Sex-inducing effects toward planarians widely present among parasitic flatworms

Kiyono Sekii; Soichiro Miyashita; Kentaro Yamaguchi; Ikuma Saito; Yuria Saito; Sayaka Manta; Masaki Ishikawa; Miyu Narita; Taro Watanabe; Riku Ito; Mizuki Taguchi; Ryohei Furukawa; Aoi Ikeuchi; Kayoko Matsuo; Goro Kurita; Takashi Kumagai; Sho Shirakashi; Kazuo Ogawa; Kimitoshi Sakamoto; Ryo Koyanagi; Noriyuki Satoh; Mizuki Sasaki; Takanobu Maezawa; Madoka Ichikawa-Seki; Kazuya Kobayashi

doi:10.1016/j.isci.2022.105776

Sex-inducing effects toward planarians widely present among parasitic flatworms

iScience. 2022 Dec 8;26(1):105776. doi: 10.1016/j.isci.2022.105776. eCollection 2023 Jan 20.

Authors

Kiyono Sekii¹, Soichiro Miyashita¹, Kentaro Yamaguchi¹, Ikuma Saito¹, Yuria Saito¹, Sayaka Manta¹, Masaki Ishikawa¹, Miyu Narita¹, Taro Watanabe¹, Riku Ito¹, Mizuki Taguchi², Ryohei Furukawa², Aoi Ikeuchi³, Kayoko Matsuo⁴, Goro Kurita⁵, Takashi Kumagai⁶, Sho Shirakashi⁷, Kazuo Ogawa⁸, Kimitoshi Sakamoto¹, Ryo Koyanagi⁹, Noriyuki Satoh⁹, Mizuki Sasaki¹⁰, Takanobu Maezawa¹¹, Madoka Ichikawa-Seki³, Kazuya Kobayashi¹

Affiliations

¹ Department of Biology, Faculty of Agriculture and Life Science, Hirosaki University, Bunkyo-cho 3, Hirosaki, Aomori 036-8561, Japan.
² Department of Biology, Research and Education Center for Natural Sciences, Keio University, 4-1-1 Hiyoshi, Kohoku-ku, Yokohama, Kanagawa 223-8521, Japan.
³ Laboratory of Veterinary Parasitology, Faculty of Agriculture, Iwate University, 3-18-8 Ueda, Morioka, Iwate 020-8550, Japan.
⁴ Faculty of Applied Biological Sciences, Gifu University, 1-1 Yanagido, Gifu 501-1193, Japan.
⁵ Kurita Animal Hospital, 139-1 Koga, Koga, Ibaraki 306-0016, Japan.
⁶ Section of Environmental Parasitology, Graduate School, Tokyo Medical & Dental University, 1-5-45, Yushima, Bunkyo-ku, Tokyo 113-8510, Japan.
⁷ Aquaculture Research Institute, Kindai University, Shirahama 3153, Nishimuro-gun, Wakayama 649-2211, Japan.
⁸ Meguro Parasitological Museum, 4-1-1 Shimo-Meguro, Meguro, Tokyo 153-0064, Japan.
⁹ Marine Genomics Unit, Okinawa Institute of Science and Technology Graduate University, Onna, Okinawa 904-0495, Japan.
¹⁰ Department of Parasitology, Asahikawa Medical University, 2-1-1-1 Midorigaoka-Higashi, Asahikawa, Hokkaido 078-8510, Japan.
¹¹ Department of Integrated Science and Technology, National Institute of Technology, Tsuyama College, 624-1 Numa, Tsuyama, Okayama 708-8509, Japan.

Abstract

Various parasitic flatworms infect vertebrates for sexual reproduction, often causing devastating diseases in their hosts. Consequently, flatworms are of great socioeconomic and biomedical importance. Although the cessation of parasitic flatworm sexual reproduction is a major target of anti-parasitic drug design, little is known regarding bioactive compounds controlling flatworm sexual maturation. Using the planarian Dugesia ryukyuensis, we observed that sex-inducing substances found in planarians are also widespread in parasitic flatworms, such as monogeneans and flukes (but not in tapeworms). Reverse-phase HPLC analysis revealed the sex-inducing substance(s) eluting around the tryptophan retention time in the fluke Calicophoron calicophorum, consistent with previous studies on the planarian Bipalium nobile, suggesting that the substance(s) is likely conserved among flatworms. Moreover, six of the 18 ovary-inducing substances identified via transcriptome and metabolome analyses are involved in purine metabolism. Our findings provide a basis for understanding and modifying the life cycles of various parasitic flatworms.

Keywords: Developmental genetics; Parasitology.