Sub-cellular Localisation of the White/Scarlet ABC Transporter to Pigment Granule Membranes Within the Compound Eye of Drosophila Melanogaster

The white, scarlet, and browngenes of Drosophila melanogasterencode ABC transporters involved with the uptake and storage of metabolic precursors to the red and brown eye colour pigments. It has generally been assumed that these proteins are localised in the plasma membrane and transport precursor molecules from the heamolymph into the eye pigment cells. However, the immuno-electron microscopy experiments in this study reveal that the White and Scarlet proteins are located in the membranes of pigment granules within pigment cells and retinula cells of the compound eye. No evidence of their presence in the plasma membrane was observed. This result suggests that, rather than tranporting tryptophan into the cell across the plasma membrane, the White/Scarlet complex transports a metabolic intermediate (such as 3-hydroxy kynurenine) from the cytoplasm into the pigment granules. Other functional implications of this new finding are discussed. This revised version was published online in July 2006 with corrections to the Cover Date.     

The compound eye of<Emphasis Type="Italic"> Scutigera coleoptrata</Emphasis> (Linnaeus, 1758) (Chilopoda: Notostigmophora): an ultrastructural reinvestigation that adds support to the Mandibulata concept

The lateral compound eye of Scutigera coleoptrata was examined by electron microscopy. Each ommatidium consists of a dioptric apparatus, formed by a cornea and a multipartite eucone crystalline cone, a bilayered retinula and a surrounding sheath of primary pigment and interommatidial pigment cells. With reference to the median eye region, each cone is made up of eight cone segments belonging to four cone cells. The nuclei of the cone cells are located proximally outside the cone near the transition area between distal and proximal retinula cells. The connection between nuclear region and cone segment is via a narrow cytoplasmic strand, which splits into two distal cytoplasmic processes. Additionally, from the nuclear region of each cone cell a single cytoplasmic process runs in a proximal direction to the basement membrane. The bilayered rhabdom is usually made up of the rhabdomeres of 9–12 distal retinula cells and four proximal retinula cell. The pigment shield is composed of primary pigment cells (which most likely secrete the corneal lens) and interommatidial pigment cells. The primary pigment cells underlie the cornea and surround, more or less, the upper third of the crystalline cone. By giving rise to the cornea and by functioning as part of the pigment shield these pigment cells serve a double function. Interommatidial pigment cells extend from the cornea to the basement membrane and stabilise the ommatidium. In particular, the presence of cone cells, primary pigment cells as well as interommatidial pigment cells in the compound eye of S. coleoptrata is seen as an important morphological support for the Mandibulata concept. Furthermore, the phylogenetic significance of these cell types is discussed with respect to the Tetraconata.     

The compound eye in the opaque-eye phenotype ofDrosophila melanogaster

The compound eye of the opaque-eye mutant ofDrosophila melanogaster was investigated by means of electron microscopy to determine the morphological and physical properties of ommatidial elements. These elements in the mutant were found to differ from those of the wild-type flies in the following ways: (1) The cuticular lens was thinner than that of the control and lacked the typical lamellar construction. (2) The Semper cells were irregular in shape and contained many membranous inclusions similar to those found in degenerating cells; also their nuclei contained virus-like particles. (3) The primary pigment cells contained an abundance of drosopterin-containing granules which were lacking in those of wild-type flies. (4) The superior and inferior central photoreceptor cells were misplaced and their rhabdomeres evidenced some degeneration. (5) The secondary pigment cells had only one type of pigment granules instead of the three types found in the control. These morphological changes in ommatidial elements induced physical abnormalities such as the apparent opaqueness of the eye, the lack of a pseudopupil, the probable disability of the photoreceptor cells to respond to light and the inability of the dioptric system to produce utilizable geometrical images.     

Requirement of the roughest gene for differentiation and time of death of interommatidial cells during pupal stages of Drosophila compound eye development

The roughest locus of Drosophila melanogaster encodes a transmembrane protein of the immunoglobulin superfamily required for several developmental processes, including axonal pathfinding in the developing optic lobe, mechanosensory bristle differentiation and myogenesis. In the compound eye, rst was previously shown to be required for establishing the correct number and spacing of secondary and tertiary pigment cells during the final steps of ommatidial assembly. We have further investigated its function in the developing pupal retina by performing a developmental and molecular analysis of a novel dominant rst allele, rst(D). In addition to showing evidence that rst(D) is a regulatory mutant, the results strongly suggest a previously unnoticed role of the rst gene in the differentiation of secondary/tertiary pigment cell fate as well as establishing the correct timing of surplus cell removal by programmed cell death in the compound eye.     

大草蛉成虫复眼的外部形态及其显微结构

用扫描电镜和光学显微镜观察了大草蛉Chrysopa pallens Ramber成虫复眼的外部形态及明、暗适应和性别对其显微结构的影响。结果发现：（1）其复眼呈半球形,位于头部两侧,略成“八”字形排列,单个复眼约由3 600个小眼组成,最前和最后小眼之间的夹角约为180°,最上和最下小眼之间的夹角约200°;（2）小眼主要由角膜、晶锥和6～8个小网膜细胞、基膜组成,外围环绕有2个初级虹膜色素细胞和6个次级虹膜色素细胞,基膜处有色素颗粒分布;（3）暗适应时,晶锥开裂程度较大,远端5～7个网膜细胞核向远端移动,与晶锥近端相接或接近,次级虹膜色素颗粒亦向远端移动包围晶锥;明适应时,晶锥开裂程度小或闭合,远端网膜细胞核向近端移动,透明带显现,大部分次级虹膜色素颗粒亦向近端移动分布在小网膜细胞柱周围,包被透明带;（4）在相同的明、暗适应下,雌、雄成虫复眼的显微结构无明显差异。结果表明大草蛉复眼为透明带明显的重叠象眼,其小眼不但具有次级虹膜色素颗粒纵向移动的常规调光机制,还存在晶锥开闭、远端网膜细胞核移动和基膜色素颗粒纵向扩散的调光新机制。     

Evidence for hemocyanin formation in the compound eye of Squilla mantis (Crustacea,Stomatopoda)

Summary In the retina and in the subretinal space of the compound eye of Squilla mantis a special kind of pigment cell is present. The crystalline inclusions of this cell have been identified as hemocyanin, as determined (i) by the dimensional congruence of the crystalline substructure with the dimensions of isolated, purified hemocyanin, and (ii) by the immunofluorescence reaction using anti-hemicyanin antibodies. The ultrastructure of these cells, their location and the presence of crystalline bodies in their cytoplasm suggest that they are sites of hemocyanin synthesis and homologous to the cyanocytes or cyanoblasts of Limulus.Supported by grant No. 3,012-0.76 of the Swiss National Science Foundation     

南五台蝎蛉成虫复眼的超微结构

采用扫描电镜和组织切片法,观察南五台蝎蛉Panorpa nanwutaina Chou成虫复眼的超微结构。南五台蝎蛉复眼近半椭球形,包括1500～1600个小眼。小眼表面光滑,由角膜、晶体、2个初级和12个次级色素细胞、视杆、以及基膜组成。角膜为多层片状纤维结构;晶体含有4个晶锥细胞;视杆由若干个视网膜细胞组成。晶体、视杆周围、和色素细胞内含有大量的色素颗粒,基膜两侧也有色素颗粒分布。南五台蝎蛉的复眼属于并列像眼。与普通蝎蛉P.communis L.小眼的次级色素细胞数目不同。讨论了南五台蝎蛉角膜的功能以及感觉毛和次级色素细胞在分类中的作用。     

Post-larval development of compound eyes and stemmata of Chaoborus crystallinus (De Geer, 1776) (Diptera : Chaoboridae): Stage-specific reconstructions within individual organs of vision

During metamorphosis, the dioptric apparatus of the larval compound eye of Chaoborus crystallinus (Diptera : Nematocera) is radically reconstructed. The thin larval cornea of the ommatidia is replaced by strongly curved corneal lenses, and the eucone larval cone is replaced by an imaginal cone of the acone type. Curvature of the future lens is already apparent in very young pupae, in which the cornea consists only of a thin epicuticle with corneal nipples. Fibrillary cuticle is secreted by cone and primary pigment cells throughout pupal development. Lens formation is accompanied by movement of the nuclei of the accessory pigment cells. The larval cone disintegrates unexpectedly late in young, images. During late pupal development, 7 cone cell projections emerge. In contrast to the dioptric apparatus, the retinula cells and rhabdom remain almost unchanged during metamorphosis. The main refractive element of the larval ommatidium appears to be the cone, while that of the imaginal ommatidium is the corneal lens. In addition to the compound eyes, the pairs of stemmata are retained during the whole post-larval development. Pupal stemmata show no structural differences from the larval stemmata. The stemmata are still present in 2-day-old images (“retained stemmata”), but the primary stemma loses its dioptric apparatus and is proximally relocated to the basal region of the compound eye. The reconstructions in the visual system of Chaoborus, which occur during ontogeny, are probably connected with the change from aquatic living larvae to aerial adults, and appear to fulfill stage-specific needs of vision.     

Regional differences in a nematoceran retina (Insecta,Diptera)

Summary The compound eye of Psychoda cinerea comprises two types of ommatidia, arranged so as to divide the retina into distinct dorsal and ventral regions. The P-type ommatidium, in the ventral part of the eye, differs fundamentally from the other dipteran ommatidia so far described, and is regarded as a primitive ommatidium. The acone dioptric apparatus is the same in both types, with a spherical lens and four Semper cells, the processes of which expand below the rhabdom to form a ring of pigment sacs. Only the distal region of the rhabdom is surrounded by a continuous ring of screening pigment, formed by 2 primary and 12–16 secondary pigment cells. The highly pigmented retinula cells penetrate the basement membrane proximally at about the level of their nuclei; in this region they are separated from the hemolymph by glial elements. The rhabdomeres R1–6 are fused to form a tube. The two types of ommatidia are defined by the arrangement of the retinula cells R7/8: in the T type the central rhabdomeres are one below the other, in the usual tandem position, whereas in the P type only R8 is central, with R7 in the peripheral ring. In the proximal region of the retina, retinula cells with parallel microvilli in neighboring ommatidia are joined in rows by lateral processes from the R8 cells. All the rhabdomeres are short and not twisted, which suggests that the retinula cells are highly sensitive to direction of polarization. The eye can adapt by a number of retinomotor processes. These findings, together with observations of behavior, imply that the psychodids have well-developed visual abilities.     

Fas ligand (CD95 ligand) controls angiogenesis beneath the retina

A principal cause of blindness is subretinal neovascularization associated with age-related macular degeneration. Excised neovascular membranes from patients with age-related macular degeneration demonstrated a pattern of Fas+ new vessels in the center of the vascular complex, surrounded by FasL+ retinal pigment epithelial cells. In a murine model, Fas (CD95)-deficient (Ipr) and FasL-defective (gld) mice had a significantly increased incidence of neovascularization compared with normal mice. Furthermore, in gld mice there is massive subretinal neovascularization with uncontrolled growth of vessels. We found that cultured choroidal endothelial cells were induced to undergo apoptosis by retinal pigment epithelial cells through a Fas-FasL interaction. In addition, antibody against Fas prevented vascular tube formation of choroidal endothelial cells derived from the eye in a three-dimensional in vitro assay. Thus, FasL expressed on retinal pigment epithelial cells may control the growth and development of new subretinal vessels that can damage vision.     

Post emergence maturation of the eye of the adult black carpet beetle,Attagenus megatoma (Fab.): An electron microscope study

The black carpet beetle, Attagenus megatoma (Fab.), has been reported to exhibit negative phototaxis immediately after emergence. In later adult life, after the period during which most oviposition has occurred, the beetles are found to be photopositive. The compound eyes of one-day-old (Post-emergence) and nine-day-old (Post-ovipositional) female beetles were studied by electron microscopy and a number of strong differences were found between eyes at the two ages. The corneal facets of one-day eyes had the form of convex-concave lenses, while those of nine-day beetles were double-convex lenses. The primary and secondary pigment cells of young eyes were large and contained much endoplasmic reticulum and little accessory pigment. In the older eyes the pigment cells were reduced and contained much pigment, the proportion of endoplasmic reticulum being greatly reduced by comparison with the one-day eye. The cross-sectional area of the rhabdom was greater in the older eye. The possible relationships between age-related changes in eye morphology and behavioral changes during the same period are discussed.     

A Scanning Electron Microscope Study on the Internal Structure of the Peritreme of the Female Mite Varroa jacobsoni (Oudemans, 1904)

The peritreme of the adult female mite Varroa jacobsoni is located laterally above coxa III and is enclosed within a peritrematal shield which has a slit at the end. The peritrematal shield is cuticular in nature. The peritreme is lined with a thick inner membrane which has numerous tooth-like projections. The outer membrane of the peritreme is thin and smooth. In between these two membranes is a layer of columnar cells. The internal structure of the peritreme in relation to the female mite's ability to adjust to different atmospheric conditions is discussed.     

An apposition‐like compound eye with a layered rhabdom in the small diving beetle Agabus japonicus (Coleoptera,Dytiscidae)

The fine structure of the compound eyes of the adult diving beetle Agabus japonicus is described with light, scanning, and transmission electron microscopy. The eye of A. japonicus is mango‐shaped and consists of about 985 ommatidia. Each ommatidium is composed of a corneal facet lens, an eucone type of crystalline cone, a fused layered rhabdom with a basal rhabdomere, seven retinula cells (including six distal cells and one basal cell), two primary pigment cells and an undetermined number of secondary pigment cells that are restricted to the distalmost region of the eye. A clear‐zone, separating dioptric apparatus from photoreceptive structures, is not developed and the eye thus resembles an apposition eye. The cross‐sectional areas of the rhabdoms are relatively large indicative of enhanced light‐sensitivity. The distal and central region of the rhabdom is layered with interdigitating microvilli suggesting polarization sensitivity. According to the features mentioned above, we suggest that 1) the eye, seemingly of the apposition type, occurs in a taxon for which the clear‐zone (superposition) eye is characteristic; 2) the eye possesses adaptations to function in a dim‐light environment; 3) the eye may be sensitive to underwater polarized light or linearly water‐reflected polarized light. J. Morphol. 275:1273–1283, 2014. © 2014 Wiley Periodicals, Inc.     

THE DEVELOPMENT OF PIGMENT GRANULES IN THE EYES OF WILD TYPE AND MUTANT DROSOPHILA MELANOGASTER

The eye pigment system in Drosophila melanogaster has been studied with the electron microscope. Details in the development of pigment granules in wild type flies and in three eye color mutants are described. Four different types of pigment granules have been found. Type I granules, which carry ommochrome pigment and occur in both primary and secondary pigment cells of ommatidia, are believed to develop as vesicular secretions by way of the Golgi apparatus. The formation of Type II granules, which are restricted to the secondary pigment cells and contain drosopterin pigments, involves accumulation of 60- to 80-A fibers producing an elliptical granule. Type III granules appear to be empty vesicles, except for small marginal areas of dense material; they are thought to be abnormal entities containing ommochrome pigment. Type IV granules are characteristic of colorless mutants regardless of genotype, and during the course of development they often contain glycogen, ribosomes, and show acid phosphatase activity; for these reasons and because of their bizarre and variable morphology, they are considered to be autophagic vacuoles. The 300-A particles commonly found in pigment cells are identified as glycogen on the basis of their morphology and their sensitivity to salivary digestion.     

Terminal synthesis of xanthommatin in Drosophila melanogaster. II. Enzymatic formation of the phenoxazinone nucleus

Xanthommatin, the brown eye pigment of Drosophila melanogaster is a phenoxazinone compound formed by the bimolecular oxidative condensation of 3-hydroxykynurenine. Evidence is presented in this report for an enzyme system in drosophila which catalyzes the formation of the phenoxazinone chromophore of xanthommatin. This enzyme system, which is separable from the interfering activities of phenol oxidase and cytochrome oxidase, is relatively inactive in crude extracts but can be activated either by heat treatment or by passage through Sephadex G-50. The preliminary characterization of several properties of the enzyme-catalyzed reaction and their biological significance are discussed.Supported by USPHS grant GM12323 and by the Robert A. Welch Foundation, Houston, Texas.Postdoctoral Fellow supported by USPHS (1 FO2 GM44, 562-01) and the Rosalie B. Hite Memorial Fund.     

The effect of temperature onshibire ts cell clones in the compound eye ofDrosophila melanogaster

Summary We have analysed the effect of temperature on both developing and adult eye cell clones homozygous forshi ^ST139, a temperature-sensitive mutant ofDrosophila melanogaster. The mutant gene, autonomous in its cellular expression, causes structural modifications of ommatidial cells when adult clones of cells are exposed to the restrictive temperature (29°C) for several days. However, the mutant phenotype reverses to normal within 4 days at the permissive temperature (20°C). The results of pulse, shift-up and shift-down experiments show that the temperaturesensitive period for developing compound eye cells is from the late second instar up to the early pupa. Cytodifferentiation of compound eye cells is blocked by restrictive temperature treatment during this period, whereas cell proliferation does not seem to be directly affected. These results are discussed with regard to the other known aspects of the phenotype observed in mutant individuals.     

Defective expression of the mu3 subunit of the AP-3 adaptor complex in the Drosophila pigmentation mutant carmine

The adaptor protein (AP) complexes AP-1, AP-2, and AP-3 mediate coated vesicle formation and sorting of integral membrane proteins in the endocytic and late exocytic pathways in mammalian cells. A search of the Drosophila melanogaster expressed sequence tag (EST) database identified orthologs of family members mammalian medium (μ) chain families μ1, μ2, and μ3, of the corresponding AP complexes, and δ-COP, the analogous component of the coatomer (COPI) complex. The Drosophila orthologs exhibit a high degree of sequence identity to mammalian medium chain and δ-COP proteins. Northern analysis demonstrated that medium chain and δ-COP mRNAs are expressed uniformly throughout fly development. Medium chain and δ-COP genes were cytologically mapped and the μ3 gene was found to localize to a region containing the pigmentation locus carmine (cm). Analysis of genomic DNA of the cm ¹ mutant allele indicated the presence of a large insertion in the coding region of the μ3 gene and Northern analysis revealed no detectable μ3 mRNA. Light microscopy of the cm ¹ mutant showed a reduction in primary, secondary, and tertiary pigment granules in the adult eye. These findings provide evidence of a role for μ3 in the sorting processes required for pigment granule biogenesis in Drosophila. Received: 7 June 1999 / Accepted: 4 July 1999     

The emergence of order in the Drosophila pupal retina

During pupation, long-range order is imposed on the autonomously developing ommatidia which compose the Drosophila eye. To accomplish this, eight additional cell types arise: the primary, secondary, and tertiary pigment cells, and the four cells that form the bristle. These cells form an interweaving lattice between ommatidia. The lattice is refined when excess cells are removed to bring neighboring ommatidia into register. Recent evidence suggests that in larval development, local contacts direct cell fate. The same appears to be true during pupal development: the contacts a cell makes predict the cell type it will become. Cells which contact the anterior or posterior cone cells in an ommatidium invariably become primary pigment cells. Cells which contact primary pigment cells from different ommatidia become secondary and tertiary pigment cells. Bristle development is in several ways distinct from ommatidial development. The four cells of each bristle group appear to be immediate descendents of a single founder cell. During their early differentiation, they do not make stereotyped contacts with surrounding ommatidial cells, but do make particular contacts within the bristle group. And unlike the surrounding ommatidia, differentiation of the bristles radiates from the center of the eye to the edges. As cells are removed during two stages of programmed cell death, the bristles are brought into their final position. When all cells in the lattice have achieved their final position, a second stage of retinal development begins as structures specific to each cell type are produced. This paper follows these various stages of pupal development, and suggests how local cell-cell contacts may produce the cells needed for a functional retina.     

Eye color pigment granules in Drosophila mauritiana: mosaics produced by excision of a transposable element

Compound eyes of the white-peach (wpch) mutant strain of Drosophila mauritiana have some pigment and receptor cells with wild-type eye color pigmentation. These eyes are mosaic, because excision of a transposable element reverts wpch to wild type during the development of somatic cells. Wild-type patches have three types of pigment granule residing in three respective cell types: primary pigment cells, secondary pigment cells, and retinula (visual receptor) cells. Most aspects of these granules, as well as all other aspects of compound eye ultrastructure, are exactly as in the better studied sibling species D. melanogaster. In the wpch parts of the eye, small and giant unpigmented "pigment granules" reside in secondary pigment cells. These white granules are just like the corresponding granules of w mutant D. melanogaster. Small vs. large patches of pigmented cells likely represent excision events occurring late vs. early respectively during development. Mosaics of eye color markers have been important in developmental analyses; the ease of constructing mosaics of D. mauritiana gives this preparation advantages for mosaic analyses.     

Structure and functional aspects of the scotopic compound eye of the sugarcane borer moth

Morphology and functional aspects of the scotopic compound eye of the moth Diatraea saccharalis, studied using light and electron microscopy, is presented. An ommatidium is composed of a laminate corneal lens, four Semper cells, a refractive cone, two primary pigment cells, six screening pigment cells, a crystalline tract that functions as an optical waveguide, and six to eight sensory retinular cells. Accessory light regulators consist of screening pigment cells that, in the dark-adapted position, increase receptor sensitivity by permitting light rays to cross over to adjacent ommatidia and specialized tracheal regions that enhance sensitivity by reflecting light back toward sensory receptors.