Yolk Formation in a Stony Coral Euphyllia ancora (Cnidaria, Anthozoa): Insight Into the Evolution of Vitellogenesis in Nonbilaterian Animals

Abstract

Vitellogenin (Vg) is a major yolk protein precursor in numerous oviparous animals. Numerous studies in bilateral oviparous animals have shown that Vg sequences are conserved across taxa and that Vgs are synthesized by somatic-cell lineages, transported to and accumulated in oocytes, and eventually used for supporting embryogenesis. In nonbilateral animals (Polifera, Cnidaria, and Ctenophora), which are regarded as evolutionarily primitive, although Vg cDNA has been identified in 2 coral species from Cnidaria, relatively little is known about the characteristics of yolk formation in their bodies. To address this issue, we identified and characterized 2 cDNA encoding yolk proteins, Vg and egg protein (Ep), in the stony coral Euphyllia ancora. RT-PCR analysis revealed that expression levels of both Vg and Ep increased in the female colonies as coral approached the spawning season. In addition, high levels of both Vg and Ep transcripts were detected in the putative ovarian tissue, as determined by tissue distribution analysis. Further analyses using mRNA in situ hybridization and immunohistochemistry determined that, within the putative ovarian tissue, these yolk proteins are synthesized in the mesenterial somatic cells but not in oocytes themselves. Furthermore, Vg proteins that accumulated in eggs were most likely consumed during the coral embryonic development, as assessed by immunoblotting. The characteristics of Vg that we identified in corals were somewhat similar to those of Vg in bilaterian oviparous animals, raising the hypothesis that such characteristics were likely present in the oogenesis of some common ancestor prior to divergence of the cnidarian and bilaterian lineages.

Testicular somatic cells in the stony coral Euphyllia ancora express an endogenous green fluorescent protein

“…However, few studies have examined the characteristics and function of gonadal somatic cells in corals. Previously, the authors of the present study have found that several types of yolk proteins are produced by the ovarian somatic cells adjacent to oocytes and are then transported to and accumulate in oocytes during oogenesis in the stony coral Euphyllia ancora (Shikina, Chiu, Lee, & Chang, 2015;Shikina et al, 2013). These findings clearly demonstrate that gonadal somatic cells are specialized to support oocyte development and play a crucial role in coral oogenesis.…”

“…Characteristic differences in somatic tissues/cells between males and females remain unclear. Our previous study has demonstrated that yolk protein synthesis occurs in ovarian somatic cells in E. ancora , and the expression of these yolk proteins is rarely detected in testicular cells (Shikina et al, , Shikina, Chung et al, ). The present study immunohistochemically demonstrated that the expression of GFP is mainly observed in the testicular somatic cells, with lower expression in ovarian somatic cells.…”

“…For instance, the single gametogenic cycle requires approximately half a year in males and a year in females, and annual spawning occurs during a short period in April or May every year (Shikina et al, ). In addition, techniques for the isolation of different parts of polyp tissues (e.g., testis, ovary, tentacle, and mesenterial filament) from living corals have been established in this species of coral (Shikina et al, ), facilitating investigations of differences among different parts of polyp tissues at mRNA and protein levels (Shikina et al, ).…”

Two vitellogenins in the loliginid squidUroteuthis edulis: Identification and specific expression in ovarian follicles

“…Although VTG is suggested to be synthesized by somatic cells in the putative ovarian tissue of the coral Euphyllia ancora , a diploblast cnidarian considered to be a long divergent branch of metazoans (Shikina et al, ), our present report of VTG expression solely in ovarian tissue, without transport by hemolymph, is unique; in other invertebrates, such as crustaceans, VTG is synthesized in the hepatopancreas and ovary (Subramoniam, ), while in insects it is synthesized in the fat body (Tufail et al, ) and in nematodes it is reportedly produced in the intestine (Wahli, ). Ovary‐specific expression of VTG was reported in the abalone (Matsumoto, Yamano, Kitamura, & Hara, ) and the oyster (Matsumoto, Nakamura, Mori, & Kayano, ; Ni et al, ), which are species belonging to the same molluscan group as cephalopods.…”

De novo transcriptome assembly from the gonads of a scleractinian coral, Euphyllia ancora: Molecular mechanisms underlying scleractinian gametogenesis

“…Gonad isolation not only requires an understanding of polyp anatomy, but also technical skill. The present study applied previously established techniques for gonad isolation from E. ancora polyps [12] to the current transcriptomic study. Bioinformatics methods to eliminate contigs from symbiotic dino agellates or other contaminants were also employed [31].…”