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Daphnia Magna Eri Sumiya1,2, Yukiko Ogino1,2†, Hitoshi Miyakawa2†, Chizue Hiruta2, Kenji Toyota1,2, Shinichi Miyagawa1,2 and Taisen Iguchi1,2*

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Daphnia Magna Eri Sumiya1,2, Yukiko Ogino1,2†, Hitoshi Miyakawa2†, Chizue Hiruta2, Kenji Toyota1,2, Shinichi Miyagawa1,2 and Taisen Iguchi1,2* Sumiya et al. Frontiers in Zoology 2014, 11:60 http://www.frontiersinzoology.com/content/11/1/60 RESEARCH Open Access Roles of ecdysteroids for progression of reproductive cycle in the fresh water crustacean Daphnia magna Eri Sumiya1,2, Yukiko Ogino1,2†, Hitoshi Miyakawa2†, Chizue Hiruta2, Kenji Toyota1,2, Shinichi Miyagawa1,2 and Taisen Iguchi1,2* Abstract Introduction: Daphnia magna exhibits a parthenogenetic reproductive cycle linked to a moulting cycle, but regulatory mechanisms of neither moulting nor reproductive cycle are understood in daphnids. Moulting is regulated by ecdysteroids in insects. A previous study showed that a titre of ecdysteroids changed during the reproductive cycle in D. magna; however, no clear correlation among titre, moulting and reproductive cycles has been proved in daphnids. To understand endocrine mechanisms underlying the coordinated reproductive cycle, we analysed the expression of genes coding for enzymes in ecdysteroids synthesis or inactivation pathways, and the effects of 20-hydroxyecdysone (20E) on moulting and ovulation in D. magna. Results: We cloned orthologues of neverland (nvd) and shade (shd) in the ecdysteroids synthesis pathway, and Cyp18a1 in the ecdysteroids inactivation pathway previously identified in insects. Gene expression of Cyp18a1 changed conversely with the fluctuation in ecdysteroids titre during the intermoulting period. Tissue-specific expression analysis of nvd showed a prominent expression in the gut. Furthermore, treatment of adult female D. magna with 20E inhibited moulting and/or ovulation. Conclusions: Our cloning and phylogenetic analyses showed that nvd and shd as well as Cyp18a1 are evolutionary conserved in D. magna, suggesting that these genes appeared in arthropods before the radiation of insects. The gene expression analysis during the reproductive cycle indicated that Cyp18a1 possibly regulates the decline of ecdysteroid titre before moulting and ovulation. Furthermore, the expression of nvd in the gut suggested that ecdysone might be synthesised in the gut. Exogenous 20E-treatment resulted in the failure of not only moulting, but also ovulation, suggesting that a low level of ecdysteroids before moulting is required for moulting and ovulation in D. magna. Keywords: Daphnia magna, Ecdysteroids, Moulting, Reproductive cycle, 20-hydroxyecdysone Introduction involving ecdysteroids, neuropeptides, biogenic amines, Crustacea and Insecta comprising monophyletic group, opioids, juvenile hormones, and vertebrate-type steroids the Pancrustacea, are the most diverse animal group in [3]. Daphnids show characteristic features in reproduction. aquatic habitats [1]. Reproductive diversity as an adapta- They reproduce parthenogenetically every three days tion to environmental conditions may have facilitated under favourable conditions, and the reproductive cycle the radiation of crustaceans [2]. Reproduction of decapod occurs synchronously with the moulting cycle. After crustaceans is regulated by complex endocrine mechanisms moulting, mother daphnids ovulate new eggs from the ovary into the brood pouch (ovulation). At the end of each * Correspondence: [email protected] reproductive cycle, the mother releases the brood from †Equal contributors the pouch to the surrounding water. After this release, the 1Faculty of Life Science, Graduate University for Advanced Studies mother moults again and repeats the cycle. These events (SOKENDAI), 5-1 Higashiyama Myodaiji, Okazaki, Aichi 444-8787, Japan 2Okazaki Institute for Integrative Bioscience, National Institute for Basic occur in a very systematic order with intervals that span Biology, National Institutes of Natural Sciences, and Department of Basic approximately three days depending on the condition. Biology, 5-1 Higashiyama Myodaiji, Okazaki, Aichi 444-8787, Japan © 2014 Sumiya et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Sumiya et al. Frontiers in Zoology 2014, 11:60 Page 2 of 12 http://www.frontiersinzoology.com/content/11/1/60 Consequently, a closely related system might regulate the [20]. The synthetic organ in decapods is the Y-organ. moulting and reproductive cycle. A similar association of However, the organ that synthesises and secretes ecdysone moulting with a reproductive cycle has also been reported has not been identified in microcrustaceans, including in other crustaceans such as amphipods, isopods, shrimps, daphnids. Some reports have speculated that these species prawns and a sand crab [4,5]. However, regulation of the may synthesise ecdysone in the epidermis [15,21,22] since reproductive cycle remains largely unknown in most ecdysone production in the epidermis was observed crustaceans. in vitro in the tick Ornithodoros parkeri [23]. Identifica- Ecdysteroids (ecdysone and 20-hydroxyecdysone; 20E) tion of the endocrine organ is essential to understand are steroid hormones that regulate moulting and meta- the endocrine system of daphnids. morphosis in insects. These have been extensively studied As an entry point to understand the roles of ecdyster- in insects, and are commonly called “moulting hormones” oids in the reproductive cycle in D. magna, we cloned as their major role implies. Recent studies in insects re- genes of three key enzymes for 20E synthesis or inactiva- vealed that ecdysteroids have a variety of functions besides tion: nvd,shd and Cyp18a1. Spacio-temporal expression moulting in the control of reproduction and embryogen- analyses of these genes during the reproductive cycle indi- esis [6]. In Drosophila melanogaster, ecdysteroids are re- cated that ecdysone is possibly synthesised in the gut, and quired for differentiation of germ line stem cells [7,8] and that the decline of the 20E titre before moulting [11] might prepupal development [9,10]. A pioneering study reported be regulated by Cyp18a1. In addition, exogenous 20E treat- that a titre of ecdysteroids increased at the premoult stage ment during the reproductive cycle resulted in a failure of and decreased back to the basal level before moulting in moulting and ovulation, suggesting that a low level of ecdys- Daphnia magna [11], indicating that ecdysteroids are pre- teroids before moulting is required for successful moulting dominant moulting hormones. However, in crustaceans, and ovulation in D. magna. The present study provides reports on ecdysteroidal regulation in both moulting and insight into the endocrine system that regulates the reproduction are scarce [4]. The synchronised moulting highly coordinated reproductive system in crustaceans. and reproductive cycle in daphnids implies a possibility that ecdysteroids may regulate not only moulting, but also the reproductive cycle. Results In insects, biosynthesis of ecdysteroids starts with dietary Molecular cloning and phylogenetic analysis of genes in cholesterol. Rieske oxygenase DAF-36 (neverland, nvd) 20E synthesis or inactivation pathway in D. magna converts it to 7-dehydrocholesterol [12]. After several We cloned full-length of nvd encoding 444 amino acids steps mediated by enzymes belonging to the cytochrome (a.a.), shd encoding 526 a.a. and Cyp18a1 encoding 551 P450 family (CYP450), it is converted to ecdysone. Then, a.a. from D. magna. Furthermore, we identified the Cyp314A1 (shade, shd) finally converts ecdysone into 20E, partial cDNA sequence of a distinct nvd. Aligning which is the biologically active form binding to an ecdys- amino acids of these genes with D. pulex and two one receptor (EcR) [13,14]. The complex of 20E and EcR insect species, D. melanogaster and Bombyx mori, recruits ultraspiracle (USP) in insects and daphnids or ret- revealed that both D. magna nvd contain a characteris- inoid X receptor (RXR) in decapods, and acts as a hetero- ticdomain,Rieske[2Fe-2S],andanon-hemeFe(II) dimer [15]. EcR and USP have been cloned in D. magna motif (Figure 1A) [12]. The obtained shd and Cyp18a1 [16]. Three EcR paralogues with five distinct N-terminus belonging to the P450 family have a P/G-rich domain sequences and one USP were identified [16]. These genes and five conserved P450 motifs: Helix-C, Helix-I, in the ecdysteroids biosynthesis pathway except for nvd Helix-K, PERF and Heme-binding (Figure 1B) [24]. belong to CYP450 encoding hydroxylases. D. pulex pos- Phylogenetic analysis was conducted by comparing sesses five CYP450 genes: spook, phantom, disembodied, the amino acid sequences of the obtained nvd, shd and shadow and shd [17]. In decapod crustaceans, Cyp306A1 Cyp18a1 with other available arthropod sequences. In (phantom)inkurumaprawn(Marsupenaeus japonicus) each obtained tree, D. manga and D. pulex clustered to- [18], and four CYP450s (spook, phantom, disembodied and gether with other arthropods, forming a monophyletic shadow)andnvd in cray fish (Pontastacus leptodactylus) group. This suggests that the orthologous genes of nvd, [19] have been identified to date. However, neither gene shd and Cyp18a1 were identified in D. magna.Twoof expression nor functional analyses have been explored the D. magna nvd were assembled in the Daphnia nvd in microcrustaceans such as copepoda, phyllopoda and cluster. These nvd paralogoues
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