Hox Genes Regulate Muscle Founder Cell Pattern Autonomously and Regulate Morphogenesis Through Motor Neurons

Abstract

The differentiation of myoblasts to form functional muscle fibers is a consequence of interactions between the mesoderm and ectoderm. The authors examine the role of segment identity in directing these interactions by studying the role of Hox genes in patterning adult muscles in Drosophila. Using the ‘four-winged fly’ to remove Ultrabithorax function in the developing adult, the authors alter the identity of the ectoderm of the third thoracic segment towards the second and show that this is sufficient to inductively alter most properties of the mesoderm—myoblast number, molecular diversity, and migration pattern—to that of the second thoracic segment. Not all aspects of myogenesis are determined by the segment identity of the ectoderm. The autonomous identity of the mesoderm is important for choosing muscle founder cells in the correct segmental pattern. The authors show this by removal of the function of Antennapedia, the Hox gene expressed in the mesoderm of the third thoracic segment. This results in the transformation of founder cells to a second-thoracic pattern. The authors also report a role for the nervous system in later aspects of muscle morphogenesis by specifically altering Ultrabithorax gene expression in motor neurons. Thus, ectoderm and mesoderm segment identities collaborate to direct muscle differentiation by affecting distinct aspects of the process.

Keywords::

• Antennapedia
• dumbfounded
• Hox
• motor neurons
• muscle
• myogenesis
• Ultrabithorax

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Corrigendum

ACKNOWLEDGMENTS

The authors would like to thank Sean Carroll, Danny Brower, Siegfried Roth, and Daniel Kiehart for antibodies. The support of the Central Imaging and Flow Facility of NCBS is gratefully acknowledged. This article has been written in honour of Erich Buchner, who has inspired many collaborators and colleagues hoping to follow his example and his joy of doing science. K.V.R. and V.R. would particularly like to express their gratitude to Erich for many fruitful interactions. V.R. was a postdoctoral fellow in Erich Buchner's group at the Max-Planck Institut für biologische Kybernetik, Tübingen, Germany.

Declaration of interest: This work was supported by the Department of Biotechnology (DBT), The Indo-French Centre for Advanced Scientific Research (CEFIPRA/IFCPAR), and the National Centre for Biological Sciences (NCBS), Tata Institute of Fundamental Research, to K.V.R. and a Kanwal Rekhi Fellowship to D.D.