Discovery of a receptor guanylate cyclase expressed in the sperm flagella of stony corals

Yan Zhang,Yu-Ying Ho,Shinya Shikina,Chuya Shinzato,Ching-Fong Chang,Chieh-Jhen Chen,Yi-Ling Chiu

doi:10.1038/s41598-019-51224-7

Yan Zhang, Yu-Ying Ho + Show 5 more

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https://doi.org/10.1038/s41598-019-51224-7

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Abstract

The receptor guanylate cyclases (rGCs) in animals serve as sensitive chemoreceptors to detect both chemical and environmental cues. In reproduction, rGCs were shown to be expressed on sperm and serve as receptors for egg-derived sperm-activating and sperm-attracting factors in some echinoderms and mammals. However, sperm-associated rGCs have only been identified in some deuterostomes thus far, and it remains unclear how widely rGCs are utilized in metazoan reproduction. To address this issue, this study investigated the existence and expression of rGCs, particularly asking if rGCs are involved in the reproduction of a basal metazoan, phylum Cnidaria, using the stony coral Euphyllia ancora. Six paralogous rGCs were identified from a transcriptome database of E. ancora, and one of the rGCs, GC-A, was shown to be specifically expressed in the testis. Immunohistochemical analyses demonstrated that E. ancora GC-A protein was expressed in the spermatocytes and spermatids and eventually congregated on the sperm flagella during spermatogenesis. These findings suggest that GC-A may be involved in the regulation of sperm activity and/or functions (e.g., fertilization) in corals. This study is the first to perform molecular characterization of rGCs in cnidarians and provides evidence for the possible involvement of rGCs in the reproduction of basal metazoans.

Highlights

IntroductionThe receptor guanylate cyclases (rGCs), referred to as membrane rGCs1, serve as sensitive chemoreceptors for detecting the presence of semiochemicals (e.g., peptides) and the changes in environmental cues (e.g., temperature, pH and carbon dioxide)[1,2,3]
The receptor guanylate cyclases, referred to as membrane rGCs1, serve as sensitive chemoreceptors for detecting the presence of semiochemicals and the changes in environmental cues[1,2,3]
By combining a transcriptome database search and expression analyses, we successfully demonstrated the presence of rGCs in the reproductive tissues/cells of an anthozoan cnidarian E. ancora

Summary

Introduction

The receptor guanylate cyclases (rGCs), referred to as membrane rGCs1, serve as sensitive chemoreceptors for detecting the presence of semiochemicals (e.g., peptides) and the changes in environmental cues (e.g., temperature, pH and carbon dioxide)[1,2,3]. In addition to sperm guidance, specific types of mammalian rGCs (e.g., GC-A or GC-B) and their ligands (e.g., atrial natriuretic peptide or C-type natriuretic peptide) regulate several reproductive functions, including testicular steroidogenesis[18], blood-testis barrier dynamics[19], and oocyte meiosis[20,21,22,23,24] These studies illustrate the significance of rGCs in the reproductive processes of both sexes. Basal metazoans include the nonbilaterian animal phyla Porifera (sponges), Cnidaria (corals, sea anemones, jellies, and hydras), Ctenophora (comb jelly), and Placozoa (Trichoplax) Because of their simplicity of body plan and phylogenetic position, these metazoans are regarded as evolutionarily primitive animals[29]. The available genomic and transcriptomic databases of basal metazoans have been increasing[31,32,33,34,35,36,37,38], no published studies are available for describing the characterization of rGCs in any basal metazoans

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