title: Speed and sensitivity of phototransduction in Drosophila depend on degree of saturation of membrane phospholipids.
abstract: Drosophila phototransduction is mediated via a G-protein-coupled PLC cascade. Recent evidence, including the demonstration that light evokes rapid contractions of the photoreceptors, suggested that the light-sensitive channels (TRP and TRPL) may be mechanically gated, together with protons released by PLC-mediated PIP2 hydrolysis. If mechanical gating is involved we predicted that the response to light should be influenced by altering the physical properties of the membrane. To achieve this, we used diet to manipulate the degree of saturation of membrane phospholipids. In flies reared on a yeast diet, lacking polyunsaturated fatty acids (PUFAs), mass spectrometry showed that the proportion of polyunsaturated phospholipids was sevenfold reduced (from 38 to ∼5%) but rescued by adding a single species of PUFA (linolenic or linoleic acid) to the diet. Photoreceptors from yeast-reared flies showed a 2- to 3-fold increase in latency and time to peak of the light response, without affecting quantum bump waveform. In the absence of Ca(2+) influx or in trp mutants expressing only TRPL channels, sensitivity to light was reduced up to ∼10-fold by the yeast diet, and essentially abolished in hypomorphic G-protein mutants (Gαq). PLC activity appeared little affected by the yeast diet; however, light-induced contractions measured by atomic force microscopy or the activation of ectopic mechanosensitive gramicidin channels were also slowed ∼2-fold. The results are consistent with mechanosensitive gating and provide a striking example of how dietary fatty acids can profoundly influence sensory performance in a classical G-protein-coupled signaling cascade.
authors: Department of Physiology Development and Neuroscience, Cambridge University, Cambridge CB2 3EG, United Kingdom.
authors: Alex S
authors: AS
authors: Randall
authors: Department of Physiology Development and Neuroscience, Cambridge University, Cambridge CB2 3EG, United Kingdom.
authors: Che-Hsiung
authors: CH
authors: Liu
authors: Department of Physiology Development and Neuroscience, Cambridge University, Cambridge CB2 3EG, United Kingdom.
authors: Brian
authors: B
authors: Chu
authors: Babraham Institute, Babraham, Cambridge CB22 3AT, United Kingdom.
authors: Qifeng
authors: Q
authors: Zhang
authors: Department of Biomedical Science, University of Sheffield, Sheffield S10 2TN, United Kingdom, and.
authors: Sidharta A
authors: http://orcid.org/0000-0003-2575-4362
authors: SA
authors: Dongre
authors: Department of Biomedical Science, University of Sheffield, Sheffield S10 2TN, United Kingdom, and National Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing 100875, China.
authors: Mikko
authors: http://orcid.org/0000-0002-4428-5330
authors: M
authors: Juusola
authors: Department of Physiology Development and Neuroscience, Cambridge University, Cambridge CB2 3EG, United Kingdom.
authors: Kristian
authors: http://orcid.org/0000-0002-8425-7297
authors: K
authors: Franze
authors: Babraham Institute, Babraham, Cambridge CB22 3AT, United Kingdom.
authors: Michael J O
authors: MJ
authors: Wakelam
authors: Department of Physiology Development and Neuroscience, Cambridge University, Cambridge CB2 3EG, United Kingdom, rch14@cam.ac.uk.
authors: Roger C
authors: http://orcid.org/0000-0001-5531-3264
authors: RC
authors: Hardie
mesh_terms: D000818:Animals; D002462:Cell Membrane / Q000378:metabolism / Q000502:physiology*; D004032:Diet; D004331:Drosophila melanogaster / Q000502:physiology*; D015640:Ion Channel Gating / Q000502:physiology; D008027:Light; D055537:Light Signal Transduction / Q000502:physiology*; D050356:Lipid Metabolism / Q000502:physiology; D010743:Phospholipids / Q000378:metabolism / Q000502:physiology*; D043562:Receptors, G-Protein-Coupled / Q000502:physiology; D012243:Rhodopsin / Q000378:metabolism; D059629:Signal-To-Noise Ratio; D019831:Sodium-Calcium Exchanger / Q000378:metabolism; D010738:Type C Phospholipases / Q000378:metabolism
chemical_list: D010743:Phospholipids; D043562:Receptors, G-Protein-Coupled; D019831:Sodium-Calcium Exchanger; D012243:Rhodopsin; D010738:Type C Phospholipases
keywords: PIP2; lipidomics; mechanosensitivity; phosphoinositide; phospholipase C; photoreceptors