Molecular patterning mechanism underlying metamorphosis of the thoracic leg in Manduca sexta

Abstract

The tobacco hornworm Manduca sexta, like many holometabolous insects, makes two versions of its thoracic legs. The simple legs of the larva are formed during embryogenesis, but then are transformed into the more complex adult legs at metamorphosis. To elucidate the molecular patterning mechanism underlying this biphasic development, we examined the expression patterns of five genes known to be involved in patterning the proximal-distal axis in insect legs. In the developing larval leg of Manduca, the early patterning genes Distal-less and Extradenticle are already expressed in patterns comparable to the adult legs of other insects. In contrast, Bric-a-brac and dachshund are expressed in patterns similar to transient patterns observed during early stages of leg development in Drosophila. During metamorphosis of the leg, the two genes finally develop mature expression patterns. Our results are consistent with the hypothesis that the larval leg morphology is produced by a transient arrest in the conserved adult leg patterning process in insects. In addition, we find that, during the adult leg development, some cells in the leg express the patterning genes de novo suggesting that the remodeling of the leg involves changes in the patterning gene regulation.

Hexapoda: Comparative Aspects of Later Embryogenesis and Metamorphosis

“…Dll is expressed in the distal leg in all hexapod orders in which this has been examined (Figs. 3.2C and 3.8 ; see also, e.g., Panganiban et al 1994 ;Niwa et al 1997 ;Scholtz et al 1998 ;Abzhanov and Kaufman 2000 ;Tanaka and Truman 2007 ;Schaeper et al 2013 ), as well as in other arthropods and even onychophorans (Vol. 3, Chapter 4 ;Janssen et al 2010 ).…”

“…By contrast, in winged insects, the mature Dll expression pattern has a gap between a proximal "ring" domain at the femur-trochanter boundary and a distal "sock" domain from the mid-tibia to the distal limb tip. In most species, both the sock and ring are remnants of an initially broad expression domain, and the pattern forms by downregulation of Dll in the intervening domain (e.g., Jockusch et al 2000Prpic et al 2001 ;Inoue et al 2002a ;Angelini and Kaufman 2004 ;Tanaka and Truman 2007 ). In Drosophila , downregulation of the initially broad Dll domain leaves only the sock domain; the ring domain appears de novo late in the third larval instar (Diaz-Benjumea et al 1994 ;Galindo et al 2011 ).…”

“…In Drosophila , downregulation of the initially broad Dll domain leaves only the sock domain; the ring domain appears de novo late in the third larval instar (Diaz-Benjumea et al 1994 ;Galindo et al 2011 ). A further difference is that the proximal ring co-expresses Dll , dac , and hth in Drosophila and Manduca , whereas in other species, dac and Dll show no or limited overlap proximally, leaving a proximal ring that co-expresses Dll and hth , but not dac (Prpic et al 2001 ;Inoue et al 2002a ;Angelini and Kaufman 2004 ;Tanaka and Truman 2007 ).…”

“…dac expression in an intermediate leg domain is conserved in the embryos of collembolans, thysanurans, orthopterans, hemipterans, coleopterans, and lepidopterans ( Fig. 3.8 ; Prpic et al 2001 ;Inoue et al 2002a ;Angelini and Kaufman 2004 ;Tanaka and Truman 2007 ;Schaeper et al 2013 ), as well as in other arthropods (e.g., Sharma et al 2012 ). Expression dynamics and limited functional data suggest that dac is responsible for downregulation of Dll , generating the gap in between the sock and ring domains across winged insects (Prpic et al 2001 ;Inoue et al 2002a ;Angelini and Kaufman 2004 ).…”

PBX/extradenticle is required to re-establish axial structures and polarity during planarian regeneration

“…This transcription factor has been shown to have broad roles in embryonic and postembryonic patterning events in vertebrates (Karlsson et al, 2010;Capellini et al, 2011;Vitobello et al, 2011) and members of the Ecdysozoa protostome clade (Peifer and Wieschaus, 1990;González-Crespo et al, 1998;Van Auken et al, 2002;Merabet et al, 2005;Yang et al, 2005;Tanaka and Truman, 2007;Prpic and Telford, 2008). Given the growing evidence for roles of other TALE class proteins in regeneration, this gene represented a good candidate for a central role in planarian regeneration (Mercader et al, 2005;Felix and Aboobaker, 2010;Shaikh et al, 2011).…”