Stem cells from innate sexual but not acquired sexual planarians have the capability to form a sexual individual

Abstract

Planarian species may harbor as many as three populations with different reproductive strategies. Animals from innate asexual (AS) and innate sexual (InS) populations reproduce only by fission and cross-fertilization, respectively, whereas the third population switches seasonally between the two reproductive modes. AS worms can be experimentally sexualized by feeding them with minced InS worms; we termed the resulting animals "acquired sexual" (AqS) worms. Both AqS and InS worms exhibit sexualizing activity when used as feed, suggesting that they maintain their sexual state via endogenous sexualizing substances, although the mechanisms underlying determination of reproductive strategy and sexual switching in these metazoans remain enigmatic. Therefore, we compared the endogenous sexualizing activity of InS worms and AqS worms. First, we amputated mature worms and assessed if they could re-enter a sexual state. Regenerants of InS worms, but not AqS worms, were only sexual, indicating that sexual state regulation comprises two steps: (1) autonomous initiation of sexualizing substance production and (2) maintenance of the sexual state by continuous production of sexualizing substances. Next, InS neoblasts were characterized by transplantation, finding that they successfully engrafted, proliferated, and replaced all recipient cells. Under such conditions, the AS recipients of InS worm neoblasts, but not those of AqS worms, became sexual. These results clearly show that there is a neoblast-autonomous determination of reproductive strategy in planarians.

Why isn’t sex optional? Stem-cell competition, loss of regenerative capacity, and cancer in metazoan evolution

“…Observations in planaria suggest a more subtle form of competition between germline and nongermline stem cells. Asexual planaria can be sexualized by feeding them sexual planaria (Hoshi et al 2003;Nodono et al 2012) or by transplanting totipotent stem cells (neoblasts) from sexual planaria into (Nodono et al 2012;Guedelhoefer and Sánchez Alvarado 2012). Unlike neoblasts of asexual planaria, those of sexual planaria both encode and express instructions for making germ cells and gonadal structures.…”

Establishment of a new method to isolate viable x‐ray‐sensitive cells from planarian by fluorescence‐activated cell sorting

“…To understand the proliferation of neoblasts and the following regeneration processes, the transplantation experiment of the purified neoblasts into the x‐ray‐irradiated neoblasts‐less planarians is a powerful approach. In the previous reports, wild type of neoblasts were transplanted into the x‐ray‐irradiated eye‐deficient mutants of Dugesia ryukyuensis and successfully induced the regeneration of the head, including the eyes (Kobayashi et al, 2008; Nodono et al, 2012). Furthermore, in another species of planarian, Schmidtea mediterranea , x‐ray‐irradiated planarians were rescued by transplantation of a single cell, indicating that all types of cells can be generated from a single cell (Wagner et al, 2011; Zeng et al, 2018).…”

Effects of aluminum on the behavior and regeneration of planarian

“…Most importantly, their anatomical and physiological nature makes them most suitable for toxicity studies. Planarians have a short life cycle and both sexual and asexual reproduction forms, which are beneficial features for researchers [8]. Furthermore, the development and regeneration of the body occurs approximately within one week, thereby rendering the observation of regeneration to be conducted within a short period [9].…”