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Phylogeny disambiguates the evolution of heat-shock cis-regulatory elements in Drosophila.

Tian S, Haney RA, Feder ME - PLoS ONE (2010)

Bottom Line: 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 broad dimensions of variation uncovered are particularly important as they suggest a substantial challenge for functional studies.

View Article: PubMed Central - PubMed

Affiliation: Department of Organismal Biology and Anatomy, University of Chicago, Chicago, Illinois, United States of America.

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.

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The distribution of HSEs is most variable in Hsp27.In the melanogaster subgroup, it is the only heat-shock gene with no HSE within 200 bp of the TSS. The multispecies genome alignment provides support for a rearrangement in D. ananassae and one or more deletions in the obscura group that remove intervening sequence and explain differences in distance to the TSS. We conservatively assume a single origin of proximal HSE sequence in Drosophila Hsp27 promoters, with subsequent modifications of length and distance to the TSS. A second, more distal HSE is found in all species, and appears to be orthologous in the melanogaster and obscura groups. A gain of a third distal HSE has occurred in the melanogaster subgroup. D. willistoni and D. virilis also have a third HSE, suggesting lineage specific gains. However, although the regions compared are directly adjacent to an orthologous coding region, ambiguity exists in the relationships of individual HSE in D. willistoni and the species of the subgenus Drosophila, and these HSEs are colored white.
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pone-0010669-g005: The distribution of HSEs is most variable in Hsp27.In the melanogaster subgroup, it is the only heat-shock gene with no HSE within 200 bp of the TSS. The multispecies genome alignment provides support for a rearrangement in D. ananassae and one or more deletions in the obscura group that remove intervening sequence and explain differences in distance to the TSS. We conservatively assume a single origin of proximal HSE sequence in Drosophila Hsp27 promoters, with subsequent modifications of length and distance to the TSS. A second, more distal HSE is found in all species, and appears to be orthologous in the melanogaster and obscura groups. A gain of a third distal HSE has occurred in the melanogaster subgroup. D. willistoni and D. virilis also have a third HSE, suggesting lineage specific gains. However, although the regions compared are directly adjacent to an orthologous coding region, ambiguity exists in the relationships of individual HSE in D. willistoni and the species of the subgenus Drosophila, and these HSEs are colored white.

Mentions: The 13 species of Drosophila exhibit at least 419 computationally identifiable 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. For example, HSEs range from two 5 bp subunits, [in Hsp23, Hsp26, DnaJ-1, and Hsp70 (Figures 3, 4, 6, 8)] to eleven subunits [in Hsp68 (Figure 7)]. Importantly, phylogenetic conservation in the 13 species suggests that certain features are functionally significant and are therefore subject to selection. These features include:


Phylogeny disambiguates the evolution of heat-shock cis-regulatory elements in Drosophila.

Tian S, Haney RA, Feder ME - PLoS ONE (2010)

The distribution of HSEs is most variable in Hsp27.In the melanogaster subgroup, it is the only heat-shock gene with no HSE within 200 bp of the TSS. The multispecies genome alignment provides support for a rearrangement in D. ananassae and one or more deletions in the obscura group that remove intervening sequence and explain differences in distance to the TSS. We conservatively assume a single origin of proximal HSE sequence in Drosophila Hsp27 promoters, with subsequent modifications of length and distance to the TSS. A second, more distal HSE is found in all species, and appears to be orthologous in the melanogaster and obscura groups. A gain of a third distal HSE has occurred in the melanogaster subgroup. D. willistoni and D. virilis also have a third HSE, suggesting lineage specific gains. However, although the regions compared are directly adjacent to an orthologous coding region, ambiguity exists in the relationships of individual HSE in D. willistoni and the species of the subgenus Drosophila, and these HSEs are colored white.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2871787&req=5

pone-0010669-g005: The distribution of HSEs is most variable in Hsp27.In the melanogaster subgroup, it is the only heat-shock gene with no HSE within 200 bp of the TSS. The multispecies genome alignment provides support for a rearrangement in D. ananassae and one or more deletions in the obscura group that remove intervening sequence and explain differences in distance to the TSS. We conservatively assume a single origin of proximal HSE sequence in Drosophila Hsp27 promoters, with subsequent modifications of length and distance to the TSS. A second, more distal HSE is found in all species, and appears to be orthologous in the melanogaster and obscura groups. A gain of a third distal HSE has occurred in the melanogaster subgroup. D. willistoni and D. virilis also have a third HSE, suggesting lineage specific gains. However, although the regions compared are directly adjacent to an orthologous coding region, ambiguity exists in the relationships of individual HSE in D. willistoni and the species of the subgenus Drosophila, and these HSEs are colored white.
Mentions: The 13 species of Drosophila exhibit at least 419 computationally identifiable 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. For example, HSEs range from two 5 bp subunits, [in Hsp23, Hsp26, DnaJ-1, and Hsp70 (Figures 3, 4, 6, 8)] to eleven subunits [in Hsp68 (Figure 7)]. Importantly, phylogenetic conservation in the 13 species suggests that certain features are functionally significant and are therefore subject to selection. These features include:

Bottom Line: 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 broad dimensions of variation uncovered are particularly important as they suggest a substantial challenge for functional studies.

View Article: PubMed Central - PubMed

Affiliation: Department of Organismal Biology and Anatomy, University of Chicago, Chicago, Illinois, United States of America.

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.

Show MeSH
Related in: MedlinePlus