The evolving role of the orphan nuclear receptor ftz‐f1, a pair‐rule segmentation gene. Issue 6 (November 2013)

• Record Type: Journal Article
• Authors: Heffer, Alison; Grubbs, Nathaniel; Mahaffey, James; Pick, Leslie
• Is Part Of: Evolution & development. Volume 15:Issue 6(2013)
• Page Start: 406
• Page End: 417
• Publication Date: 2013-11
• Subjects: Evolution (Biology) -- Periodicals; Developmental biology -- Periodicals; 576.82
• DOI: 10.1111/ede.12050
• Languages: English
• ISSNs: 1520-541X

Abstract

<abstract abstract-type="main" xml:lang="en"> <title>SUMMARY</title> <sec id="ede12050-sec-0001" sec-type="section"> <p>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 <italic>Drosophila melanogaster</italic> (<italic>Dm</italic>), it has been found that their expression and function in segmentation in short‐ and intermediate‐germ insects often differ. <italic>Drosophila ftz‐f1</italic> encodes an orphan nuclear receptor that functions as a maternally expressed pair‐rule segmentation gene, responsible for the formation of alternate body segments during <italic>Drosophila</italic> embryogenesis. Here we investigated the expression and function of <italic>ftz‐f1</italic> in the short‐germ beetle, <italic>Tribolium castaneum</italic> (<italic>Tc</italic>). We found that <italic>Tc‐ftz‐f1</italic> is expressed in stripes in <italic>Tribolium</italic> embryos. These stripes overlap alternate <italic>Tc</italic>‐Engrailed (<italic>Tc</italic>‐En) stripes, indicative of a pair‐rule expression pattern. To test whether <italic>Tc‐ftz‐f1</italic> has pair‐rule function, we utilized embryonic RNAi, injecting double‐stranded RNA corresponding to <italic>Tc‐ftz‐f1</italic> coding or non‐coding regions into early <italic>Tribolium</italic> embryos. Knockdown of <italic>Tc‐ftz‐f1</italic> produced pair‐rule segmentation defects, evidenced by loss of expression of alternate En stripes. In addition, a later role for <italic>Tc‐ftz‐f1</italic> in cuticle formation was revealed. These results identify a new pair‐rule gene in <italic>Tribolium</italic> and suggest that its role in segmentation may be shared among holometabolous insects. Interestingly, while <italic>Tc‐ftz‐f1</italic> is expressed in pair‐rule stripes, the gene is ubiquitously expressed in <italic>Drosophila</italic> embryos. Thus, the pair‐rule function of <italic>ftz‐f1</italic> is conserved despite differences in expression patterns of <italic>ftz‐f1</italic> genes in different lineages. This suggests that <italic>ftz‐f1</italic> expression changed after the divergence of lineages leading to extant beetles and flies, likely due to differences in <italic>cis</italic>‐regulatory sequences. We propose that the dependence of <italic>Dm</italic>‐Ftz‐F1 on interaction with the homeodomain protein Ftz which is expressed in stripes in <italic>Drosophila</italic>, loosened constraints on <italic>Dm</italic>‐<italic>ftz‐f1</italic> expression, allowing for ubiquitous expression of this pair‐rule gene in <italic>Drosophila</italic>.</p> </sec> </abstract>