title: The evolving role of the orphan nuclear receptor ftz-f1, a pair-rule segmentation gene.
abstract: Segmentation is a critical developmental process that occurs by different mechanisms in diverse taxa. In insects, there are three common modes of embryogenesis-short-, intermediate-, and long-germ development-which differ in the number of segments specified at the blastoderm stage. While genes involved in segmentation have been extensively studied in the long-germ insect Drosophila melanogaster (Dm), it has been found that their expression and function in segmentation in short- and intermediate-germ insects often differ. Drosophila ftz-f1 encodes an orphan nuclear receptor that functions as a maternally expressed pair-rule segmentation gene, responsible for the formation of alternate body segments during Drosophila embryogenesis. Here we investigated the expression and function of ftz-f1 in the short-germ beetle, Tribolium castaneum (Tc). We found that Tc-ftz-f1 is expressed in stripes in Tribolium embryos. These stripes overlap alternate Tc-Engrailed (Tc-En) stripes, indicative of a pair-rule expression pattern. To test whether Tc-ftz-f1 has pair-rule function, we utilized embryonic RNAi, injecting double-stranded RNA corresponding to Tc-ftz-f1 coding or non-coding regions into early Tribolium embryos. Knockdown of Tc-ftz-f1 produced pair-rule segmentation defects, evidenced by loss of expression of alternate En stripes. In addition, a later role for Tc-ftz-f1 in cuticle formation was revealed. These results identify a new pair-rule gene in Tribolium and suggest that its role in segmentation may be shared among holometabolous insects. Interestingly, while Tc-ftz-f1 is expressed in pair-rule stripes, the gene is ubiquitously expressed in Drosophila embryos. Thus, the pair-rule function of ftz-f1 is conserved despite differences in expression patterns of ftz-f1 genes in different lineages. This suggests that ftz-f1 expression changed after the divergence of lineages leading to extant beetles and flies, likely due to differences in cis-regulatory sequences. We propose that the dependence of Dm-Ftz-F1 on interaction with the homeodomain protein Ftz which is expressed in stripes in Drosophila, loosened constraints on Dm-ftz-f1 expression, allowing for ubiquitous expression of this pair-rule gene in Drosophila.
authors.affiliation: Department of Entomology and Program in Molecular & Cell Biology, University of Maryland, College Park, MD, 20742, USA.
authors.forename: Alison
authors.initials: A
authors.lastname: Heffer
authors.forename: Nathaniel
authors.initials: N
authors.lastname: Grubbs
authors.forename: James
authors.initials: J
authors.lastname: Mahaffey
authors.forename: Leslie
authors.initials: L
authors.lastname: Pick
mesh_terms: D000818:Animals; D004331:Drosophila melanogaster / Q000378:metabolism; D019143:Evolution, Molecular; D018507:Gene Expression Regulation, Developmental; D019476:Insect Proteins / Q000737:chemistry / Q000235:genetics* / Q000378:metabolism; D057093:Orphan Nuclear Receptors / Q000737:chemistry / Q000235:genetics* / Q000378:metabolism; D014231:Tribolium / Q000196:embryology* / Q000235:genetics* / Q000378:metabolism
chemical_list: D019476:Insect Proteins; D057093:Orphan Nuclear Receptors