Implications of the Tribolium Deformed mutant phenotype for the evolution of Hox gene function

Abstract

Among insects, the genetic regulation of regional identities in the postoral head or gnathal segments (mandibular, maxillary, and labial) is best understood in the fly Drosophila melanogaster . In part, normal gnathal development depends on Deformed (Dfd) and Sex combs reduced (Scr) , genes in the split Drosophila homeotic complex. The gnathal segments of Dfd and Scr mutant larvae are abnormal but not homeotically transformed. In the red flour beetle, Tribolium castaneum , we have isolated loss-of-function mutations of the Deformed ortholog. Mutant larvae display a strong transformation of mandibular appendages to antennae. The maxillary appendages, normally composed of an endite and a telopodite, develop only the telopodite in mutant larvae. We previously reported that mutations in the beetle Scr and Antennapedia orthologs cause the labial and thoracic appendages, respectively, to be transformed to antennae. Moreover, a deficiency of most of the beetle homeotic complex causes all gnathal (as well as thoracic and abdominal) segments to develop antennae. These and other observations are consistent with the hypothesis that ancestral insect homeotic gene functions have been modified considerably during the evolution of the highly specialized maggot head. One of the ancestral homeobox genes that arose close to the root of the Eumetazoa appears to have given rise to Dfd, Scr , and the Antennapedia homeobox-class homeotic genes. Evidence from both Tribolium and Drosophila suggests that this ancestral gene served to repress anterior development as well as confer a trunk-specific identity.

Patterning of the Adult Mandibulate Mouthparts in the Red Flour Beetle, Tribolium castaneum

“…Therefore, we hypothesize that the difference in the number of palp segments results from specific activation of pdm in the maxillary palp. Loss of function in the Hox gene Deformed during T. castaneum embryogenesis causes a transformation of the larval maxillae toward labial identity (Brown et al 1999(Brown et al , 2000. Since Hox genes are the primary determinants of body segment identity, we propose that pdm is activated by Deformed and repressed by the labial Hox gene Sex combs reduced.…”

Establishment of Tribolium as a Genetic Model System and Its Early Contributions to Evo-Devo

“…In addition to abdominal-A, sequences and expression patterns were described for the orthologs of labial (Nie et al 2001), proboscipedia (Shippy et al 2000a,b), Deformed (Brown et al 1999a(Brown et al , 2000, fushi tarazu (Brown et al 1994), Sex combs reduced (Curtis et al 2001), Antennapedia (Brown et al 2002b and our unpublished results), Ultrabithorax (Bennett et al 1999), and Abdominal-B (He 1996). Except for the latter gene and some other minor exceptions, expression patterns are well conserved in the two insects, showing that the basis of the effect of Hox genes on morphological differences lies in changes in target and other downstream genes (see below).…”

“…This strategy directly paralleled that used to define genetically the Drosophila Antennapedia complex (see Denell 1994). This effort generated a Deformed loss-of-function allele (Brown et al 2000) as well as new alleles at some of the other genes. No labial variants were found, and we know now that knockdown of the gene by RNAi also does not result in a detectable phenotype (S. Brown, personal communication).…”

“…Beeman et al (1996) went on to demonstrate the efficacy of using a balancer to isolate autosomal recessive-lethal mutations. We also continued to isolate induced and spontaneous viable mutations at a steady rate, including a screen to detect mutations that failed to complement a deficiency of the Hox region (Brown et al 2000).…”

Preliminary phylogeny of Tribolium beetles (Coleoptera: Tenebrionidae) resolved by combined analysis of mitochondrial genes

“…Some of the species are easily cultured in the laboratory and the genus has been extensively used in genetic analyses (Sokoloff, 1972;Beeman et al, 1996;Bennett et al, 1999;Brown et al, 2000). Thanks to its convenient genetic set-up, Tribolium castaneum is predisposed to become one of the three most important insect model systems beside Drosophila and Bombyx mori (Schmidt & Tautz, 1999;Brown et al, 2003;Nagaraju & Goldsmith, 2002).…”