Editors' ChoiceDevelopmental Biology

PTTH Induces Photophobia

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Sci. Signal.  10 Sep 2013:
Vol. 6, Issue 292, pp. ec216
DOI: 10.1126/scisignal.2004706

When fruit fly larvae near the end of larval development, they stop feeding and begin wandering in search of a dark place in which to pupariate and undergo metamorphosis. The neuropeptide prothoracicotropic hormone (PTTH) is produced by four larval brain neurons that project onto the prothoracic gland, where PTTH binds to the receptor kinase Torso to trigger production of the steroid hormone ecdysone. This PTTH-induced ecdysone pulse induces wandering behavior, and Yamanaka et al. report that PTTH also mediates the light avoidance response. Whereas knocking down torso in the prothoracic gland prevented the ecdysone pulse and pupariation, it did not affect the light avoidance behavior of wandering larvae. However, knocking down torso throughout the nervous system eliminated the light avoidance response. PTTH was secreted into the hemolymph, so the authors tested whether PTTH acted on distant neurons implicated in light sensing—the paired Bolwig’s organ (larval eyes) located anterior to the brain and the class IV dendritic arborization (da) neurons lining the body wall. Both Bolwig's organ and the class IV da neurons expressed torso, and knocking down torso in either group of neurons eliminated light avoidance but did not prevent wandering. Photoreceptor activation leads to opening of transient receptor potential (TRP) channels, which results in membrane depolarization and neuron firing. The abundance of photoreceptor proteins and transcripts was not affected in torso mutants, but live calcium imaging revealed reduced activity in the class IV da neurons of torso mutants that was comparable to the loss of TrpA1 in these cells. Genetic interaction experiments were also consistent with PTTH-Torso signaling affecting light avoidance behavior downstream of photoreceptor activation and upstream of TRP channel opening. These results illustrate that larval wandering and photophobia are independent behaviors, yet they depend upon the same neuroendocrine signal to coordinate their initiation.

N. Yamanaka, N. M. Romero, F. A. Martin, K. F. Rewitz, M. Sun, M. B. O’Connor, P. Léopold, Neuroendocrine control of Drosophila larval light preference. Science 341, 1113–1116 (2013). [Abstract] [Full Text]