Transcriptomic analysis reveals differences in the regulation of amino acid metabolism in asexual and sexual planarians

Kiyono Sekii,Hikaru Okamoto,Shuji Shigenobu,Nanna Nagao,Kazuya Kobayashi,Yasuhisa Matsui,Katsushi Yamaguchi,Shunta Yorimoto,Ryohei Furukawa,Takanobu Maezawa

doi:10.1038/s41598-019-42025-z

Abstract

Many flatworms can alternate between asexual and sexual reproduction. This is a powerful reproductive strategy enabling them to benefit from the features of the two reproductive modes, namely, rapid multiplication and genetic shuffling. The two reproductive modes are enabled by the presence of pluripotent adult stem cells (neoblasts), by generating any type of tissue in the asexual mode, and producing and maintaining germ cells in the sexual mode. In the current study, RNA sequencing (RNA-seq) was used to compare the transcriptomes of two phenotypes of the planarian Dugesia ryukyuensis: an asexual OH strain and an experimentally sexualized OH strain. Pathway enrichment analysis revealed striking differences in amino acid metabolism in the two worm types. Further, the analysis identified serotonin as a new bioactive substance that induced the planarian ovary de novo in a postembryonic manner. These findings suggest that different metabolic states and physiological conditions evoked by sex-inducing substances likely modulate stem cell behavior, depending on their different function in the asexual and sexual reproductive modes. The combination of RNA-seq and a feeding assay in D. ryukyuensis is a powerful tool for studying the alternation of reproductive modes, disentangling the relationship between gene expression and chemical signaling molecules.

Highlights

Many flatworms can alternate between asexual and sexual reproduction
We generated a catalogue of transcripts associated with the different reproduction modes of the planarian D. ryukyuensis
By investigating the expression pattern of differentially expressed genes (DEG) with high fold expression changes between the asexual and sexual modes, we found that most sexual DEGs were expressed in the testis or yolk gland, which was reasonable given that these organs are numerous and distributed throughout the planarian body (Fig. 1)

Summary

Introduction

Many flatworms can alternate between asexual and sexual reproduction. This is a powerful reproductive strategy enabling them to benefit from the features of the two reproductive modes, namely, rapid multiplication and genetic shuffling. Bioactive substances that induce the differentiation of neoblasts into germ cells and sexual reproduction (hereafter called “sex-inducing substances”) exist[9,10,11], and are broadly conserved beyond the species barrier, at least within the order Tricladida[12] These examples indicate the presence of a common molecular mechanism shared among flatworms, which controls the behavior of neoblasts depending on the reproductive mode; namely, switching between differentiation into various somatic tissues of a new clonal individual(s) in the asexual mode, and differentiation into germ cells in the sexual mode, in addition to the general stem cell functions, such as growth and tissue homeostasis[5,13]. The study of D. ryukyuensis may provide useful insights for understanding their parasitic relatives

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