Abstract
Heat-shock genes have a well-studied control mechanism for their expression that is mediated through cis-regulatory motifs known as heat-shock elements (HSEs). The evolution of important features of this control mechanism has not been investigated in detail, however. Here we exploit the genome sequencing of multiple Drosophila species, combined with a wealth of available information on the structure and function of HSEs in D. melanogaster, to undertake this investigation. We find that in single-copy heat shock genes, entire HSEs have evolved or disappeared 14 times, and the phylogenetic approach bounds the timing and direction of these evolutionary events in relation to speciation. In contrast, in the multi-copy gene Hsp70, the number of HSEs is nearly constant across species. HSEs evolve in size, position, and sequence within heat-shock promoters. In turn, functional significance of certain features is implicated by preservation despite this evolutionary change; these features include tail-to-tail arrangements of HSEs, gapped HSEs, and the presence or absence of entire HSEs. The variation among Drosophila species indicates that the cis-regulatory encoding of responsiveness to heat and other stresses is diverse. The broad dimensions of variation uncovered are particularly important as they suggest a substantial challenge for functional studies.
Highlights
Cis-acting sequences are clearly vital to the regulation of gene expression and its evolution [1], the decoding of the organizational basis for this regulation and evolution is still a work in progress despite considerable effort, numerous research studies, and substantial genomic data
As have others [3] that a way forward may be in the combination of two aspects: a cis-regulatory sequence whose mechanism of controlling gene expression is understood in detail, and a robust phylogeny of successively more distantly related species
Phylogeny implicates function The 13 species of Drosophila exhibit at least 419 computationally identifiable heat-shock elements (HSEs) in the 8 heat-shock genes under study (Table S1, Table S2, Figures 2–9). This estimate includes 223 in usually single-copy genes (Hsp22, Hsp23, Hsp26, Hsp27, DnaJ-1, Hsp68, and Hsp83), with the balance in Hsp70, which is always multi-copy. These HSEs vary in occurrence, number, position, and conformity with the canonical sequence
Summary
Cis-acting sequences are clearly vital to the regulation of gene expression and its evolution [1], the decoding of the organizational basis for this regulation and evolution is still a work in progress despite considerable effort, numerous research studies, and substantial genomic data. A phylogenetic approach has two advantages beyond ‘‘phylogenetic footprinting’’; i.e., the identification of putative cis-regulatory sequence through conservation [4] It poses specific hypotheses about where in evolution changes have arisen; these hypotheses may in turn anchor other hypotheses about specific genetic mechanisms of evolutionary change and the adaptive consequences of the change. It highlights which features of the cis-regulatory sequence are free to evolve and which are stabilized by selection, providing corroboration for functional studies and possibly suggesting other, unrecognized features of the functional mechanism for further testing [5,6,7]. We exemplify these points in the cis-regulatory sequences governing the heat-shock response, heat-shock elements (HSEs)
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