Abstract
BackgroundThe Hox family of transcription factors has a fundamental role in segmentation pathways and axial patterning of embryonic development and their clustered organization is linked with the regulatory mechanisms governing their coordinated expression along embryonic axes. Among chordates, of particular interest are the Hox paralogous genes in groups 1-4 since their expression is coupled to the control of regional identity in the anterior nervous system, where the highest structural diversity is observed.ResultsTo investigate the degree of conservation in cis-regulatory components that form the basis of Hox expression in the anterior nervous system, we have used assays for transcriptional activity in ascidians and vertebrates to compare and contrast regulatory potential. We identified four regulatory sequences located near the CiHox1, CiHox2 and CiHox4 genes of the ascidian Ciona intestinalis which direct neural specific domains of expression. Using functional assays in Ciona and vertebrate embryos in combination with sequence analyses of enhancer fragments located in similar positions adjacent to Hox paralogy group genes, we compared the activity of these four Ciona cis-elements with a series of neural specific enhancers from the amphioxus Hox1-3 genes and from mouse Hox paralogous groups 1-4.ConclusionsThis analysis revealed that Kreisler and Krox20 dependent enhancers critical in segmental regulation of the hindbrain appear to be specific for the vertebrate lineage. In contrast, neural enhancers that function as Hox response elements through the action of Hox/Pbx binding motifs have been conserved during chordate evolution. The functional assays reveal that these Hox response cis-elements are recognized by the regulatory components of different and extant species. Together, our results indicate that during chordate evolution, cis-elements dependent upon Hox/Pbx regulatory complexes, are responsible for key aspects of segmental Hox expression in neural tissue and appeared with urochordates after cephalochordate divergence.
Highlights
The Hox family of transcription factors has a fundamental role in segmentation pathways and axial patterning of embryonic development and their clustered organization is linked with the regulatory mechanisms governing their coordinated expression along embryonic axes
To enable evolutionary comparisons to probe the degree of conservation of Hox regulatory elements directing anterior neural expression in mouse, amphioxus and Ciona we selected a series of Hox rhombomere-specific enhancer elements characterized in mouse embryos for their ability to direct segmental expression of Hox genes in paralogous groups 1, 2, 3 or 4
We have compared neural specific regulatory elements of the anterior Hox genes from three different chordate species, the cephalochordate amphioxus, the urochordate Ciona intestinalis and the vertebrate mouse to begin to understand the mechanisms that led to the evolution of neural structures in the chordate lineage
Summary
The Hox family of transcription factors has a fundamental role in segmentation pathways and axial patterning of embryonic development and their clustered organization is linked with the regulatory mechanisms governing their coordinated expression along embryonic axes. The availability of genomic sequences from an increasingly large number of species has shed light on many aspects of the evolution of Hox gene organization. This data has opened new questions on Recent genomic analyses have demonstrated that only vertebrates have a compact and well organized Hox cluster, while most of the other chordates and invertebrates analysed so far have “an intact but disorganized, a split or an atomized cluster” with a highly variable gene number [2]. The cephalochordate amphioxus has a single and intact cluster quite similar to compact vertebrate organization and the Hox and 6 genes show both temporal and spatial colinearity of expression along the anteroposterior axis of the developing neural tube [5,6]. It has been suggested that rapid embryogenesis and a simplification in body organization are at the basis of the breakdown of central Hox genes in these organisms
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