Abstract
A new assay was designed, named checker, that measures the individual response to light in the fruitfly Drosophila melanogaster larva. In this assay the Drosophila larva apparently modulates its pattern of locomotion when faced with a choice between a dark and lit environment by orienting its movement towards the dark environment. We show that, in this assay, a response to light can be measured as an increase in residence time in the dark versus the lit quadrant. Mutations that disrupt phototransduction in the adult Drosophila abolish the larval response to light, demonstrating that this larval visual function is similar to that of the adult fly. Similarly, no response to light was detected in strains where the larval visual system (photoreceptors and target area) was disrupted by a mutation in the homeobox containing gene sine oculis (so) gene. Ablation of photoreceptors by the targeted expression of the cell death gene hid under the control of the photoreceptor-specific transcription factor glass (gl) abolishes this response entirely. Finally, we demonstrate that this response to light can be mediated by rhodopsins other than the blue absorbing Rh1.
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REFERENCES
Ashburner, M. (1989). Drosophila: A Laboratory Handbook, Cold Spring Habor Laboratory Press, Cold Spring Harbor.
Bloomquist, B. T., Shortridge, R. D., Schneuwly, S., Perdew, M., Montell, C., Steller, H., Rubin., G., and Pak., W. L. (1988). Isolation of a putative phospholipase C gene of Drosophila, norpA, and its role in phototransduction. Cell 54:723–733.
Bolwig, N. (1946). Sense and sense organs of the anterior end of the house fly larvae. Vidensk. Medd. Dan. Naturhist. Foren. 109: 81–217.
Busto, M., Iyengar, B., and Campos, A. R. (1999). Genetic dissection of behavior: Modulation of locomotion by light in the Drosophila melanogaster larva requires genetically distinct visual system functions. J. Neurosci. 19:3337–3344.
Campos, A. R., Lee, K. J., and Steller, H. (1995). Establishment of neuronal connectivity during development of the Drosophila visual system. J. Neurobiol. 28:313–329.
Cheyette, B. N. R., Green, P. J., Martin, K., Garren, H., Hartenstein, V., and Zipursky, S. L. (1994). The Drosophila sine oculis locus encodes a homeodomain-containing protein required for the development of the entire visual system. Neuron 12:997–996.
Fischbach, K. F., and Technau, G. (1984). Cell degeneration in the developing optic lobes of the sine oculis and small-optic-lobes mutants of Drosophila melanogaster. Dev. Biol. 104:219–239.
Fraenkel, G. S., and Gunn, D. L. (1961). The Orientation of Animals, Dover, New York.
Gordesky-Gold, B., Warrick, J. M., Bixler, A., Beasley, J. E., and Tompkins, L. (1995). Hypomorphic mutations in the larval photokinesis A (lphA) gene have stage-specific effects on visual system function in Drosophila melanogaster.Genetics 139: 1623–1629.
Green, P., Hartenstein, A. Y., and Hartenstein, V. (1993). The embryonic development of the Drosophila visual system. Cell Tissue Res. 273:583–598.
Grether, M. E., Abrams, J. M., Agapite, J., White, K., and Steller, H. (1995). The head involution defective gene of Drosophila melanogaster functions. Genes Dev. 9:1694–1708.
Hardie, R. C., and Minke, B. (1995). Phosphoinositide-mediated phototransduiction in Dorosophila photoreceptorsd: The role of Ca2+ and trp.Cell Calcium 18:256–274.
Hofstee, C. A., Henderson, S., Hardie, R. C., and Stavenga, D. G. (1996). Differential effects of ninaC proteins (p132 and p174) on light-activated currents and pupil mechanisms in Drosophila photoreceptors. Visual Neurosci. 13:897–906.
Kernan, M., Cowan, D., and Zuker, C. (1994). Genetic dissection of mechanosensory transduction mechanoreception-defective mutations of Drosophila. Neuron 12:1195–1206.
Kim, S., McKay, R. R., Miller, K., and Shortridge, R. D. (1995). Multiple subtypes of phospholipase C are encoded by the norpA gene of. J. Biol.Chem. 270:14376–14382.
Lilly, M., and Carlson, J. R. (1990). Smellblind: A gene required for Drosophila olfaction. Genetics 124:293–302.
Meinertzhagen, I. A., and Hanson, T. E. (1993). The development of the optic lobe. In Bate, M., and Arias, A. M., (eds.), The Development of Drosophila melanogaster, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp. 1363–1482.
Miklos, G. L. G., and Rubin, G. M. (1996). The role of the genome project in determining gene function: Insights from model organisms. Cell 86:521–529.
Monte, P., Woodard, C., Ayer, R., Lilly, M., Sun, H., and Carlson, J. R. (1989). Characterization of the larval olfactory response in Drosophila and its genetic basis.Behav. Genet. 19: 267–283.
Montell, C., and Rubin, G. M. (1988). The Drosophila ninaC locus encodes two photoreceptor cell specific proteins with domains homologous to protein kinases and the myosin heavy chain head. Cell 52:757–772.
Moses, K., Ellis, M. C., and Rubin, G. M. (1989). The glass gene encodes a zinc-finger protein required by Drosophila photoreceptor cells.Nature 340:531–536.
Osborne, K. A., Robichon, A., Burgess, E., Butland, S., Shaw, R. A., Coulthard, A., Pereira, H. S., Greenspan, R. J., and Sokolowski, M. B. (1997). Natural behavior polymorphism due to a cGMP protein kinase of Drosophila. Science 277:834–836.
O'Tousa, J. E., Leonard, D. S., and Pak, W. L. (1989). Morphological defects in Orajk84 photoreceptors caused by mutation in R1–6 opsin gene of Drosophila.J. Neurogenet. 6:41–52.
Pak, W. L., Grossfield, J., and Arnold, K. S. (1970). Mutants of the visual pathway of Drosophila melanogaster.Nature 227:518–520.
Park, Y., Caldwell, M. C., and Datta, S. (1997). Mutation of the central nervous system neuroblast proliferation repressor ana leads to defects in larval olfactory behavior.J. Neurobiol. 33:199–211.
Pearn, M. T., Randall, L. L., Shortridge, R. D., Burg, M. G., and Pak, W. L. (1996). Molecular, biochemical, and electrophysiological characterization of. J. Biol. Chem. 271:4937–4945.
Pollock, J. A., and Benzer, S. (1988). Transcript localization of four opsin genes in the three visual organs of Drosophila; RH2 is ocellus specific.Nature 333:779–782.
Porter, J. A., Hicks, J. L., Williams, D. S., and Montell, C. (1992). Differential localizations of and requirements for the two Drosophila ninaC kinase/myosins in photoreceptor cells. J. Cell. Biol. 116:683–693.
Porter, J. A., and Montell, C. (1993). Distinct roles of the Drosophila ninaC kinase and myosin domains revealed by systematic mutagenesis. J. Cell. Biol. 122:601–612.
Ranganathan, R., Malicki, D. M., and Zuker, C. S. (1995). Signal transduction in Drosophila photoreceptors. Annu. Rev. Neurosci. 18:283–317.
Sawin-McCormack, E., Sokolowski, M. B., and Campos, A. R. (1995). Characterization and genetic analysis of Drosophila melanogaster photobehavior during larval development.J. Neurogenetics 10:119–135.
Schmucker, D., Jackle, H., and Gaul, U. (1997). Genetic analysis of the larval optic nerve projection in Drosophila. Development 124:937–948.
Sehgal, A., Price, J., and Young, W. (1992). Ontogeny of a biological clock in Drosophila melanogaster.PNAS 89:1423–1427.
Serikaku, M. A., and O'Tousa, J. E. (1994). Sine oculis is a homeobox gene required for Drosophila visual system development. Genetics 138:1137–1150.
Steller, H., Fischbach, K. F., and Rubin, G. (1987). Disconnected: A locus required for neuronal pathway function in the visual system of Drosophila.Cell 50:1139–1153.
Tully, T., Cambiazo, V., and Kruse, L. (1994). Memory through metamorphosis in normal and mutant Drosophila. J. Neurosci. 14:68–74.
Zipursky, S. L., Venkatesh, T. R., Teplow, D. B., and Benzer, S. (1984). Neuronal development in the Drosophila retina: monoclonal antibodies as molecular probes. Cell 36:15–26.
Zuker, C. S., Cowman, A. F., and Rubin, G. M. (1985). Isolation and structure of a rhodopsin gene from D. melanogaster.Cell 40:851–858.
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Hassan, J., Busto, M., Iyengar, B. et al. Behavioral Characterization and Genetic Analysis of the Drosophila melanogaster Larval Response to Light as Revealed by a Novel Individual Assay. Behav Genet 30, 59–69 (2000). https://doi.org/10.1023/A:1002090627601
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DOI: https://doi.org/10.1023/A:1002090627601