Ultrastructural study of vitellogenesis in Maritrema feliui (Digenea, Microphallidae)

Abstract

During vitellogenesis in the microphallid trematode Maritrema feliui, we distinguished four stages: (I) a stem cell stage of the gonial type; (II) an early differentiation stage with the main cell activity concentrated on the initiation of protein synthetic activity and the beginning of shell globule formation; (III) an advanced differentiation stage concentrated on a rapid intensification of protein synthetic activity, the progressive fusion of individual shell globules into large shell globule clusters and the formation of saturated lipid droplets and a small amount of β-glycogen particles in the peripheral cytoplasm, considered as a store of nutritive reserves for the developing embryos; and (IV) the mature vitellocyte. Early vitellocyte maturation is characterised by: (1) an increase in cell volume; (2) extensive development of large, labyrinth-like cisternae of GER that produce proteinaceous granules; (3) the development of Golgi complexes engaged in packaging this material; and (4) a continuous enlargement of proteinaceous granules within vacuoles and their transformation into shell globule clusters composed of the heterogeneous material observed during vitellocyte cytodifferentiation. Mature vitelline cells are very rich in two types of cell inclusions accumulated in large amounts in their cytoplasm: (1) shell globule clusters, which play an important role in eggshell formation; and (2) a few osmiophobic lipid droplets of a saturated nature that undoubtedly represent nutritive reserves for the developing embryos. In addition, there are small numbers of β-glycogen particles in the peripheral cytoplasm of mature vitellocytes of this species. The general pattern and ultrastructure of vitellogenesis in M. feliui greatly resembles those observed in another microphallid trematode, Maritrema linguilla, in other digeneans and in some lower cestodes. Quantitative and qualitative variations in lipids (saturated and unsaturated) and glycogen (α-glycogen rosettes and β-glycogen particles) during platyhelminth vitellogenesis between the different species of trematodes and some lower cestodes are identified and discussed.

Ultrastructural evidence for completion of the entire miracidial maturation in intrauterine eggs of the digenean Brandesia turgida (Brandes, 1888) (Plagiorchiida: Pleurogenidae)

“…In particular, the variations in maternal characteristics such as uterine structure and development may reflect differences in the maternal strategies in establishing larval readiness for progression to the next stage of the life cycle (Conn 1987, 1993; Conn and Forman 1993; Conn et al 2009; Świderski et al 2012). The early eggs of B. turgida , like those of Maritrema feliui (Świderski et al 2011a, 2013b), in comparison with the early eggs of two species of bothriocephalidean cestodes Bothriocephalus clavibothrium (Świderski and Mokhtar 1974; Świderski 1994b; Świderski and Mackiewicz 2007a, b) and Clestobothrium crassiceps (Świderski et al 2013c) as well as caryophyllidean cestode Khawia sinensis (Bruňanská et al 2012) contain a much smaller number of vitellocytes per fertilized ovum. However, during the in utero development of B. turgida eggs, both nutritive and protective functions of the vitelline cells and embryonic envelopes are taken over by the uterus.…”

Ultrastructure of the vitellarium in the digeneans Phyllodistomum angulatum (Plagiorchiida, Gorgoderidae) and Azygia lucii (Strigeida, Azygiidae)

“…The sequential cytodifferentiation of immature vitelline cells assumes the production and subsequent accumulation in their cytoplasm of several inclusions, including vitelline globules, lipid droplets and glycogen. It is apparent from previous descriptions of vitelline cells that a number of differences exist between the composition and amount of these inclusions in various digenean species (Tulloch and Shapiro 1957;Koulish 1969;Irwin and Threadgold 1970;Hanna 1976;Grant et al 1977;Irwin and Maguire 1979;Erasmus et al 1982;Fukuda et al 1983;Holy and Wittrock 1986;Fairweather et al 1988;Hendow and James 1989;Podvyaznaya 1990Podvyaznaya , 2003Sharma and Swarnakar 1992;Chaymardanov and Tanyüksel 1995;Świderski et al 2011).…”

Ultrastructural characteristics of the vitellarium of Brandesia turgida (Brandes, 1888) (Digenea: Pleurogenidae) and an examination of the potential usefulness of such vitelline traits in digenean systematics

“…It belongs to the family Pleurogenidae Looss, 1899, a group which is included in the large superfamily Microphalloidea Ward, 1901 along with 17 other families (Bray et al, 2008). Ultrastructural investigations of vitellogenesis in the Digenea have previously been undertaken by Tulloch and Shapiro (1957), Björkman and Thorsell (1963), Burton (1963), Koulish (1969), Irwin and Thread-.... gold (1970), Hanna (1976), Grant et al (1977), Irwin and Maguire (1979), Erasmus et al (1982), Fukuda et al (1983), Holy and Wittrock (1986), Hendow and James (1989), Podvyaznaya (1990Podvyaznaya ( , 2003, Sharma and Swarnakar (1992), Chaymardanov and Tanyüksel (1995), Sampour (2008), Świderski et al (2011Świderski et al ( ), Poddubnaya et al (2012 and Greani et al (2012a, b). Although little attention has been paid to the study of the ultrastructural architecture of the digenean vitellarium itself, three aspects of vitelline cytoarchitecture have been suggested as possibly useful phylogenetic indicators for digeneans (Poddubnaya et al, 2012) and for parasitic platyhelminths in general (Poddubnaya et al, 2013).…”

“…In relation to this, no members of the family Pleurogenidae have been studied in terms of their vitelline ultrastructure, but, within the superfamily Microphalloidea, species of three other families, i.e. the Microphallidae (see Hendow & James, 1989;Świderski et al, 2011), the Lecithodendriidae (see Podvyaznaya, 1990) and the Gyrabascidae (see Podvyaznaya, 2003), have been investigated. In the present study, the ultrastructure of the vitellarium of Brandesia turgida (Plagiorchiida: Pleurogenidae), a parasite which lives in crypts within the intestinal wall of the frog Pelophylax ridibundus (Pallas, 1771) [=Rana ridi-HELMINTHOLOGIA, 50, 2: 119 -126, 2013 Ultrastructural characteristics of the vitellarium of Brandesia turgida (Brandes, 1888) (Digenea: Pleurogenidae) and an examination of the potential usefulness of such vitelline traits in digenean systematics …”