Reproduction: Shedding light on spawning in jellyfish

An opsin receptor has a central role in the production and release of eggs by female jellyfish.
  1. Laurinda A Jaffe  Is a corresponding author
  1. University of Connecticut Health Center, United States

For a marine creature about to spawn in the vastness of the ocean, timing is everything. Release gametes before or after everybody else, and chances are the precious cells will drift away without ever encountering their male or female counterparts. In jellyfish, an increase in the amount of sunlight at dawn causes males and females to release sperm and eggs into the water at the same time, therefore improving the chances of fertilization. In female jellyfish, the rise in the amount of sunlight falling on the cells surrounding the oocyte – the future egg – also stimulates the final steps in the process of egg production (Figure 1A; Ikegami et al., 1978; Freeman, 1987). However, the molecular basis of the detection of the light signal has long been a mystery.

The effect of light on oocytes in the jellyfish Clytia hemisphaerica.

(A) An ovary before (left) and 90 minutes after (right) light stimulation. Before light stimulation the ovary contains resting oocytes (as indicated by the presence of a large oocyte nucleus; arrow), which need to transform into mature eggs for fertilization. Light triggers the breakdown of the nuclear envelope and later the release of mature eggs from the ovary. (B) This image of the outer layer of an ovary has a lace-like appearance due to staining of the cell contours in white, with large round oocytes visible behind in grey. In this layer are scattered star-shaped cells that contain both the opsin light receptors and the peptides (labeled in green) that are released from these cells to stimulate the oocytes. In the close-up image on the right, the star-shaped cells are highlighted by staining their characteristic cytoskeleton in pink; the nuclei of the surrounding cells are visible in blue. The left image is about 760 microns across; the right image is about 100 microns across.

IMAGE CREDIT: Evelyn Houliston

Now, in eLife, Evelyn Houliston, Tsuyoshi Momose and colleagues at the Laboratoire de Biologie du Développement de Villefranche-sur-mer – including Gonzalo Quiroga-Artigas as first author and researchers at labs in Japan and Germany – report that they have identified the receptor that performs this role in a species of jellyfish called Clytia hemisphaerica (Quiroga Artigas et al., 2018). This protein belongs to the opsin family of receptors, which are responsible for the detection of light throughout the animal world, including in the visual system of vertebrates. Opsins are also involved in the circadian system of many animals (Cermakian and Sassone-Corsi, 2002). Moreover, both the opsin family and the receptors that transmit the signal for oocyte maturation and ovulation in vertebrates are subgroups of a larger family of receptors called G-protein-coupled receptors.

Opsin genes had previously been identified in other jellyfish species, and their expression detected in the gonads of some of these, so there was a good chance that they were involved controlling reproduction. It was also known that the receptor that triggered spawning in response to light was not located in the oocyte itself, but in a layer of cells adjacent to it (Freeman, 1987). While examining gene expression in this location, Quiroga-Artigas et al. found that one opsin (Opsin9) appeared to be very highly expressed in star-shaped cells in the outer layer of the ovary (Figure 1B). Next, they edited Clytia’s genome with CRISPR/Cas 9 technology to generate jellyfish lacking Opsin9. These animals failed to release eggs in response to light, thus identifying Opsin9 as the light receptor.

In separate work, Houliston, Ryusaku Deguchi (Miyagi University of Education) and co-workers also discovered that cells expressing Opsin9 produce very short peptides which, when released, act on the oocyte to stimulate maturation and ovulation (Takeda et al., 2017). In jellyfish that lack Opsin9, these peptides are not released, which explains why these animals fail to spawn (Quiroga Artigas et al., 2018). However, the details of the mechanism responsible for the secretion of the peptides, and the details of how these peptides then act on the oocytes, remain to be determined.

Across the animal kingdom, the regulatory pathways that control oocyte maturation all seem to be variations on the jellyfish theme, with G-protein-coupled receptors having central roles. In vertebrates, for example, a G-protein-coupled receptor in the pituitary gland controls the release of luteinizing hormone (Stamatiades and Kaiser, 2017), which then travels through the bloodstream to the ovaries, where it acts on another G-protein-coupled receptor to stimulate the final stage of egg production and ovulation (Jaffe and Egbert, 2017). In birds, light-activated opsins play an active role in coordinating seasonal reproduction, but these receptors are present in the brain, not the ovaries (Halford et al., 2009). Learning more about the ways in which light controls spawning in jellyfish is therefore an important step towards the understanding of the origin and evolution of the processes controlling reproduction.

References

Article and author information

Author details

  1. Laurinda A Jaffe

    Laurinda A Jaffe is in the Department of Cell Biology, University of Connecticut Health Center, Farmington, United States

    For correspondence
    ljaffe@uchc.edu
    Competing interests
    No competing interests declared
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2636-5721

Publication history

  1. Version of Record published: January 22, 2018 (version 1)

Copyright

© 2018, Jaffe

This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 1,241
    Page views
  • 108
    Downloads
  • 0
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Laurinda A Jaffe
(2018)
Reproduction: Shedding light on spawning in jellyfish
eLife 7:e34258.
https://doi.org/10.7554/eLife.34258
  1. Further reading

Further reading

    1. Developmental Biology
    Sol Sotillos, Isabel von der Decken ... James Castelli-Gair Hombría
    Research Article Updated

    The identification of genes affecting gonad development is essential to understand the mechanisms causing Variations/Differences in Sex Development (DSD). Recently, a DLC3 mutation was associated with male gonadal dysgenesis in 46,XY DSD patients. We have studied the requirement of Cv-c, the Drosophila ortholog of DLC3, in Drosophila gonad development, as well as the functional capacity of DLC3 human variants to rescue cv-c gonad defects. We show that Cv-c is required to maintain testis integrity during fly development. We find that Cv-c and human DLC3 can perform the same function in fly embryos, as flies carrying wild type but not patient DLC3 variations can rescue gonadal dysgenesis, suggesting functional conservation. We also demonstrate that the StART domain mediates Cv-c's function in the male gonad independently from the GAP domain's activity. This work demonstrates a role for DLC3/Cv-c in male gonadogenesis and highlights a novel StART domain mediated function required to organize the gonadal mesoderm and maintain its interaction with the germ cells during testis development.

    1. Cell Biology
    2. Developmental Biology
    Peng Ding, Chuan Gao ... Junjie Gao
    Research Article Updated

    The skeletal system contains a series of sophisticated cellular lineages arising from the mesenchymal stem cells (MSCs) and hematopoietic stem cells (HSCs) that determine the homeostasis of bone and bone marrow. Here, we reasoned that osteocyte may exert a function in regulation of these lineage cell specifications and tissue homeostasis. Using a mouse model of conditional deletion of osteocytes by the expression of diphtheria toxin subunit α in dentin matrix protein 1 (DMP1)-positive osteocytes, we demonstrated that partial ablation of DMP1-positive osteocytes caused severe sarcopenia, osteoporosis, and degenerative kyphosis, leading to shorter lifespan in these animals. Osteocytes reduction altered mesenchymal lineage commitment, resulting in impairment of osteogenesis and induction of osteoclastogensis. Single-cell RNA sequencing further revealed that hematopoietic lineage was mobilized toward myeloid lineage differentiation with expanded myeloid progenitors, neutrophils, and monocytes, while the lymphopoiesis was impaired with reduced B cells in the osteocyte ablation mice. The acquisition of a senescence-associated secretory phenotype (SASP) in both osteogenic and myeloid lineage cells was the underlying cause. Together, we showed that osteocytes play critical roles in regulation of lineage cell specifications in bone and bone marrow through mediation of senescence.