The magnitude and time course of activation of the heat-shock transcription factor (HSF) differ among Drosophila melanogaster lines evolving at 18 degrees C, 25 degrees C or 28 degrees C for more than 20 years. At lower heat-shock temperatures (27–35 degrees C), flies from the 18 degrees C population had higher levels of activated HSF (as detected by an electrophoretic mobility shift assay) than those reared at 25 degrees C and 28 degrees C. At higher temperatures (36 and 37 degrees C), however, the 28 degrees C flies had the highest levels of HSF. These differences persisted after one generation of acclimation at 25 degrees C, suggesting that phenotypic plasticity was limited. In addition, larvae from the 28 degrees C lines activated HSF less rapidly after a 35 degrees C heat shock than those from the 18 degrees C and 25 degrees C populations. These results are similar but not identical to previously reported differences in expression of Hsp70 (the major heat-inducible stress protein in Drosophila melanogaster) among the experimental lines. We conclude that HSF activation evolves rapidly during laboratory culture at diverse temperatures and could play an important role in the evolution of the heat-shock response.

REFERENCES

Bettencourt
B. R.
,
Feder
M. E.
(
1999
).
Gene conversion and natural selection drive molecular evolution in Drosophila.
Am. Zool
39
,
83
–.
Bettencourt
B. R.
,
Feder
M. E.
,
Cavicchi
S.
(
1999
).
Experimental evolution of Hsp70 expression and thermotolerance in Drosophila melanogaster.
Evolution
53
,
484
–.
Brennecke
T.
,
Gellner
K.
,
Bosch
T. C.
(
1998
).
The lack of a stress response in Hydra oligactis is due to reduced hsp70 mRNA stability.
Eur. J. Biochem
255
,
703
–.
Cavicchi
S.
,
Guerra
D.
,
Giorgi
G.
,
Pezzoli
C.
(
1985
).
Temperature-related divergence in experimental populations of Drosophila melanogaster. I. Genetic and developmental basis of wing size and shape variation.
Genetics
109
,
665
–.
Cavicchi
S.
,
Guerra
D.
,
La Torre
V.
,
Huey
R. B.
(
1995
).
Chromosomal analysis of heat-shock tolerance in Drosophila melanogaster evolving at different temperatures in the laboratory.
Evolution
49
,
676
–.
Clos
J.
,
Rabindran
S.
,
Wisniewski
J.
,
Wu
C.
(
1993
).
Induction temperature of human heat shock factor is reprogrammed in a Drosophila cell environment.
Nature
364
,
252
–.
Cotto
J. J.
,
Morimoto
R. I.
(
1999
).
Stress-induced activation of the heat-shock response: cell and molecular biology of heat-shock factors.
Biochem. Soc. Symp
64
,
105
–.
Crill
W. D.
,
Huey
R. B.
,
Gilchrist
G. W.
(
1996
).
Within-and between-generation effects of temperature on the morphology and physiology of Drosophila melanogaster.
Evolution
50
,
1205
–.
Favatier
F.
,
Jacquier-Sarlin
M. R.
,
Swierczewski
E.
,
Polla
B. S.
(
1999
).
Polymorphism in the regulatory sequence of the human hsp70-1 gene does not affect heat shock factor binding or heat shock protein synthesis.
Cell Mol. Life Sci
56
,
701
–.
Feder
J. H.
,
Rossi
J. M.
,
Solomon
J.
,
Solomon
N.
,
Lindquist
S.
(
1992
).
The consequences of expressing hsp70 in Drosophila cells at normal temperatures.
Genes Dev
6
,
1402
–.
Feder
M. E.
,
Cartano
N. V.
,
Milos
L.
,
Krebs
R. A.
,
Lindquist
S. L.
(
1996
).
Effect of engineering hsp70 copy number on Hsp70 expression and tolerance of ecologically relevant heat shock in larvae and pupae of Drosophila melanogaster.
J. Exp. Biol
199
,
1837
–.
Feder
M. E.
,
Hofmann
G. E.
(
1999
).
Heat-shock proteins, molecular chaperones and the stress response: evolutionary and ecological physiology.
Annu. Rev. Physiol
61
,
243
–.
Frydenberg
J.
,
Pierpaoli
M.
,
Loeschcke
V.
(
1999
).
Drosophila melanogaster is polymorphic for a specific repeated (CATA) sequence in the regulatory region of hsp23.
Gene
236
,
243
–.
Gehring
W. J.
,
Wehner
R.
(
1995
).
Heat shock protein synthesis and thermotolerance in Cataglyphis, an ant from the Sahara desert.
Proc. Natl. Acad. Sci. USA
92
,
2994
–.
Gupta
R. S.
,
Singh
B.
(
1994
).
Phylogenetic analysis of 70kD heat shock protein sequences suggests a chimeric origin for the eukaryotic cell nucleus.
Curr. Biol
4
,
1104
–.
Hess
M. A.
,
Duncan
R. F.
(
1996
).
Sequence and structure determinants of Drosophila Hsp70 mRNA translation: 5UTR secondary structure specifically inhibits heat shock protein mRNA translation.
Nucleic Acids Res
24
,
2441
–.
Jedlicka
P.
,
Mortin
M. A.
,
Wu
C.
(
1997
).
Multiple functions of Drosophila heat shock transcription factor in vivo.
EMBO J
16
,
2452
–.
Jenkins
N. L.
,
Hoffmann
A. A.
(
1994
).
Genetic and maternal variation for heat resistance in Drosophila from the field.
Genetics
137
,
783
–.
Li
B.
,
Weber
J. A.
,
Chen
Y.
,
Greenleaf
A. L.
,
Gilmour
D. S.
(
1996
).
Analyses of promoter-proximal pausing by RNA Polymerase II on the hsp70 heat shock gene promoter in a Drosophila nuclear extract.
Mol. Cell. Biol
16
,
5433
–.
Lindquist
S.
(
1980
).
Varying patterns of protein synthesis in Drosophila during heat shock: implications for regulation.
Dev. Biol
77
,
463
–.
Mason
P. B.
,
Lis
J. T.
(
1997
).
Cooperative and competitive interactions at the Hsp70 promoter.
J. Biol. Chem
272
,
33227
–.
Morimoto
R. I.
(
1998
).
Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones and negative regulators.
Genes Dev
12
,
3788
–.
Peterson
R. B.
,
Lindquist
S.
(
1989
).
Regulation of HSP70 synthesis by messenger RNA degradation.
Cell Regulation
1
,
135
–.
Quintana
A.
,
Prevosti
A.
(
1990
).
Genetic and environmental factors in the resistance of Drosophilasubobscura adults to high temperature shock. II. Modification of heat resistance by indirect selection.
Theor. Appl. Genet
80
,
847
–.
Sarge
K. D.
(
1995
).
Male germ cell-specific alteration in temperature set point of the cellular stress response.
J. Biol. Chem
270
,
18745
–.
Sarge
K. D.
,
Bray
A. E.
,
Goodson
M. L.
(
1995
).
Altered stress response in testis.
Nature
374
,
126
–.
Satyal
S. H.
,
Chen
D.
,
Fox
S. G.
,
Kramer
J. M.
,
Morimoto
R. I.
(
1998
).
Negative regulation of heat shock transcriptional response by HSBP1.
Genes Dev
12
,
1962
–.
Sorensen
J. G.
,
Michalak
P.
,
Justesen
J.
,
Loeschcke
V.
(
1999
).
Expression of the heat-shock protein HSP70 in Drosophila buzzatii lines selected for thermal resistance.
Hereditas
131
,
155
–.
Stephanou
G.
,
Alahiotis
S. N.
(
1983
).
Non-Mendelian inheritance of heat-sensitivity in Drosophila melanogaster.
Genetics
103
,
93
–.
Velazquez
J. M.
,
Sonoda
S.
,
Bugaisky
G.
,
Lindquist
S.
(
1983
).
Is the major Drosophila heat shock protein present in cells that have not been heat shocked?.
J. Cell Biol
96
,
286
–.
Welte
M. A.
,
Tetrault
J. M.
,
Dellavalle
R. P.
,
Lindquist
S. L.
(
1993
).
A new method for manipulating transgenes: engineering heat tolerance in a complex, multicellular organism.
Curr. Biol
3
,
842
–.
Westwood
J. T.
,
Wu
C.
(
1993
).
Activation of Drosophila heat shock factor: conformational change associated with a monomer-to-trimer transition.
Mol. Cell. Biol
13
,
3481
–.
Wu
C.
(
1980
).
The 5ends of Drosophila heat shock genes in chromatin are hypersensitive to DNase I.
Nature
286
,
854
–.
Zapata
J. M.
,
Maroto
E. G.
,
Sierra
J. M.
(
1991
).
Inactivation of mRNA cap-binding protein complex in Drosophila melanogaster embryos under heat shock.
J. Biol. Chem
266
,
16007
–.
Zatsepina
O. G.
,
Ulmasov
K. A.
,
Beresten
S. F.
,
Molodtsov
V. B.
,
Rybtsov
S. A.
,
Evgen'ev
M. B.
(
2000
).
Thermotolerant desert lizards characteristically differ in terms of heat-shock system regulation.
J. Exp. Biol
203
,
1017
–.
Zimarino
V.
,
Wu
C.
(
1987
).
Induction of sequence-specific binding of Drosophila heat shock activator protein without protein synthesis.
Nature
327
,
727
–.
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