The brachyceran de novo gene PIP82, a phosphorylation target of aPKC, is essential for proper formation and maintenance of the rhabdomeric photoreceptor apical domain in Drosophila

Autor: Emma Bergh, Andrew C. Zelhof, Markus Friedrich, Simpla Mahato, Lauren E. Feder, Jonathan Rylee, Matthew E. Larsen, Steven G. Britt, Xulong Liang
Jazyk: angličtina
Rok vydání: 2020
Předmět:
Photoreceptors
Male
Cancer Research
Sensory Receptors
Light
Transcription
Genetic
Vision
Social Sciences
QH426-470
Biochemistry
Animals
Genetically Modified
0302 clinical medicine
Animal Cells
Loss of Function Mutation
Medicine and Health Sciences
Psychology
Drosophila Proteins
Post-Translational Modification
Phosphorylation
Genetics (clinical)
Phylogeny
Protein Kinase C
Neurons
0303 health sciences
biology
Drosophila Melanogaster
Physics
Electromagnetic Radiation
Intracellular Signaling Peptides and Proteins
Eukaryota
Cell Polarity
Gene Expression Regulation
Developmental
Cell Differentiation
Animal Models
Rhabdomere
Biological Evolution
Cell biology
Insects
medicine.anatomical_structure
Experimental Organism Systems
Physical Sciences
Sensory Perception
Drosophila
Female
Photoreceptor Cells
Invertebrate
Drosophila melanogaster
Cellular Types
Anatomy
Visual phototransduction
Research Article
Signal Transduction
Lineage (genetic)
Arthropoda
Ocular Anatomy
Research and Analysis Methods
Retina
03 medical and health sciences
Model Organisms
Microscopy
Electron
Transmission
Ocular System
medicine
Genetics
Animals
Molecular Biology
Ecology
Evolution
Behavior and Systematics
030304 developmental biology
Diptera
Cell Membrane
Organisms
Biology and Life Sciences
Afferent Neurons
Proteins
Cell Biology
Apical membrane
Subcellular localization
biology.organism_classification
Invertebrates
Cellular Neuroscience
Phototransduction
Animal Studies
Eyes
Head
030217 neurology & neurosurgery
Neuroscience
Zdroj: PLoS Genetics, Vol 16, Iss 6, p e1008890 (2020)
PLoS Genetics
ISSN: 1553-7404
1553-7390
Popis: The Drosophila apical photoreceptor membrane is defined by the presence of two distinct morphological regions, the microvilli-based rhabdomere and the stalk membrane. The subdivision of the apical membrane contributes to the geometrical positioning and the stereotypical morphology of the rhabdomeres in compound eyes with open rhabdoms and neural superposition. Here we describe the characterization of the photoreceptor specific protein PIP82. We found that PIP82’s subcellular localization demarcates the rhabdomeric portion of the apical membrane. We further demonstrate that PIP82 is a phosphorylation target of aPKC. PIP82 localization is modulated by phosphorylation, and in vivo, the loss of the aPKC/Crumbs complex results in an expansion of the PIP82 localization domain. The absence of PIP82 in photoreceptors leads to misshapped rhabdomeres as a result of misdirected cellular trafficking of rhabdomere proteins. Comparative analyses reveal that PIP82 originated de novo in the lineage leading to brachyceran Diptera, which is also characterized by the transition from fused to open rhabdoms. Taken together, these findings define a novel factor that delineates and maintains a specific apical membrane domain, and offers new insights into the functional organization and evolutionary history of the Drosophila retina.
Author summary Photoreceptors are the critical cells for detecting light. Changes in their morphology, organization and wiring in visual systems can greatly influence light sensitivity and visual acuity. Here we address the role of the protein PIP82 in regulating photoreceptor morphology and its potential role in the adaptive transformation from fused to open rhabdoms in insect photoreceptor organization. Our data indicate PIP82 is a downstream effector molecule of a conserved transcriptional pathway regulating photoreceptor differentiation. However, our phylogenetic analysis demonstrates that PIP82 is not present in all insects. PIP82 presence correlates with the appearance of open rhabdoms in brachyceran flies and the specialization of the photoreceptor apical domain into two distinct functional domains, the rhabdomere and stalk membrane. We find PIP82 only localizes to the rhabdomere apical domain. Moreover, the localization of PIP82 is regulated by aPKC dependent phosphorylation revealing a cellular mechanism to potentially delineate the boundary between the two apical domains of open rhabdoms. Loss of function analysis demonstrates PIP82 is necessary to generate and maintain rhabdomere morphology via the proper localization of proteins to the rhabdomere. Taken together our findings reveal a process in which a potential de novo protein intersects with known regulators of apical/basal polarity and cellular trafficking which facilitated the evolutionary transition from fused to open rhabdoms in early brachyceran flies.
Databáze: OpenAIRE
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