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

Go Nagamatsu,Kazuya Kobayashi,Ryohei Furukawa,Takanobu Maezawa,Kiyono Sekii,Masaki Ishikawa

doi:10.1186/s40851-021-00173-z

Abstract

BackgroundMany animals switch between asexual and sexual reproduction in nature. We previously established a system for the sexual induction of planarian Dugesia ryukyuensis by feeding asexual planarians with minced sexual planarians. We identified dl-tryptophan (Trp) as one of the sex-inducing substances. dl-Trp can induce ovarian development, the first and essential step of sexual induction. d-Trp must act as a principal bioactive compound in terms of ovarian development, because the ovary-inducing activity of d-Trp was 500 times more potent than that of l-Trp. However, how Trp controls sexual induction is still unknown.ResultsIn this study, qRT-PCR analyses suggested that the putative amino acid transporter gene Dr-SLC38A9 is highly expressed in sexual worms, especially in the yolk glands. In situ hybridization analyses showed that Dr-SLC38A9 is expressed in the ovarian primordia of asexual worms and in the mature ovaries, testes, and yolk glands of sexual worms. In addition, Dr-SLC38A9 RNA interference during sexual induction resulted in the suppression of the development of reproductive organs. These results suggest that Dr-SLC38A9 is involved in the development of these organs. Moreover, we demonstrated that the reproductive organ-specific expression of Dr-SLC38A9 is enhanced by the addition of d-Trp.ConclusionWe propose that d-Trp activates the expression of Dr-SLC38A9 to promote sexual induction in the planarian D. ryukyuensis.

Highlights

Many animals switch between asexual and sexual reproduction in nature
Isolation of the putative amino acid transporter gene DrSLC38A9 in D. ryukyuensis We searched for amino acid transporter genes enriched in sexual planarians using the RNA-seq data of D. ryukyuensis [27]
We focused on the DEG data between asexual and sexual planarians and identified three annotated amino acid transporter genes (TR33723|c0_g1_i1, vesicular inhibitory amino acid transporter; TR37685|c0_g2_i3, excitatory amino acid transporter 2; and TR38642|c0_g1_i2, sodium-coupled neutral amino acid transporter 9 isoform × 1)

Summary

Introduction

Many animals switch between asexual and sexual reproduction in nature. We previously established a system for the sexual induction of planarian Dugesia ryukyuensis by feeding asexual planarians with minced sexual planarians. Some asexual planarians may develop hermaphroditic reproductive organs from neoblasts in the adult stage and undergo sexual reproduction, depending on environmental conditions [8,9,10,11,12,13]. Within approximately 1 month, asexual worms develop a pair of ovaries, yolk glands, testes, copulatory apparatus, and a genital pore, in that order (Fig. S1) [18, 19]. This sex-induction process is divided into five stages (Fig. S1) [18, 19]. Yolk gland cells are produced in the yolk gland, which is a reproductive organ unique to planarians [20, 21]

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Discussion

Conclusion