Abstract
Hedgehog (Hh) genes play major roles in animal development and studies of their evolution, expression and function point to major differences among chordates. Here we focused on Hh genes in lampreys in order to characterize the evolution of Hh signalling at the emergence of vertebrates. Screening of a cosmid library of the river lamprey Lampetra fluviatilis and searching the preliminary genome assembly of the sea lamprey Petromyzon marinus indicate that lampreys have two Hh genes, named Hha and Hhb. Phylogenetic analyses suggest that Hha and Hhb are lamprey-specific paralogs closely related to Sonic/Indian Hh genes. Expression analysis indicates that Hha and Hhb are expressed in a Sonic Hh-like pattern. The two transcripts are expressed in largely overlapping but not identical domains in the lamprey embryonic brain, including a newly-described expression domain in the nasohypophyseal placode. Global alignments of genomic sequences and local alignment with known gnathostome regulatory motifs show that lamprey Hhs share conserved non-coding elements (CNE) with gnathostome Hhs albeit with sequences that have significantly diverged and dispersed. Functional assays using zebrafish embryos demonstrate gnathostome-like midline enhancer activity for CNEs contained in intron2. We conclude that lamprey Hh genes are gnathostome Shh-like in terms of expression and regulation. In addition, they show some lamprey-specific features, including duplication and structural (but not functional) changes in the intronic/regulatory sequences.
Highlights
Lampreys and hagfish are the only two groups of agnathans that have survived to date
Screening of a river lamprey (Lf) cosmid genomic library generated several positive clones which were subjected to Southern blot and showed two types of restriction profiles (Fig. 1B), raising the possibility of the existence of two distinct Hh genes in Lampetra fluviatilis (Lf) genome
coding elements (CNE) are enriched and clustered around genes involved in developmental regulation
Summary
Lampreys and hagfish are the only two groups of agnathans (meaning jawless vertebrates) that have survived to date They belong to a monophyletic group, the cyclostomes, considered as the sister group of extant gnathostomes (or jawed vertebrates) [1,2,3], see [4]. They are promised to be a first-class model for the study of the evolution of vertebrate developmental mechanisms, owing to this key phylogenetic position and to the special anatomical features they present (reviewed in [5]). The Hedgehog family is further enlarged due to a teleost-specific WGD, and there are two Shh (shha and shhb, the latter previously called tiggy-winkle hh), two Ihh (ihha and ihhb), but one Dhh member
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