A dynamic cell recruitment process drives growth of the Drosophila wing by overscaling the Vestigial expression pattern

Abstract

Organs mainly attain their size by cell growth and proliferation, but sometimes also grow through recruitment of undifferentiated cells. Here we investigate the participation of cell recruitment in establishing the pattern of Vestigial (Vg), the product of the wing selector gene in Drosophila. We find that the Vg pattern overscales along the dorsal-ventral (DV) axis of the wing imaginal disc, i.e., it expands faster than the DV length of the pouch. The overscaling of the Vg pattern cannot be explained by differential proliferation, apoptosis, or oriented-cell divisions, but can be recapitulated by a mathematical model that explicitly considers cell recruitment. By impairing cell recruitment genetically, we find that the Vg pattern almost perfectly scales and adult wings are approximately 20% smaller. Furthermore, using fluorescent reporter tools, we provide direct evidence that cell recruitment takes place in a specific time between early and mid third-instar larval development. Altogether, our work quantitatively shows when, how, and by how much cell recruitment shapes the Vg pattern and drives growth of the Drosophila wing.

Interplay between cell proliferation and recruitment controls the duration of growth and final size of the Drosophila wing

“…A numerical estimate of ε (using the parameter values reported in Table 1) is 1.0×10 -4 , about 1/10 of the proliferation rate. This relative recruitment rate integrated over the expected duration of the recruitment process during third larval instar (36 h) is consistent with our previously-reported relative contribution of cell recruitment of about 20% [26].…”

“…To quantify the W and R cells within the wing pouch, we used the immunofluorescence images stained with Vg, Wingless (Wg), and DAPI in y, w (considered wild type in this study) discs used in a previous publication [26]. For initial conditions W 0 and R 0 , we took early third instar images and counted manually (twice by two different observers).…”

“…For the optimization problem in Fig. 4C, we considered couples of parameters ( ρ, k ) within the black area of parameter space in Fig.4C, that defines those parameter sets that correspond to a t f within the range of 24 and 36 hours, which is the time in which the recruitment process takes place [26]. For each parameter set ( ρ, k ), we perturbed α (only α W in Fig.…”

“…The wing disc of Drosophila grows exponentially during three larval instars, mainly through cell proliferation and, to a lesser extent, through cell recruitment, a process by which undifferentiated neighboring cells are incorporated into the wing tissue by the induction of the wing selector gene, vestigial ( vg ) [23,24,25]. This process occurs only during the third larval instar and contributes to about 20% of adult wing size (including proliferation of newly recruited cells) [26]. However, it is unknown whether there is a crosstalk between cell proliferation and recruitment to coordinate growth and achieve the proper wing size.…”

Growth control in the Drosophila wing disk

“…Understanding what downstream factors allow proliferation in the wing disk but not the peripodial membrane may shed light on the MFM. In addition, the Vg feed‐forward recruitment pathway, which may contribute up to 20% of the final disk size (Muñoz‐Nava, Alvarez, Chara, Flores‐Flores, & Nahmad, ), must somehow be integrated into the MFM.…”