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trithorax regulates the expression of multiple Hox genes within the embryonic dorsal vessel and is required for heart proper and aorta specification


Authors:
Adam Farmer 1, 2, 3; Shaad Ahmad 1, 2, 3; Kristopher Schwab 1, 2, 3

Affiliations:
1) Department of Biology, Indiana State University, Terre Haute, IN; 2) The Rich and Robin Porter Cancer Research Center, Indiana State University, Terre Haute, IN; 3) The Center for Genomic Advocacy, Indiana State University, Terre Haute, IN

Keywords:
c. homeotics; a. axis specification

The Drosophila melanogaster embryonic dorsal vessel is a linear myoepithelial tube comprised of a posterior large-diameter heart proper region that intakes and anteriorly propels hemolymph through a narrow tube designated the aorta. The aorta is divided into an anterior and posterior region consisting of contractile cardiac cells (CC) derived from differing lineages. The anterior-most aorta contains Tinman (Tin)-positive CCs, while the posterior aorta and heart proper CCs are arranged in repeated ‘hemisegments’ composed of two anterior Seven-up (Svp)-positive cells and four Tin-positive cells. Several Hox genes have critical roles in the anterior-posterior patterning of the dorsal vessel. Furthermore, the Antennapedia (Antp) and the Bithorax Complex (Bx-C) genes are expressed in a spatial colinear manner within the dorsal vessel.

In the developing embryo, Hox gene expression is positively regulated by trithorax group (TrG) genes coordinating the proper segmental and morphological identities. Here, we identify the trithorax (trx) gene as an essential regulator of Hox gene expression within the dorsal vessel. Within trx null embryos, the heart proper region of the stage 16 dorsal vessel remains structurally identical to the narrow posterior aorta; the posterior region does not develop the luminal dilation, nor the CCs assume the characteristic cellular morphology of heart CCs. Additionally, the posterior region of the trx null dorsal vessel adopts a posterior aortic fate as indicated by the loss of the heart luminal marker Multiplexin, an extracellular ligand necessary for heart luminal dilation. The homeotic transformation of the heart proper into the posterior aorta implies dysregulation of Hox gene expression with the trx null embryo. Indeed, Abdominal-A (Abd-A) expression is completely lost within the trx null dorsal vessel resembling the abd-A null phenotype. Additionally, other Hox genes are dysregulated, notably at the anterior and posterior ends of the dorsal vessel. The anterior-most expression of Antp was absent from the posterior aorta, while Abdominal-B (Abd-B) expression localized to the posterior-most CCs of A8 segment was also lost. Although the higher Ubx levels expressed in the posterior aorta were reduced, low levels of Ultrabithorax (Ubx) expression persisted within the dorsal vessel. Overall, trx is required for Antp and Bx-C protein expression within the dorsal vessel which establishes heart and aorta specification. The inactivation of trx results with a striking homeotic transformation of the heart proper region into the posterior aorta similar to the abd-A null phenotype.