Two orthodenticle -related genes in the short-germ beetle Tribolium castaneum

Abstract

To investigate the molecular basis of head evolution, we searched for genes related to the Drosophila orthodenticle (otd) homeobox gene in the short-germ beetle Tribolium castaneum. Unexpectedly, we found that there are two otd-related genes in Tribolium, with predicted homeodomains highly similar to that of the single Drosophila gene. One of the two genes (Tc otd-1) is more related in both amino acid sequence and expression pattern to fruitfly otd. Tc otd-1 is expressed in a broad anterior stripe in the blastoderm embryo, suggesting a role in early head segmentation similar to that of the Drosophila gene. The second gene (Tc otd-2) is more similar in sequence to the otd-related genes isolated from different vertebrate species (the Otx gene family). Tc otd-2 is not transcribed in the blastoderm, but is expressed later in more limited subsets of cells in the anterior brain. Both Tribolium genes and the Drosophila gene are, unlike the vertebrate genes, also expressed at the developing ventral midline of the embryo. Our results are consistent with the idea that an otd/Otx gene specified anterior head structures in the last ancestor common to arthropods and vertebrates. Within the arthropod lineage, we propose that this gene acquired a function in cells at the developing midline prior to the duplication that generated the two Tribolium genes.

Head patterning and Hox gene expression in an onychophoran and its implications for the arthropod head problem

“…Considering the fact that the Eka-otd contains the conserved SIWSPASI as the otd2 genes of Parhyale and Tribolium and its early expression in E. kanagrensis, which contrasts with that of Parhyale and Tribolium, it is possible to draw the conclusion that the single E. kanangrensis otd has the combined function of otd1 and otd2 in Parhyale and Tribolium and a duplication even occurred after the split of the arthropod and onychophoran lineages. This partly supports the views that a single otd/otx gene was present in the common ancestor to vertebrates and arthropods, and that this gene was duplicated in the lineages leading to chordates and arthropods respectively (Browne et al, 2006;Li et al, 1996). Li et al (1996) suggested on basis of the expression pattern of Tribolium otd2 that the ancestral function might have been to specify certain regions in the pre antennal brain, however, our data suggest that this ancestral gene would have combined the functions of otd1 and otd2.…”

“…This partly supports the views that a single otd/otx gene was present in the common ancestor to vertebrates and arthropods, and that this gene was duplicated in the lineages leading to chordates and arthropods respectively (Browne et al, 2006;Li et al, 1996). Li et al (1996) suggested on basis of the expression pattern of Tribolium otd2 that the ancestral function might have been to specify certain regions in the pre antennal brain, however, our data suggest that this ancestral gene would have combined the functions of otd1 and otd2.…”

“…This expression pattern is similar to the expression pattern seen in Drosophila otd and for the otd2 expression in Tribolium and Parhyale (Browne et al, 2006;Li et al, 1996) The expression of Eka-otd is sometimes, however, asymmetrical around the blastopore (Fig. 2 a-b).…”

“…The paralogue that contains the WSP motif is starting to be expressed late and is more similar in amino acid sequence to the vertebrates (Browne et al, 2006). In E. Kanangrensis we found one gene homologous to otd and it contained the WSP motif that is included in the SIWSPASI motif found in vertebrates (Li et al, 1996). The otd2 genes are also in the Tribolium expressed much later than otd1.…”

“…It has been shown that the anterior expression borders of some anterior Hox-genes are conserved among arthropods and workers have aligned head segments between different arthropod groups (Abzhanov and Kaufman, 1999;Damen et al, 1998;Jager et al, 2006;Mittmann and Scholtz, 2003;Telford and Thomas, 1998) and the head patterning genes six3 and otd have been used as markers for the most anterior region of bilaterians (Li et al, 1996;Lowe et al, 2003;Posnien et al, 2009;Schinko et al, 2008;Schröder, 2003;Seo et al, 1999).…”