Light-avoidance-mediating photoreceptors tile the Drosophila larval body wall

Photoreceptors for visual perception, phototaxis or light avoidance are typically clustered in eyes or related structures such as the Bolwig organ of Drosophila larvae. Unexpectedly, we found that the class IV dendritic arborization neurons of Drosophila melanogaster larvae respond to ultraviolet, violet and blue light, and are major mediators of light avoidance, particularly at high intensities. These class IV dendritic arborization neurons, which are present in every body segment, have dendrites tiling the larval body wall nearly completely without redundancy. Dendritic illumination activates class IV dendritic arborization neurons. These novel photoreceptors use phototransduction machinery distinct from other photoreceptors in Drosophila and enable larvae to sense light exposure over their entire bodies and move out of danger.

[1]  D. Steven THE DERMAL LIGHT SENSE , 1963, Biological reviews of the Cambridge Philosophical Society.

[2]  John Tyler Bonner,et al.  Morphogenesis , 1965, The Physics of Living Matter: Space, Time and Information.

[3]  M. Sanders Handbook of Sensory Physiology , 1975 .

[4]  G A Chapman,et al.  Observations of solar irradiance variability. , 1981, Science.

[5]  Richard L. Martin,et al.  The Drosophila ninaE gene encodes an opsin , 1985, Cell.

[6]  G. Rubin,et al.  Rescue of the Drosophila phototransduction mutation trp by germline transformation. , 1985, Science.

[7]  S. Benzer,et al.  Transcript localization of four opsin genes in the three visual organs of Drosophila; RH2 is ocellus specific , 1988, Nature.

[8]  M. Saito,et al.  Expression of ion channels and mutational effects in giant Drosophila neurons differentiated from cell division-arrested embryonic neuroblasts , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  H. Steller,et al.  Genetic control of programmed cell death in Drosophila. , 1994, Science.

[10]  C. Zuker,et al.  Genetic dissection of mechanosensory transduction: Mechanoreception-defective mutations of drosophila , 1994, Neuron.

[11]  H. Steller,et al.  The head involution defective gene of Drosophila melanogaster functions in programmed cell death. , 1995, Genes & development.

[12]  M. Sokolowski,et al.  Characterization and genetic analysis of Drosophila melanogaster photobehavior during larval development. , 1995, Journal of neurogenetics.

[13]  Kendal Broadie,et al.  Gliotactin, a novel transmembrane protein on peripheral glia, is required to form the blood-nerve barrier in drosophila , 1995, Cell.

[14]  G. Rubin,et al.  P element insertion-dependent gene activation in the Drosophila eye. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[15]  W. A. Johnson,et al.  Ripped Pocket and Pickpocket, Novel Drosophila DEG/ENaC Subunits Expressed in Early Development and in Mechanosensory Neurons , 1998, The Journal of cell biology.

[16]  Liqun Luo,et al.  Mosaic Analysis with a Repressible Cell Marker for Studies of Gene Function in Neuronal Morphogenesis , 1999, Neuron.

[17]  J. Phillips,et al.  The role of extraocular photoreceptors in newt magnetic compass orientation: parallels between light-dependent magnetoreception and polarized light detection in vertebrates. , 2001, The Journal of experimental biology.

[18]  M. Ohkura,et al.  A high signal-to-noise Ca2+ probe composed of a single green fluorescent protein , 2001, Nature Biotechnology.

[19]  Roger C. Hardie,et al.  Visual transduction in Drosophila , 2001, Nature.

[20]  Yuh Nung Jan,et al.  Tiling of the Drosophila epidermis by multidendritic sensory neurons. , 2002, Development.

[21]  W. A. Johnson,et al.  Enhanced Locomotion Caused by Loss of the Drosophila DEG/ENaC Protein Pickpocket1 , 2003, Current Biology.

[22]  Y. Jan,et al.  Dendrites of Distinct Classes of Drosophila Sensory Neurons Show Different Capacities for Homotypic Repulsion , 2003, Current Biology.

[23]  Gilles Laurent,et al.  painless, a Drosophila Gene Essential for Nociception , 2003, Cell.

[24]  E. Bamberg,et al.  Channelrhodopsin-2, a directly light-gated cation-selective membrane channel , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[25]  A. Wong,et al.  Two-Photon Calcium Imaging Reveals an Odor-Evoked Map of Activity in the Fly Brain , 2003, Cell.

[26]  Brigitte Bogert,et al.  The fragile X-related Gene Affects the Crawling Behavior of Drosophila Larvae by Regulating the mRNA Level of the DEG/ENaC Protein Pickpocket1 , 2004, Current Biology.

[27]  Esteban O. Mazzoni,et al.  Circadian Pacemaker Neurons Transmit and Modulate Visual Information to Control a Rapid Behavioral Response , 2005, Neuron.

[28]  K. Yau,et al.  Non-image-forming ocular photoreception in vertebrates , 2005, Current Opinion in Neurobiology.

[29]  P. Garrity,et al.  The Drosophila ortholog of vertebrate TRPA1 regulates thermotaxis. , 2005, Genes & development.

[30]  G. Nagel,et al.  Light-Induced Activation of Distinct Modulatory Neurons Triggers Appetitive or Aversive Learning in Drosophila Larvae , 2006, Current Biology.

[31]  Chung-Hui Yang,et al.  Projections of Drosophila multidendritic neurons in the central nervous system: links with peripheral dendrite morphology , 2007, Development.

[32]  Feng Zhang,et al.  Nociceptive Neurons Protect Drosophila Larvae from Parasitoid Wasps , 2007, Current Biology.

[33]  Jeffrey C. Hall,et al.  Rhythm Defects Caused by Newly Engineered Null Mutations in Drosophila's cryptochrome Gene , 2007, Genetics.

[34]  K. Deisseroth,et al.  Circuit-breakers: optical technologies for probing neural signals and systems , 2007, Nature Reviews Neuroscience.

[35]  K. Deisseroth,et al.  optical technologies for probing neural signals and systems , 2007 .

[36]  Simon G. Sprecher,et al.  Switch of rhodopsin expression in terminally differentiated Drosophila sensory neurons , 2008, Nature.

[37]  S. Edwards,et al.  A Novel Molecular Solution for Ultraviolet Light Detection in Caenorhabditis elegans , 2008, PLoS biology.

[38]  Zhaoyang Feng,et al.  Light-sensitive neurons and channels mediate phototaxis in C. elegans , 2008, Nature Neuroscience.

[39]  W. A. Johnson,et al.  Sensory mechanisms controlling the timing of larval developmental and behavioral transitions require the Drosophila DEG/ENaC subunit, Pickpocket1. , 2008, Developmental biology.

[40]  H. Amrein,et al.  Atypical expression of Drosophila gustatory receptor genes in sensory and central neurons , 2008, The Journal of comparative neurology.

[41]  C. Montell,et al.  Control of thermotactic behavior via coupling of a TRP channel to a phospholipase C signaling cascade , 2008, Nature Neuroscience.

[42]  Chun-Fang Wu,et al.  Effects of Hyperkinetic, a β Subunit of Shaker Voltage-Dependent K+ Channels, on the Oxidation State of Presynaptic Nerve Terminals , 2008, Journal of neurogenetics.

[43]  Stefan R. Pulver,et al.  An internal thermal sensor controlling temperature preference in Drosophila , 2008, Nature.

[44]  N. Perrimon,et al.  Culture of Drosophila primary cells dissociated from gastrula embryos and their use in RNAi screening , 2009, Nature Protocols.

[45]  K. Yau,et al.  Phototransduction Motifs and Variations , 2009, Cell.

[46]  Sreekanth H. Chalasani,et al.  Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators , 2009, Nature Methods.

[47]  S. Halford,et al.  VA Opsin-Based Photoreceptors in the Hypothalamus of Birds , 2009, Current Biology.

[48]  Tao Xu,et al.  C. elegans phototransduction requires a G protein-dependent cGMP pathway and a taste receptor homolog , 2010, Nature Neuroscience.

[49]  Stefan R. Pulver,et al.  Analysis of Drosophila TRPA1 reveals an ancient origin for human chemical nociception , 2010, Nature.

[50]  Richard Y. Hwang,et al.  Pickpocket Is a DEG/ENaC Protein Required for Mechanical Nociception in Drosophila Larvae , 2010, Current Biology.