A novel cis-regulatory element drives early expression of Nkx3.2 in the gnathostome primary jaw joint

Author:

Leyhr Jake1ORCID,Waldmann Laura1,Filipek-Górniok Beata2,Zhang Hanqing34,Allalou Amin34,Haitina Tatjana1ORCID

Affiliation:

1. Subdepartment of Evolution and Development, Department of Organismal Biology, Uppsala University

2. Science for Life Laboratory Genome Engineering Zebrafish Facility, Department of Organismal Biology, Uppsala University

3. Division of Visual Information and Interaction, Department of Information Technology, Uppsala University

4. Science for Life Laboratory BioImage Informatics Facility

Abstract

The acquisition of movable jaws was a major event during vertebrate evolution. The role of NK3 homeobox 2 (Nkx3.2) transcription factor in patterning the primary jaw joint of gnathostomes (jawed vertebrates) is well known, however knowledge about its regulatory mechanism is lacking. In this study, we report a proximal enhancer element of Nkx3.2 that is deeply conserved in most gnathostomes but undetectable in the jawless hagfish and lamprey. This enhancer is active in the developing jaw joint region of the zebrafish Danio rerio, and was thus designated as jaw joint regulatory sequence 1 (JRS1). We further show that JRS1 enhancer sequences from a range of gnathostome species, including a chondrichthyan and mammals, have the same activity in the jaw joint as the native zebrafish enhancer, indicating a high degree of functional conservation despite the divergence of cartilaginous and bony fish lineages or the transition of the primary jaw joint into the middle ear of mammals. Finally, we show that deletion of JRS1 from the zebrafish genome using CRISPR/Cas9 results in a significant reduction of early gene expression of nkx3.2 and leads to a transient jaw joint deformation and partial fusion. Emergence of this Nkx3.2 enhancer in early gnathostomes may have contributed to the origin and shaping of the articulating surfaces of vertebrate jaws.

Funder

Vetenskapsrådet

Science for Life Laboratory

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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