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Broad complex isoforms have unique distributions during central nervous system metamorphosis in Drosophila melanogaster

Authors

  • Rebecca F. Spokony,

    1. Graduate Interdisciplinary Program in Insect Science, University of Arizona, Tucson, Arizona 85721-0108
    2. ARL Division of Neurobiology, University of Arizona, Tucson, Arizona 85721-0077
    Current affiliation:
    1. Dept. of Human Genetics, The University of Chicago, 920 E. 58th St., Chicago, IL 60637
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  • Linda L. Restifo

    Corresponding author
    1. Graduate Interdisciplinary Program in Insect Science, University of Arizona, Tucson, Arizona 85721-0108
    2. ARL Division of Neurobiology, University of Arizona, Tucson, Arizona 85721-0077
    3. Department of Neurology, Arizona Health Sciences Center, Tucson, Arizona 85724
    4. BIO5 Institute for Collaborative Bioresearch, University of Arizona, 85721
    • ARL Division of Neurobiology, University of Arizona, 611 Gould-Simpson Bldg., 1040 E. 4th St., Tucson, AZ 85721-0077
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Abstract

Broad Complex (BRC) is a highly conserved, ecdysone-pathway gene essential for metamorphosis in Drosophila melanogaster, and possibly all holometabolous insects. Alternative splicing among duplicated exons produces several BRC isoforms, each with one zinc-finger DNA-binding domain (Z1, Z2, Z3, or Z4), highly expressed at the onset of metamorphosis. BRC-Z1, BRC-Z2, and BRC-Z3 represent distinct genetic functions (BRC complementation groups rbp, br, and 2Bc, respectively) and are required at discrete stages spanning final-instar larva through very young pupa. We showed previously that morphogenetic movements necessary for adult CNS maturation require BRC-Z1, -Z2, and -Z3, but not at the same time: BRC-Z1 is required in the mid-prepupa, BRC-Z2 and -Z3 are required earlier, at the larval-prepupal transition. To explore how BRC isoforms controlling the same morphogenesis events do so at different times, we examined their central nervous system (CNS) expression patterns during the ≈16 hours bracketing the hormone-regulated start of metamorphosis. Each isoform had a unique pattern, with BRC-Z3 being the most distinctive. There was some colocalization of isoform pairs, but no three-way overlap of BRC-Z1, -Z2, and -Z3. Instead, their most prominent expression was in glia (BRC-Z1), neuroblasts (BRC-Z2), or neurons (BRC-Z3). Despite sequence similarity to BRC-Z1, BRC-Z4 was expressed in a unique subset of neurons. These data suggest a switch in BRC isoform choice, from BRC-Z2 in proliferating cells to BRC-Z1, BRC-Z3, or BRC-Z4 in differentiating cells. Together with isoform-selective temporal requirements and phenotype considerations, this cell-type-selective expression suggests a model of BRC-dependent CNS morphogenesis resulting from intercellular interactions, culminating in BRC-Z1-controlled, glia-mediated CNS movements in late prepupa. J. Comp. Neurol. 517:15–36, 2009. © 2009 Wiley-Liss, Inc.

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