Forces shaping a Hox morphogenetic gene-network during evolution

Abstract

The Abdominal-B selector protein induces the organogenesis of the posterior spiracles by coordinating an organ specific gene-network. The complexity of this network begs the question of how it originated during posterior spiracle evolution and what were the selective pressures driving its formation. As the network probably formed piecemeal with elements being recruited sequentially during evolution, we studied the morphogenetic consecuences of expressing in naive epithelial cells individual effector targets of the posterior spiracle network. In most cases, single target expression has little morphogenetic effect. In contrast, expression of the Cv-c RhoGAP protein increases actin based motility but also leads to epithelial polarity and adhesion defects. We show that these defects do not occur in spiracle cells normally expressing Cv-c because they have developed compensatory mechanisms. These mechanisms include the organ specific upregulation of cell polarity and adhesion molecules, which help compensating the deleterious effects caused by the transient Cv-c induced Rho1 inactivation. We show that other epithelial cells like the salivary gland, the leading edge and the trachea which also have coopted Cv-c to their morphogenetic gene-networks are also resistant to Cv-c’s deleterious effects on adhesion and epithelial polarity. We suggest that during evolution, Cv-c recruitment to any epithelium would have caused similar defects that resulted in a strong selective pressure that necessarily lead to recruit in those same cells downstream targets involved in the control of basic cell properties (adhesion and polarity regulators) to regain homeostasis. We propose based on our data, that when a selector gene cascade coopts a morphogenetic regulator, the instability caused requires the recruitment of various compensatory molecules that normalize it.