.