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Volume 17, Number 17,
Issue of September 1, 1997
pp. 6745-6760
Copyright ©1997 Society for Neuroscience
Spatial and Temporal Expression of the period and
timeless Genes in the Developing Nervous System of
Drosophila: Newly Identified Pacemaker Candidates and
Novel Features of Clock Gene Product Cycling
Received Feb. 13, 1997; revised June 6, 1997; accepted June 11, 1997.
Maki Kaneko1,
Charlotte Helfrich-Förster2, and
Jeffrey
C. Hall1
1 Department of Biology, Brandeis University, Waltham,
Massachusetts 02254, and 2 Botanisches Institut, 72076 Tübingen, Germany
The circadian timekeeping system of Drosophila
functions from the first larval instar (L1) onward but
is not known to require the expression of clock genes in larvae. We
show that period (per) and
timeless (tim) are rhythmically expressed
in several groups of neurons in the larval CNS both in light/dark
cycles and in constant dark conditions. Among the clock gene-expressing
cells there is a subset of the putative pacemaker neurons, the
"lateral neurons" (LNs), that have been analyzed mainly in adult
flies. Like the adult LNs, the larval ones are also immunoreactive to a
peptide called pigment-dispersing hormone. Their putative dendritic trees were found to be in close proximity to the terminals of the
larval optic nerve Bolwig's nerve, possibly receiving photic input
from the larval eyes. The LNs are the only larval cells that maintain a
strong cycling in PER from L1 onward, throughout metamorphosis and into adulthood. Therefore, they are the best candidates for being pacemaker neurons responsible for the larval "time memory" (inferred from previous experiments). In addition to
the LNs, a subset of the larval dorsal neurons
(DNLs) expresses per and
tim. Intriguingly, two neurons of this
DNL group cycle in PER and TIM immunoreactivity
almost in antiphase to the other DNLs and to the
LNs. Thus, the temporal expression of per and
tim are regulated differentially in different cells.
Furthermore, the light sensitivity associated with levels of the TIM
protein is different from that in the heads of adult
Drosophila.
Key words:
larval CNS;
period;
timeless;
pigment-dispersing hormone;
pacemaker;
circadian;
Bolwig's nerve
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