A comprehensive comparison of sex-inducing activity in asexual worms of the planarian Dugesia ryukyuensis: the crucial sex-inducing substance appears to be present in yolk glands in Tricladida

Abstract

BackgroundTurbellarian species can post-embryonically produce germ line cells from pluripotent stem cells called neoblasts, which enables some of them to switch between an asexual and a sexual state in response to environmental changes. Certain low-molecular-weight compounds contained in sexually mature animals act as sex-inducing substances that trigger post-embryonic germ cell development in asexual worms of the freshwater planarian Dugesia ryukyuensis (Tricladida). These sex-inducing substances may provide clues to the molecular mechanism of this reproductive switch. However, limited information about these sex-inducing substances is available.ResultsOur assay system based on feeding sex-inducing substances to asexual worms of D. ryukyuensis is useful for evaluating sex-inducing activity. We used the freshwater planarians D. ryukyuensis and Bdellocephala brunnea (Tricladida), land planarian Bipalium nobile (Tricladida), and marine flatworm Thysanozoon brocchii (Polycladida) as sources of the sex-inducing substances. Using an assay system, we showed that the three Tricladida species had sufficient sex-inducing activity to fully induce hermaphroditic reproductive organs in asexual worms of D. ryukyuensis. However, the sex-inducing activity of T. brocchii was sufficient only to induce a pair of ovaries. We found that yolk glands, which are found in Tricladida but not Polycladida, may contain the sex-inducing substance that can fully sexualize asexual worms of D. ryukyuensis.ConclusionsOur results suggest that within Tricladida, there are one or more common compounds or functional analogs capable of fully sexualizing asexual worms of D. ryukyuensis; namely, the crucial sex-inducing substance (hydrophilic and heat-stable, but not a peptide) produced in yolk glands.Electronic supplementary materialThe online version of this article (10.1186/s40851-018-0096-9) contains supplementary material, which is available to authorized users.

Sex-inducing effects toward planarians widely present among parasitic flatworms

“…When the marine flatworm Thysanozoon brocchii , which does not have an ectolecithal egg system, and the slug Ambigolimax valentianus (non-flatworm tissue) were fed to D. ryukyuensis , none exerted a sex-inducing effect able to fully sexualize the worms. 15 These results suggest that vitellocytes are important for the production and/or storage of sex-inducing substances and that sex-inducing substances are conserved within species with an ectolecithal egg system. 15 Therefore, parasitic flatworms, which do have an ectolecithal egg system ( Figure 1 A), are expected to contain sex-inducing substances.…”

“…Images are of the flatworm species used in the present study. Bdellocephala brunnea (class Turbellaria, order Tricladida, family Dendrocoelidae) was already known to harbor sex-inducing substances 11 , 15 and, thus, was used as a positive control. Monogeneans (Monogenea): Neoheterobothrium hirame (order Mazocraeidea, family Diclidophoridae) and Neobenedenia girellae (order Capsalidea, family Capsalidae).…”

“…There are two reasons to expect the presence of sex-inducing substances in parasitic flatworms. First, although the molecular identity of sex-inducing substances has not yet been determined, these are likely conserved across species, at least within the nonparasitic planarians of the order Tricladida, 15 and the presence of sex-inducing substances in their cocoons containing numerous vitellocytes and several fertilized oocytes (i.e., ectolecithal eggs) has been reported. When the marine flatworm Thysanozoon brocchii , which does not have an ectolecithal egg system, and the slug Ambigolimax valentianus (non-flatworm tissue) were fed to D. ryukyuensis , none exerted a sex-inducing effect able to fully sexualize the worms.…”

Correction to: A comprehensive comparison of sex-inducing activity in asexual worms of the planarian Dugesia ryukyuensis: the crucial sex-inducing substance appears to be present in yolk glands in Tricladida

“…Following publication of the original article [ 1 ] the author advised that unfortunately in the ‘Discussion’ section the letters ‘L’ and ‘D’ in some ‘enantiomer’ expressions were not written in the format of ‘small capitals’. Rather, they were written as lower-case letters.…”

d-Tryptophan enhances the reproductive organ-specific expression of the amino acid transporter homolog Dr-SLC38A9 involved in the sexual induction of planarian Dugesia ryukyuensis

“…In a previous study, we found that the feeding of fresh cocoons containing numerous yolk gland cells to asexual worms caused their full sexual induction [ 22 ]. This result suggests that yolk gland cells might contain sex-inducing substance(s) that trigger full sexual induction.…”