A few unanswered questions about the fly PNS

    To our knowledge, the following questions remain unanswered and uninvestigated... They are waiting for you!


1) Projection of the vtd and v'td axons to thoracic segment T3

   During embryonic and larval development, abdominal sensory neurons do not cross segmental boundaries: their axon grows from the cell body and innervates the ventral nerve cord within the segment they originate from (see references describing axonal pathways). One exception to this rule are the vtd and v'td neurons (Meritt 1995). Irrespective of their segmental origin, the axons of vtd and v'td extend anteriorly in a very lateral fascicle to the T3 neuromere where they turn medially and dorsally.

What are the molecular mechanisms that control the migration of vtd and v'td neurons up to thoracic segment T3?
What distinguishes vtd and v'td neurons from the other sensory neurons?




2) Development of an unpaired sensory organ at the midline

    At the ventral midline in segment A8 is a unique external sensory organ named vas (Dambly-Chaudière and Ghysen, 1986; Campos-Ortega and Hartenstein, 1997). This organ contains two highly Cut-positive cells (socket and shaft cells), a Prospero-positive cell (sheath cell) and an Elav-positive cell (neuron). It probably originates from an md-es lineage because there is another Cut-positive Elav-positive neuron besides the sensory neuron (presumably an md neuron) (V. Orgogozo and F. Schweisguth, unpublished observations).
As opposed to all the other characterized sensory organs, which are patterned in a perfectly bilateral manner, this organ is unpaired: there is only one vas organ per embryo/larva. Since sensory precursor cells originate from the epidermis on both sides across the midline (Orgogozo et al., 2004), the origin of this sensory organ is mysterious.

During sensory organ development, is it possible that a single vas primary precursor cell originate from the midline region in the A8 segment? If so, what are the mechanisms involved in the patterning and specification of an unpaired cell?
Is it possible that two vas primary precursor cells appear on both sides across the midline during sensory organ development? If so, what are the mechanisms that lead to the formation of a single vas organ later during sensory organ development?




3) Function of the interommatidial bristles in the Drosophila adult eye
   
    Between ommatidia in the adult Drosophila eye are small mechanosensory bristles named interommatidial bristles. Their function is unknown.
These small bristles develop during the early pupal stage after most photoreceptor cells have been specified. Each bristle group is formed by four cells: socket cell, shaft cell, sheath cell and neuron (Cagan and Ready, 1989). The socket and shaft cells degenerate in pupal life, leaving the neuron and the sheath cell in the adult (Perry, 1968). Since interommatidial bristles probably originate from a typical mechanosensory cell lineage (Lai  and Orgogozo, 2004), a glial cell is also likely to originate from the interommatidial bristle lineage.
The formation of interommatidial bristles depends on the proneural genes achaete and scute. In scute^10-1 mutants, no interommatidial bristles are formed (Frankfort et al., 2004).
Since the thermal transient receptor potential channel Pyrexia accumulates in the interommatidial bristles neurons (Lee et al., 2005), interommatidial bristles might be involved in tolerance to high temperature.

What is the function of interommatidial bristles? to sense the leg during eye cleaning? to measure speed during flight? to respond to high temperatures? to guide axon pathways via their lineage-associated glial cells?
The function of interommatidial bristles can be tested using scute mutant eye clones.




4) Evolution of the interommatidial bristle pattern in flies

     Interommatidial bristles vary in density, length and shape accross fly species (Grimaldi, 1990). The ancestral pattern appears to be sparse bristles (about one bristle for 20 facets) (Grimaldi, 1990). Derived from this condition is a high density of bristles, with 3 bristles surrounding a facet (Grimaldi, 1990), as in D. melanogaster (Wolff and Ready, 1993). Mitotic labeling and anti-Senseless staining indicates that interommatidial bristle development starts in the center of the eye and spreads radially to reach the perimeter several hours later (Cagan and Ready, 1989; Wolff and Ready, 1993; Frankfort et al., 2004). As all other cell types in the eye develop in a posterior to anterior fashion, interommatidial bristle patterning must involve mechanisms that are distinct from eye patterning. The specification of interommatidial bristles is independent of EGFR signaling (Frankfort et al., 2004).

What are the molecular mechanisms involved in the ancestral patterning of interommatidial bristles? Does it involve a classic Notch-mediated lateral inhibition mechanism?
What molecular mechanisms have been added/modified during evolution to account for the derived high density of bristles that perfectly matches the number of facets in the center of the eye?




5) Gene(s) and mutation(s) responsible for an evolutionary change in the abdominal PNS pattern in D. busckii

    In D. busckii, the abdominal PNS pattern is identical to the one observed in D. melanogaster except that the es organ vp4 in the ventral region is missing (Orgogozo and Schweisguth, 2004). Analysis of sensory development in D. busckii suggests that the precursor cells of the vp4 organ are generated but undergo apoptosis (md-solo lineage, Orgogozo and Schweisguth, 2004). D. busckii belongs to the Dorsilopha subgenus. Two other members of this subgroup have been described (Toda, 1986) but to our knowledge, none of them is maintained in laboratory.

What is the abdominal PNS pattern in the two other known members of the Dorsilopha subgenus?
If it differs from D. busckii, would it be possible to cross both species for several generations in order to find the genomic regions involved in this morphological difference?
Good candidate genes are the pro-apoptotic genes reaper and grim. Could one perform species-specific in situ hybridization against reaper or grim in an F1 hybrid from both species to test whether a change in the regulatory region of reaper or grim are responsible for this morphological change?

References

Cagan R.L., Ready, D.F. 1989. The emergence of order in the Drosophila pupal retina. Dev Biol. 136, pp. 346-62. Medline

Campos-Ortega, J.-A. and Hartenstein, V. 1997. The embryonic development of Drosophila melanogaster. Berlin/Heidelberg/New-York/Tokyo.: Springer-Verlag.

Dambly-Chaudiere, C. and Ghysen, A. 1986. The sense organs in the Drosophila larva and their relation to embryonic pattern of sensory neurons. Roux's Arch. Dev. Biol. 195, pp. 222-228.

Frankfort B.J., Pepple K.L., Mamlouk M., Rose M.F., Mardon G. 2004. Senseless is required for pupal retinal development in Drosophila. Genesis 38, pp. 182-94.  Medline

Grimaldi, D.A. 1990. A phylogenetic revised classification of genera in the Drosophilidae (Diptera). Bull. Ann. Mus. Nat. Hist. 197, pp. 1–139.

Lai E.C., Orgogozo V. 2004. A hidden program in Drosophila peripheral neurogenesis revealed: fundamental principles underlying sensory organ diversity. Dev Biol. 269, pp. 1-17. Medline

Lee Y., Lee Y., Lee J., Bang S., Hyun S., Kang J., Hong S.T., Bae E., Kaang B.K., Kim J. 2005. Pyrexia is a new thermal transient receptor potential channel endowing tolerance to high temperatures in Drosophila melanogaster. Nat Genet. 37, pp. 305-10. Medline

Merritt, D. J. and Whitington, P. M. 1995. Central projections of sensory neurons in the Drosophila embryo correlate with sensory modality, soma position, and proneural gene function. J Neurosci 15, pp. 1755-67. Medline
(please note that the nomenclature used in this paper for dorsal and ventral md neuron does not fully correspond to the nomenclature used here)

Orgogozo, V., Schweisguth, F. and Bellaiche, Y. 2004. Slit-Robo signalling prevents sensory cells from crossing the midline in Drosophila. Mech Dev. 121, pp. 427-36. Medline

Orgogozo V., Schweisguth, F. 2004. Evolution of the larval peripheral nervous system in Drosophila species has involved a change in sensory cell lineage. Dev Genes Evol. 214, pp. 442-52. Medline

Perry, M.M., 1968. Further studies on the development of the of Drosophila melanogaster: II. The interommatidial bristles. J. Morphol. 124, pp. 249– 262.

Toda, M.J. 1986. Drosophilidae (Diptera) in Burma. I. The subgenus Dorsilopha Surtevant of the genus Drosophila, with descriptions of two new species. Kontyu 54, pp. 282–290.

Wolf, T. and Ready, D.F. 1993. Pattern formation in the Drosophila retina. In The development of Drosophila melanogaster. Volume II. Eds. Michael Bate and Alfonso Martinez Arias. Cold Spring Harbor Laboratory Press, pp. 1277-1325.

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