Fine structure of the eyes of Pseudoceros canadensis (Turbellaria,Polycladida)

Summary The cerebral and epidermal ocelli of the Müller's larva and the cerebral and tentacular eyes of the adult turbellarian Pseudoceros canadensis were studied by electron microscopy. The right cerebral ocellus of the larva consists of one cup-shaped pigmented cell and three sensory cells that bear microvilli. The left cerebral eye of the larva has the above named cells plus a sensory cell with many cilia. Evolutionary significance is attributed to the presence of both ciliary and microvillar photoreceptors in an eye of a flatworm. The one epidermal ocellus of the larva is composed of two cells: a cup-shaped pigmented one bearing flattened cilia, the presumed photoreceptors, and a cell above the cup that adds a few nonciliary lamellae to the stack of ciliary ones from the pigmented cell. The adult eyes contain only microvillar receptors; cilia were not observed.     

Evolution of cerebral vesicles and their sensory organs in an ascidian larva

Sorrentino M., Manni L., Lane N. J. and Burighel P. 2000. Evolution of cerebral vesicles and their sensory organs in an ascidian larva. —Acta Zoologica (Stockholm) 81 : 243–258 The ascidian larval nervous system consists of the brain (comprising the visceral ganglion and the sensory vesicle), and, continuous with it, a caudal nerve cord. In most species two organs, a statocyst and an ocellus with ciliary photoreceptors, are contained in the sensory vesicle. A third presumptive sensory organ was sometimes found in an ‘auxiliary’ ganglionic vesicle. The development and morphology of the sensory and auxiliary ganglionic vesicles in Botryllus schlosseri and their associated organs was studied. The sensory vesicle contains a unique organ, the photolith, responding to both gravity and light. It consists of a unicellular statocyst, in the form of an expanded pigment cup receiving six photoreceptor cell extensions. Presumptive mechano‐receptor cells (S1 cells), send ciliary and microvillar protrusions to contact the pigment cup. A second group of distinctive cells (S2), slightly dorsal to the S1 cells, have characteristic microvillar extensions, resembling photoreceptor. We concur with the idea that the photolith is new and derived from a primitive statocyst and the S2 cells are the remnant of a primitive ocellus. In the ganglionic vesicle some cells contain modified cilia and microvillar extensions, which resemble the photoreceptor endings of the photolith. Our results are discussed in the light of two possible scenarios regarding the evolution of the nervous system of protochordates.     

Evolution of vertebrate retinal photoreception

Recent findings shed light on the steps underlying the evolution of vertebrate photoreceptors and retina. Vertebrate ciliary photoreceptors are not as wholly distinct from invertebrate rhabdomeric photoreceptors as is sometimes thought. Recent information on the phylogenies of ciliary and rhabdomeric opsins has helped in constructing the likely routes followed during evolution. Clues to the factors that led the early vertebrate retina to become invaginated can be obtained by combining recent knowledge about the origin of the pathway for dark re-isomerization of retinoids with knowledge of the inability of ciliary opsins to undergo photoreversal, along with consideration of the constraints imposed under the very low light levels in the deep ocean. Investigation of the origin of cell classes in the vertebrate retina provides support for the notion that cones, rods and bipolar cells all originated from a primordial ciliary photoreceptor, whereas ganglion cells, amacrine cells and horizontal cells all originated from rhabdomeric photoreceptors. Knowledge of the molecular differences between cones and rods, together with knowledge of the scotopic signalling pathway, provides an understanding of the evolution of rods and of the rods'' retinal circuitry. Accordingly, it has been possible to propose a plausible scenario for the sequence of evolutionary steps that led to the emergence of vertebrate photoreceptors and retina.     

Ultrastructural investigations of presumed photoreceptors as a means of discrimination and identification of closely related species of the genus Microphthalmus (Polychaeta,Hesionidae)

Summary Differences in the ultrastructure of presumed photoreceptors of three morphologically similar Microphthalmus populations on the opposite sides of the Atlantic (German North Sea coast and coasts of North Carolina and Massachusetts) suggest the existence of three different species. Only the European M. listensis possesses three pairs of prostomial eyes, of which one pair has rhabdomeric receptors and pigment cells. The two other pairs are unpigmented and can be found in all three species. The frontal one has ciliary receptors, the posterior one rhabdomeric sensory cells. An additional unpaired potential photoreceptor organ in the segment with the first pair of tentacular cirri is present in all individuals of this species complex. It has a relatively high number of cilia with numerous microvillar projections. — For each type of ocellus there are slight but distinct and constant differences among the species such as relative position of sensory cells, presence of dilations of the ciliary shafts, number of cilia, and shape of the sensory cells. Presence of both ciliary and rhabdomeric light-sensitive cells is discussed with reference to various theories of the evolution of photoreceptors.Abbreviations ax axonema - bb basal body - cc cup cell - ci cilium - cu cuticle - epc epidermal cell - g Golgi apparatus - gp glycogen particles - mi mitochondrion - mv microvilli - mvb multivesicular body - nu nucleus - pc pigment cell - pg pigment granule - rer rough ER - smc submicrovillar cysternae - sr striated rootlet     

The retinal topography of three species of coleoid cephalopod: significance for perception of polarized light

The retinal topography of three species of coleoid cephalopod (one cuttlefish, one squid and one octopus) was investigated to examine and compare the structure, density and organization of the photoreceptors. The aim was to determine if there were areas of increased cell density and/or cell specialization that might be related to lifestyle or phylogeny. The orientation of photoreceptors around the curved surface of the retina was also mapped to reveal how the overall arrangement of cell microvilli might enable the perception of polarized light stimuli. It was found that all species possessed an increase in photoreceptor density in a horizontal streak approximately placed at the position of a potential horizon in the habitat. The overall arrangement of photoreceptor microvillar arrangements followed lines of latitude and longitude in a global projection that has been rotated by 90°. This arrangement seems to map polarization sensitivities on the outside world in a vertical and horizontal grid. The potential significance of this and other retinal specializations is discussed in the context of phylogenetic and habitat differences between species.     

Microvillar orientation in the photoreceptors of the ant Cataglyphis bicolor

Polarization sensitivity in arthropod photoreceptors is crucially dependent on the arrangement of the microvilli within the rhabdom. Here, we present an electron-microscopical study in which the degree of microvillar alignment and changes in the cross-sectional areas of the rhabdoms along their length were studied in the compound eye of the desert ant, Cataglyphis bicolor. Serial cross-sections through the retina were taken and the orientation of the microvilli was determined in the photoreceptors of individually identified ommatidia. The reconstructions of microvillar alignment were made in the three anatomically and functionally distinct regions of the Cataglyphis compound eye: the dorsal rim area (DRA), the dorsal area (DA), and the ventral area (VA). The following morphological findings are consistent with polarization sensitivities measured previously by intracellular recordings. (1) The microvilli of the DRA photoreceptors are aligned in parallel along the entire length of the cell from the distal tip of the rhabdom down to its proximal end, near the basement membrane. The microvilli of the retinular cells R1 and R5 are always parallel to each other and perfectly perpendicular, with only minor deviation, to the microvillar orientation of the remaining receptor cells. (2) In the DA and VA regions of the eye, the microvillar tufts of the small receptors R1, R3, R5, R7, and R9 change their direction repetitively every 1-4 7m for up to 90°. In contrast, the large receptor cells R2, R4, R6, and R8 maintain their microvillar orientation rigidly. (3) In the DRA ommatidia, the cross-sectional areas of the rhabdomeres do not change along the length of the rhabdom, but substantial changes occur in the DA and VA ommatidia.     

Comparative morphology of photoreceptors in free-living plathelminths — a survey

In free-living Plathelminthes, the best-known photoreceptors are pigment-cup ocelli, eyes formed of one or several pigmented supportive cells into whose cup-shaped cavity project the light-sensitive elements of one or several sensory cells. Besides these, so-called Sehkolben, photoreceptors lacking pigment granules, are found in some species. Sensory cells in plathelminth photoreceptors most commonly use microvilli as the light-sensitive organelles, but some use cilia and combinations of microvilli and cilia. Lamellate ciliary bodies with cilia whose membranes are strongly flattened and rolled and pericerebral ciliary aggregations with interwoven cilia protruding into an intracellular cavity are likely photoreceptors in that they show amplification of membrane likely to bear photoreceptive pigments. Cells with ballooned cilia and tubular vacuoles are other differentiations to which light-sensitivity has been attributed. A variety of structures serve as lenses, all usually formed from parts of the pigment cell.     

Alterations of the eyes of Carinaria lamarcki (Gastropoda, Heteropoda) during the long pelagic cycle

 The eyes of different larval stages of Carinaria lamarcki were examined ultrastructurally. In all larval stages the eyes consist of a cornea, a lens and an everse retina. The photoreceptors in young larvae are exclusively of the ciliary type. In old larvae, however, two types of photoreceptors are present and the retina is composed of two segments: a posterior segment with altered ciliary photoreceptors (=type I sensory cells) and an anterior segment with what are presumably rhabdomeric photoreceptors (=type II sensory cells). The anterior retina is interpreted here as an accelerted character. Furthermore, the arrangement of the pigment granules changes during the long larval development being cup shaped in young larvae versus ribbon shaped in old larvae. The findings allow for the conclusions that: (a) the ciliary photoreceptors are correlated with the long larval period of Heteropoda and that (b) the eyes are altered continuously during the larval cycle. Accepted: 6 July 1998     

Non-neural ectoderm is really neural: evolution of developmental patterning mechanisms in the non-neural ectoderm of chordates and the problem of sensory cell homologies

In chordates, the ectoderm is divided into the neuroectoderm and the so-called non-neural ectoderm. In spite of its name, however, the non-neural ectoderm contains numerous sensory cells. Therefore, the term "non-neural" ectoderm should be replaced by "general ectoderm." At least in amphioxus and tunicates and possibly in vertebrates as well, both the neuroectoderm and the general ectoderm are patterned anterior/posteriorly by mechanisms involving retinoic acid and Hox genes. In amphioxus and tunicates the ectodermal sensory cells, which have a wide range of ciliary and microvillar configurations, are mostly primary neurons sending axons to the CNS, although a minority lack axons. In contrast, vertebrate mechanosensory cells, called hair cells, are all secondary neurons that lack axons and have a characteristic eccentric cilium adjacent to a group of microvilli of graded lengths. It has been highly controversial whether the ectodermal sensory cells in the oral siphons of adult tunicates are homologous to vertebrate hair cells. In some species of tunicates, these cells appear to be secondary neurons, and microvillar and ciliary configurations of some of these cells approach those of vertebrate hair cells. However, none of the tunicate cells has all the characteristics of a hair cell, and there is a high degree of variation among ectodermal sensory cells within and between different species. Thus, similarities between the ectodermal sensory cells of any one species of tunicate and craniate hair cells may well represent convergent evolution rather than homology.     

Isolation of the rhabdomeral microvillar cytoskeleton of the crayfish (Orconectes limosus) photoreceptor by a crosslinking reagent.

1. Rhabdomeral microvilli of photoreceptor cells of invertebrates contain a labile central cytoskeleton. For stabilization of the rhabdomeral cytoskeleton of the crayfish Orconectes limosus the crosslinking reagent suberic acid bis (N-hydroxysuccinimide ester) was used. 2. It was found that this crosslinking reagent can be successfully used to stabilize and isolate the microvillar cytoskeleton of crayfish photoreceptors. 3. After detergent treatment cytosolic proteins and the cell membranes were removed. 4. By the combined use of crosslinker and detergent the accessibility of antibodies or other markers to the microvillar cytoskeleton is possible. 5. This method may be useful, because at present little is known about the proteins associated with the central filament of invertebrate photoreceptors.     

Detection of plasma membrane cholesterol by filipin during microvillogenesis and ciliogenesis in quail oviduct

Using filipin as a probe for the presence of membrane cholesterol, the evolution of cholesterol distribution in the apical plasma membrane was studied during estrogen-induced ciliogenesis in quail oviduct and compared with the distribution of intramembrane particles (IMPs). Ciliary growth is preceded by the first step of microvillus differentiation. Microvilli emerge in membrane domains rich in IMPs and devoid of filipin-cholesterol (f-c) complexes. However growing microvillus membrane shows f-c complexes. During ciliary growth, microvilli lengthen from 0.5 to 2 microns, indicating that the microvillar membrane is not a membrane reservoir for ciliogenesis. During ciliary growth, the characteristic ciliary necklace IMP rows appear progressively at the base of cilia. The first IMP row is organized in a membrane circlet lacking of f-c complexes, whereas the new shaft membrane in the middle of the circlet exhibits numerous complexes. These two different domains of the cilia keep their specificity during ciliary growth. Only the ciliary tip shows fewer complexes than the shaft membrane. The apical membrane of differentiated ciliated cells is thus composed of various domains, the ciliary shaft full of f-c complexes and poor in IMPs, the ciliary necklace is devoid of f-c complexes and rich in IMPs, the microvilli membrane is rich in both IMPs and f-c complexes, and the interciliary membrane is poor in both f-c complexes and IMPs, whereas the undifferentiated cells exhibit an apical membrane in which f-c complexes and IMPs are distributed homogeneously.     

Ca(2+)-dependent and Ca2+ release-dependent excitation in leech photoreceptors: evidence from a novel "inside-out" cell model

We have developed a novel, electrophysiologically intact and light-sensitive "inside-out" cell model (IOCM) of microvillar photoreceptors of the leech Hirudo medicinalis. Light responses recorded from the IOCM with sharp microelectrodes are depolarizations with amplitudes of up to 50-60 mV. In darkness, graded elevations of the free Ca(2+) concentration in the "intracellular medium" (ICM) reversibly increase the conductance of the microvillar membrane leading to Ca(2+)-induced graded voltage changes up to approximately 50 mV. The threshold for Ca(2+)-induced voltage changes is approximately 0.06 microM, EC(50) is approximately 1.2 microM, and saturation occurs at approximately 20 microM free Ca(2+). Small Ca(2+) elevations (<0.6 microM) produce discrete waves of depolarization resembling quantum bumps. Stimulating IOCMs with short (20-ms) and long (5-s) light stimuli produces transient light responses (repolarization within ca. 200 ms) in an ICM containing only 10nM free Ca(2+). At 0.44 microM free Ca(2+) in the ICM, the microvillar membrane depolarizes by 10-20 mV and responses to 5-s light steps have an initial transient component and a plateau component, similar to responses in intact cells. Generation of the plateau component in IOCMs is suppressed by heparin and cyclopiazonic acid (CPA), agents that block inositol 1,4,5-trisphosphate (Ins(1,4,5)P(3))-induced Ca(2+) release from and Ca(2+) uptake into the endoplasmic reticulum (ER). These results indicate that there is a Ca(2+)-dependent conductance in the microvillar membrane and that the light-induced Ins(1,4,5)P(3)- and Ca(2+) release-mediated intracellular Ca(2+) elevation in leech photoreceptors contributes to the generation of the receptor potential, particularly the plateau component of responses to long steps of light.     

Ultrastructural study of sensory cells of the proboscidial glandular epithelium of Riseriellus occultus (Nemertea,Heteronemertea)

Only one sensory cell type has been observed within the glandular epithelium of the proboscis in the heteronemertine Riseriellus occultus. These bipolar cells are abundant and scattered singly throughout the proboscis length. The apical surface of each dendrite bears a single cilium enclosed by a ring of six to eight prominent microvilli. The cilium has the typical 9×2 + 2 axoneme arrangement and is equipped with a cross-striated vertical rootlet extending from the basal body. No accessory centriole or horizontal rootlet was observed. Large, modified microvilli (stereovilli) surrounding the cilium are joined together by a system of fine filaments derived from the glycocalyx. Each microvillus contains a bundle of actin-like filaments which anchor on the indented inner surface of a dense, apical ring situated beneath the level of the ciliary basal body. The tip of the cilium is expanded and modified to form a bulb-like structure which lies above the level where the surrounding microvilli terminate. In the region where the cilium emerges from the microvillar cone, the membrane of the microvillar apices makes contact with a corresponding portion of the ciliary membrane. At this level microvilli and cilium are apparently firmly linked by junctional systems resembling adherens junctions. The results suggest that these sensory cells may be mechanoreceptors. © 1996 Wiley-Liss, Inc.     

A direct signaling role for phosphatidylinositol 4,5-bisphosphate (PIP2) in the visual excitation process of microvillar receptors

In microvillar photoreceptors the pivotal role of phospholipase C in light transduction is undisputed, but previous attempts to account for the photoresponse solely in terms of downstream products of phosphatidylinositol 4,5-bisphosphate (PIP2) hydrolysis have proved wanting. In other systems PIP2 has been shown to possess signaling functions of its own, rather than simply serving as a precursor molecule. Because illumination of microvillar photoreceptors cells leads to PIP2 break-down, a potential role for this phospholipid in phototransduction would be to help maintain some element(s) of the transduction cascade in the inactive state. We tested the effect of intracellular dialysis of PIP2 on voltage-clamped molluscan photoreceptors and found a marked reduction in the amplitude of the photocurrent; by contrast, depolarization-activated calcium and potassium currents were unaffected, thus supporting the notion of a specific effect on light signaling. In the dark, PIP2 caused a gradual outward shift of the holding current; this change was due to a decrease in membrane conductance and may reflect the suppression of basal openings of the light-sensitive conductance. The consequences of depleting PIP2 were examined in patches of light-sensitive microvillar membrane screened for the exclusive presence of light-activated ion channels. After excision, superfusion with anti-PIP2 antibodies induced the appearance of single-channel currents. Replenishment of PIP2 by exogenous application reverted the effect. These data support the notion that PIP2, in addition to being the source of inositol trisphosphate and diacylglycerol, two messengers of visual excitation, may also participate in a direct fashion in the control of the light-sensitive conductance.     

Subcellular calcium localization and AT0-dependent Ca2+-uptake by smooth endoplasmic reticulum in an invertebrate photoreceptor cell. An ultrastrucutral, cytochemical and X-ray microanalytical study.

In Hirudo medicinalis an extensive and highly elaborate three dimensional network of smooth endoplasmic reticulum cisternae is found in very close structural relationship to the receptive (microvillar) membrane, as reported for many other invertebrates. A variant of the potassium pyroantimonate technique showed that these submicrovillar endoplasmic reticulum cisternae (SMC) and mitochondria are major intracellular calcium stores. Furthermore, using saponine-skinned photoreceptors for an in situ accumulation experiment, calcium oxalate precipitates in SMC demonstrate that this organelle is able to accumulate Ca2+ from a concentration of 2 x 10(-5) M, when ATP, Mg2+, and oxalate ions are present in the accumulation medium. This result provides direct evidence for the hypothesis that SMC may play a particularly important role in the regulation of intracellular ionized calcium in invertebrate photoreceptor cells. Morphological evidence supports this view.     

First evidence of unpigmented rhabdomeric photoreceptors in a Microstomum species (Plathelminthes, Macrostomorpha, Microstomidae) and ultrastructure of photoreceptor-like ciliary aggregations

Microstomum spiculifer possesses a pair of intracerebral photoreceptors each consisting of a single rhabdomeric sensory cell and two cup or mantle cells. The mantle cells are devoid of pigment. In addition, four so-called ciliary aggregations, presumed to have a light-sensing function, are present. Each ciliary aggregation represents a specialized cell with an internal cavity filled with axonemes of modified cilia. Rhabdomeric photoreceptors consisting of one to three sensory cells and a single pigmented or unpigmented mantle cell are widespread within taxa of the Plathelminthes Rhabditophora. On the contrary, the existence of two mantle cells forming the eye cup is only known for M. spiculifer and a few other species of the Macrostomida. Therefore, at least two hypotheses are possible: (1) two cup cells are a basic characteristic of the Rhabditophora and a reduction from two to one cup cell has occurred secondarily or (2) the stem species of the Rhabditophora possessed rhabdomeric eyes with one cup cell, and two mantle cells have evolved within the Macrostomorpha. The existence of ciliary aggregates has been documented for several taxa of the Plathelminthes Rhabditophora. From their distribution it can not be concluded whether these differentiations are either a basic feature of the Rhabditophora or have evolved several times convergently. Accepted: 26 September 1999     

New insights into the evolutionary history of photoreceptor cells

Although the common descent of all life has been widely accepted since Darwin's time, new research occasionally provides us with arresting reminders of the unity of evolutionary history. Recent papers by Arendt et al. and Panda et al. provide one such reminder. They illustrate that the two classes of animal photoreceptors, ciliary and rhabdomeric photoreceptors, are likely to share an ancient common ancestor and have been evolving in parallel since their duplication over 600 million years ago.     

Origin and evolution of animal life cycles

The ‘origin of larvae’ has been widely discussed over the years, almost invariably with the tacit understanding that larvae are secondary specializations of early stages in a holobenthic life cycle. Considerations of the origin and early radiation of the metazoan phyla have led to the conclusion that the ancestral animal (= metazoan) was a holopelagic organism, and that pelago-benthic life cycles evolved when adult stages of holopelagic ancestors became benthic, thereby changing their life style, including their feeding biology. The literature on the larval development and phylogeny of animal phyla is reviewed in an attempt to infer the ancestral life cycles of the major animal groups. The quite detailed understanding of larval evolution in some echinoderms indicates that ciliary filter-feeding was ancestral within the phylum, and that planktotrophy has been lost in many clades. Similarly, recent studies of the developmental biology of ascidians have demonstrated that a larval structure, such as the tail of the tadpole larva, can easily be lost, viz. through a change in only one gene. Conversely, the evolution of complex structures, such as the ciliary bands of trochophore larvae, must involve numerous genes and numerous adaptations. The following steps of early metazoan evolution have been inferred from the review. The holopelagic ancestor, blastaea, probably consisted mainly of choanocytes, which were the feeding organs of the organism. Sponges may have evolved when blastaea-like organisms settled and became reorganized with the choanocytes in collar chambers. The eumetazoan ancestor was probably the gastraea, as suggested previously by Haeckel. It was holopelagic and digestion of captured particles took place in the archenteron. Cnidarians and ctenophores are living representatives of this type of organization. The cnidarians have become pelago-benthic with the addition of a sessile, adult polyp stage; the pelagic gastraea-like planula larva is retained in almost all major groups, but only anthozoans have feeding larvae. Within the Bilateria, two major lines of evolution can be recognized: Protostomia and Deuterostomia. In protostomes, trochophores or similar types are found in most spiralian phyla; trochophore-like ciliary bands are found in some rotifers, whereas all other aschelminths lack ciliated larvae. It seems probable that the trochophore was the larval type of the ancestral, pelago-benthic spiralian and possible that it was ancestral in all protostomes. Most of the non-chordate deuterostome phyla have ciliary filter-feeding larvae of the dipleurula type, and this strongly indicates that the ancestral deuterostome had this type of larva.     

The ciliary rootlet maintains long-term stability of sensory cilia

The striated ciliary rootlet is a prominent cytoskeleton originating from basal bodies of ciliated cells. Although a familiar structure in cell biology, its function has remained unresolved. In this study, we carried out targeted disruption in mice of the gene for rootletin, a component of the rootlet. In the mutant, ciliated cells are devoid of rootlets. Phototransduction and ciliary beating in sensory and motile cilia initially exhibit no apparent functional deficits. However, photoreceptors degenerate over time, and mutant lungs appear prone to pathological changes consistent with insufficient mucociliary clearance. Further analyses revealed a striking fragility at the ciliary base in photoreceptors lacking rootlets. In vitro assays suggest that the rootlet is among the least dynamic of all cytoskeletons and interacts with actin filaments. Thus, a primary function of the rootlet is to provide structural support for the cilium. Inasmuch as photoreceptors elaborate an exceptionally enlarged sensory cilium, they are especially dependent on the rootlet for structural integrity and long-term survival.