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BIOLOGICAL SCIENCES / EVOLUTION
Evolution of cis elements in the differential expression of two Hoxa2 coparalogous genes in pufferfish (Takifugu rubripes)
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*Stowers Institute for Medical Research, Kansas City, MO 64110; and Departments of Pathology and Laboratory Medicine and Anatomy and Cell Biology, University of Kansas Medical Center, Kansas City, KS 66160
Communicated by Michael S. Levine, University of California, Berkeley, CA, February 6, 2006 (received for review November 1, 2005)
Sequence divergence in cis-regulatory elements is an important mechanism contributing to functional diversity of genes during evolution. Gene duplication and divergence provide an opportunity for selectively preserving initial functions and evolving new activities. Many vertebrates have 39 Hox genes organized into four clusters (Hoxa–Hoxd); however, some ray-finned fishes have extra Hox clusters. There is a single Hoxa2 gene in most vertebrates, whereas fugu (Takifugu rubripes) and medaka (Oryzias latipes) have two coparalogous genes [Hoxa2(a) and Hoxa2(b)]. In the hindbrain, both genes are expressed in rhombomere (r) 2, but only Hoxa2(b) is expressed in r3, r4, and r5. Multiple regulatory modules directing segmental expression of chicken and mouse Hoxa2 genes have been identified, and each module is composed of a series of discrete elements. We used these modules to investigate the basis of differential expression of duplicated Hoxa2 genes, as a model for understanding the divergence of cis-regulatory elements. Therefore, we cloned putative regulatory regions of the fugu and medaka Hoxa2(a) and -(b) genes and assayed their activity. We found that these modules direct reporter expression in a chicken assay, in a manner corresponding to their endogenous expression pattern in fugu. Although sequence comparisons reveal many differences between the two coparalogous genes, specific subtle changes in seven cis elements of the Hoxa2(a) gene restore segmental regulatory activity. Therefore, drift in subsets of the elements in the regulatory modules is responsible for the differential expression of the two coparalogous genes, thus providing insight into the evolution of cis elements.
Hox gene regulation | hindbrain | vertebrate development | fugu
Conflict of interest statement: No conflicts declared.
To whom correspondence should be addressed at: Stowers Institute for Medical Research, 1000 East 50th Street, Kansas City, MO 64110. E-mail: rek{at}stowers-institute.org
© 2006 by The National Academy of Sciences of the USA
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