Antagonistic role of the BTB-zinc finger transcription factors Chinmo and Broad-Complex in the juvenile/pupal transition and in growth control

Abstract

During development, the growing organism transits through a series of temporally regulated morphological stages to generate the adult form. In humans, for example, development progresses from childhood through to puberty and then to adulthood, when sexual maturity is attained. Similarly, in holometabolous insects, immature juveniles transit to the adult form through an intermediate pupal stage when larval tissues are eliminated and the imaginal progenitor cells form the adult structures. The identity of the larval, pupal, and adult stages depends on the sequential expression of the transcription factors <i>chinmo</i>, <i>Br-C,</i> and <i>E93</i>. However, how these transcription factors determine temporal identity in developing tissues is poorly understood. Here, we report on the role of the larval specifier <i>chinmo</i> in larval and adult progenitor cells during fly development. Interestingly, <i>chinmo</i> promotes growth in larval and imaginal tissues in a Br-C-independent and -dependent manner, respectively. In addition, we found that the absence of <i>chinmo</i> during metamorphosis is critical for proper adult differentiation. Importantly, we also provide evidence that, in contrast to the well-known role of <i>chinmo</i> as a pro-oncogene, Br-C and E93 act as tumour suppressors. Finally, we reveal that the function of <i>chinmo</i> as a juvenile specifier is conserved in hemimetabolous insects as its homolog has a similar role in <i>Blatella germanica</i>. Taken together, our results suggest that the sequential expression of the transcription factors Chinmo, Br-C and E93 during larva, pupa an adult respectively, coordinate the formation of the different organs that constitute the adult organism.