The lineage-specific gene ponzr1 is essential for zebrafish pronephric and pharyngeal arch development.

Publication Type:

Journal Article

Source:

Development (Cambridge, England), Volume 139, Issue 4, p.793-804 (2012)

Keywords:

Animalsdigestive disease, digestive deseases Animals, Genetically Modifieddigestive disease, digestive deseases Biological Evolutiondigestive disease, digestive deseases Biological Markersdigestive disease, digestive deseases Branchial Regiondigestive disease, digestive deseases Embryo, Nonmammaliandigestive disease, digestive deseases Gene Expression Regulation, Developmentaldigestive disease, digestive deseases Gene Knockdown Techniquesdigestive disease, digestive deseases Kidneydigestive disease, digestive deseases Morphogenesisdigestive disease, digestive deseases PAX2 Transcription Factordigestive disease, digestive deseases Phenotypedigestive disease, digestive deseases Pronephrosdigestive disease, digestive deseases Transcription Factorsdigestive disease, digestive deseases Zebrafishdigestive disease, digestive deseases Zebrafish Proteins

Abstract:

The Homeobox (Hox) and Paired box (Pax) gene families are key determinants of animal body plans and organ structure. In particular, they function within regulatory networks that control organogenesis. How these conserved genes elicit differences in organ form and function in response to evolutionary pressures is incompletely understood. We molecularly and functionally characterized one member of an evolutionarily dynamic gene family, plac8 onzin related protein 1 (ponzr1), in the zebrafish. ponzr1 mRNA is expressed early in the developing kidney and pharyngeal arches. Using ponzr1-targeting morpholinos, we show that ponzr1 is required for formation of the glomerulus. Loss of ponzr1 results in a nonfunctional glomerulus but retention of a functional pronephros, an arrangement similar to the aglomerular kidneys found in a subset of marine fish. ponzr1 is integrated into the pax2a pathway, with ponzr1 expression requiring pax2a gene function, and proper pax2a expression requiring normal ponzr1 expression. In addition to pronephric function, ponzr1 is required for pharyngeal arch formation. We functionally demonstrate that ponzr1 can act as a transcription factor or co-factor, providing the first molecular mode of action for this newly described gene family. Together, this work provides experimental evidence of an additional mechanism that incorporates evolutionarily dynamic, lineage-specific gene families into conserved regulatory gene networks to create functional organ diversity.