Stable transgenesis in the marine annelid Platynereis dumerilii sheds new light on photoreceptor evolution
Open accessAbstract
Research in eye evolution has mostly focused on eyes residing in the head. In contrast, noncephalic light sensors are far less understood and rather regarded as evolutionary innovations. We established stable transgenesis in the annelid Platynereis, a reference species for evolutionary and developmental comparisons. EGFP controlled by cis-regulatory elements of r-opsin, a characteristic marker for rhabdomeric photoreceptors, faithfully recapitulates known r-opsin expression in the adult eyes, and marks a pair of pigment-associated frontolateral eyelets in the brain. Unexpectedly, transgenic animals revealed an additional series of photoreceptors in the ventral nerve cord as well as photoreceptors that are located in each pair of the segmental dorsal appendages (notopodia) and project into the ventral nerve cord. Consistent with a photosensory function of these noncephalic cells, decapitated animals display a clear photoavoidance response. Molecular analysis of the receptors suggests that they differentiate independent of pax6, a gene involved in early eye development of many metazoans, and that the ventral cells may share origins with the Hesse organs in the amphioxus neural tube. Finally, expression analysis of opn4×-2 and opn4m-2, two zebrafish orthologs of Platynereis r-opsin, reveals that these genes share expression in the neuromasts, known mechanoreceptors of the lateral line peripheral nervous system. Together, this establishes that noncephalic photoreceptors are more widespread than assumed, and may even reflect more ancient aspects of sensory systems. Our study marks significant advance for the understanding of photoreceptor cell (PRC) evolution and development and for Platynereis as a functional lophotrochozoan model system.
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The marine bristleworm Platynereis dumerilii is well suited to tackle the endocrine basis of this integration.
“The marine bristleworm Platynereis dumerilii is well suited to tackle the endocrine basis of this integration.”
From Corazonin signaling integrates energy homeostasis and lunar phase to regulate aspects of growth and sexual maturation in <i>Platynereis</i> (2020) · cites this paper as [9]
Platynereis is molecularly accessible, and various genetic toolkits allow functional studies.
“Moreover, this species is molecularly accessible, and various genetic toolkits allow functional studies (9–11).”
From Corazonin signaling integrates energy homeostasis and lunar phase to regulate aspects of growth and sexual maturation in <i>Platynereis</i> (2020) · cites this paper as [9]
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Self-citation
- Authors
- Backfisch, B., Veedin Rajan, V. B., Fischer, R. M., Lohs, C., Arboleda, E., Tessmar-Raible, K., & Raible, F.
- Affiliations
- California Institute of Technology (US)
- Max F. Perutz Laboratories, Department of Microbiology, Immunobiology, and Genetics, University of Vienna, A-1030 Vienna, Austria
- Corresponding author
- Raible, Florian
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2012-12-17
- Volume
- 110
- Issue
- 1
- Pages
- 193-198
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3538230
- OpenAlex
- W2151980532
- Cited by
- 93
- References
- 51
- Citations by year
- 2026: 2 · 2025: 5 · 2024: 5 · 2023: 2 · 2022: 7 · 2021: 8 · 2020: 6 · 2019: 8 · 2018: 5 · 2017: 4 · 2016: 10 · 2015: 6 · 2014: 17 · 2013: 8
- FWCI
- 3.98
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Austrian Science Fund (#AY0041321)
- Universität Wien
- Georg-August-Universität Göttingen
- FP7 Ideas: European Research Council (260304)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Retinal Development and Disorders
- Keywords
- Platynereis dumerilii, photoreceptor evolution, rhabdomeric photoreceptors, notopodia, melanopsin, neuromasts, lateral line, eye evolution
- MeSH terms
- Animals, Base Sequence, Biological Evolution, Immunohistochemistry, Molecular Sequence Data, Polychaeta, Zebrafish, In Situ Hybridization, Sequence Analysis, DNA, DNA Primers, Photoreceptor Cells, Invertebrate, Gene Transfer Techniques, Microscopy, Confocal, Gene Expression Profiling, Animals, Genetically Modified, Green Fluorescent Proteins, Opsins
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