Phenotypic plasticity in Drosophila pigmentation caused by temperature sensitivity of a chromatin regulator network.
Phenotypic plasticity is the ability of a genotype to produce contrasting phenotypes in different environments. Although many examples have been described, the responsible mechanisms are poorly understood. In particular, it is not clear how phenotypic plasticity is related to buffering, the maintenance of a constant phenotype against genetic or environmental variation. We investigate here the genetic basis of a particularly well described plastic phenotype: the abdominal pigmentation in female Drosophila melanogaster. Cold temperature induces a dark pigmentation, in particular in posterior segments, while higher temperature has the opposite effect. We show that the homeotic gene Abdominal-B (Abd-B) has a major role in the plasticity of pigmentation in the abdomen. Abd-B plays opposite roles on melanin production through the regulation of several pigmentation enzymes. This makes the control of pigmentation very unstable in the posterior abdomen, and we show that the relative spatio-temporal expression of limiting pigmentation enzymes in this region of the body is thermosensitive. Temperature acts on melanin production by modulating a chromatin regulator network, interacting genetically with the transcription factor bric-à-brac (bab), a target of Abd-B and Hsp83, encoding the chaperone Hsp90. Genetic disruption of this chromatin regulator network increases the effect of temperature and the instability of the pigmentation pattern in the posterior abdomen. Colocalizations on polytene chromosomes suggest that BAB and these chromatin regulators cooperate in the regulation of many targets, including several pigmentation enzymes. We show that they are also involved in sex comb development in males and that genetic destabilization of this network is also strongly modulated by temperature for this phenotype. Thus, we propose that phenotypic plasticity of pigmentation is a side effect reflecting a global impact of temperature on epigenetic mechanisms. Furthermore, the thermosensitivity of this network may be related to the high evolvability of several secondary sexual characters in the genus Drosophila.
Gibert
Jean-Michel
JM
Institut für Tierzucht und Genetik, Veterinärmedizinische Universität Wien, Vienna, Austria. jmg@i122server.vu-wien.ac.at
Peronnet
Frédérique
F
Schlötterer
Christian
C
D000005:Abdomen / Q000502:physiology; D000483:Alleles; D000818:Animals; D002843:Chromatin / Q000235:genetics* / Q000378:metabolism*; D004268:DNA-Binding Proteins / Q000378:metabolism; D029721:Drosophila Proteins / Q000378:metabolism; D004331:Drosophila melanogaster / Q000201:enzymology / Q000235:genetics* / Q000502:physiology*; D005260:Female; D005786:Gene Expression Regulation; D018841:HSP90 Heat-Shock Proteins / Q000378:metabolism; D018398:Homeodomain Proteins / Q000378:metabolism; D008297:Male; D008543:Melanins / Q000096:biosynthesis; D009154:Mutation / Q000235:genetics; D010641:Phenotype; D010858:Pigmentation / Q000235:genetics / Q000502:physiology*; D011485:Protein Binding; D013696:Temperature; D013997:Time Factors; D014157:Transcription Factors / Q000378:metabolism
C062393:Abd-B proteins, Drosophila; C093752:Bric-a-brac protein 1, Drosophila; D002843:Chromatin; D004268:DNA-Binding Proteins; D029721:Drosophila Proteins; D018841:HSP90 Heat-Shock Proteins; D018398:Homeodomain Proteins; D008543:Melanins; D014157:Transcription Factors