Developmental competence and the induction of ectopic proboscises in Drosophila melanogaster

Abstract

Developmental competence is the response of a cell(s) to information. Determination of adult labial identity in Drosophila requires Proboscipedia (PB) and Sex combs reduced (SCR); however, co-ectopic expression of PB and SCR is not sufficient for induction of ectopic adult labial identity, because the developmental information supplied by PB and SCR is suppressed. The evolutionarily conserved LASCY, DYTQL, NANGE motifs, and the C-terminal domain of SCR are sequence elements that mediate some, or all, of the suppression of ectopic proboscis determination. Therefore, the developmentally competent primordial proboscis cells provide an environment devoid of suppression, allowing PB and SCR to determine proboscis identity. SCR derivatives lacking suppression sequences weakly induce ectopic proboscis transformations independently of PB, suggesting that SCR may be the activity required for induction of adult labial identity, as is the case for larval labial identity. A possible explanation for PB independence of SCR in determination of adult and embryonic labial identity is PB operates as a competence factor that switches SCR from determining T1 identity to labial identity during metamorphosis. Lastly, labial determination is not conserved between SCR and murine HOXA5, suggesting that SCR has acquired this activity during evolution.

Acquisition of a Leucine Zipper Motif as a Mechanism of Antimorphy for an Allele of theDrosophila HoxGeneSex Combs Reduced

“…Rather, a missense mutation introduces a leucine zipper motif into the SCR N-terminus, resulting in an acquired capacity for inhibiting endogenous SCR activity. The ability of a single amino acid change in SCR 14 to alter SCR activity is supported by the observation that deletions of either the octapeptide motif or the LASCY motif do not decrease SCR activity for inducing ectopic sex comb bristles on the T2 leg as drastically as the SCR 14 substitution (Percival-Smith et al 2013). We have been unsuccessful in a number of assays in detecting hetero-oligomerization between SCR + and SCR 14 peptides; therefore, there are two possible explanations for the inhibition noted in this study.…”

“…In the proboscis, ectopic expression of SCR 14 121 TT resulted in an increase in the number of rows of pseudotrachea. A recent study suggests that SCR has two distinct activities that determine the labial and prothoracic segmental identities; therefore, this positive interaction may reflect a distinct effect of SCR 14 on SCR labial activity compared with SCR prothoracic activity (Percival-Smith et al 2013). …”

“…Surprisingly, although both of these regions are important for HOX function, the only essential domain is the DNA-binding HD (Berry and Gehring 2000; Tayyab et al 2004; Joshi et al 2007). An explanation for this finding is the observation of differential pleiotropy: the additive, context-dependent function of HOX protein motifs and domains (Hittinger et al 2005; Prince et al 2008; Sivanantharajah and Percival-Smith 2009; Merabet et al 2011; Percival-Smith et al 2013). …”

“…SCR has 10 protein motifs and domains conserved at different taxonomical levels: bilateran-specific (octapeptide, YPWM, HD, and KMAS); protostome-specific or arthropod-specific (LASCY, SCKY, PQDL, and NANGE); and insect-specific (DTYQL and C-terminal domain) (Percival-Smith et al 2013). During development, SCR establishes the identity of the labial and prothoracic segments.…”

Post-translational modifications ofDrosophila melanogasterHOX protein, Sex combs reduced

“…These genes encode transcription factors (TFs) that regulate expression of target genes by binding to DNA-binding sites with a 60 amino acid DNAbinding homeodomain (HD) (Gehring et al, 1994). The HOX protein, Sex combs reduced (SCR) is essential for the formation of larval salivary glands, adult proboscis and adult prothoracic legs in Drosophila melanogaster (Lewis et al, 1980;Struhl, 1982;Panzer et al, 1992;Percival-Smith et al, 1997;Percival-Smith et al, 2013). Besides the highly conserved HD, there are other small motifs in SCR required for function ( Figure 1).…”