Insights into the evolutionary origin of the pineal color discrimination mechanism from the river lamprey

Research article

Wada, Seiji / Kawano-Yamashita, Emi / Sugihara, Tomohiro / Tamotsu, Satoshi / Koyanagi, Mitsumasa / Terakita, Akihisa

和田, 清二 / 山下(川野), 絵美 / 杉原, 智博 / 保, 智己 / 小柳, 光正 / 寺北, 明久

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研究グループは、奈良女子大学の研究グループと共同で、哺乳類以外の脊椎動物において「第3の目」とも呼ばれる松果体の光感覚のメカニズムについて、脊椎動物の中で「原始的」とも呼べる特徴を多く残し、進化研究で重要視されてきた円口類ヤツメウナギを用いて解析しました。その結果、異なる2種類の光受容タンパク質をそれぞれ含む2種類の光受容細胞を用いて色を感じるという、松果体色感覚の新規のメカニズム(2細胞システム)を発見しました。本研究グループは、魚類と爬虫類の松果体では、ヤツメウナギの場合とは異なり、上述の2種類の光受容タンパク質が一つの細胞にセットになって存在する1細胞システムにより色検出していることを既に明らかにしています。今回の研究成果から、強い光の下では、1細胞システムの方が2細胞システムよりも明瞭な色検出が可能であることが明らかになり、現存する魚類や爬虫類がもつ1細胞システムは、もともと目と同じように2つの光受容タンパク質が別々の2細胞に別れていた2細胞システムが1つの細胞中に融合したかのような進化を遂げた結果である可能性を示しています。すなわち、より多くの細胞を巻き込んで進化したとされる目の色検出のメカニズムの進化とは異なり、2細胞から1細胞の方向に進化したことを初めて提唱するものです。これは、松果体色検出についてこれまでの常識を覆すとともに、進化のみならず未解明の機能を探る上で重要な発見といえます。

Background: Pineal-related organs in cyclostomes, teleosts, amphibians, and reptiles exhibit color opponency, generating antagonistic neural responses to different wavelengths of light and thereby sensory information about its "color". Our previous studies suggested that in zebrafish and iguana pineal-related organs, a single photoreceptor cell expressing both UV-sensitive parapinopsin and green-sensitive parietopsin generates color opponency in a "one-cell system." However, it remains unknown to what degree these opsins and the single cell-based mechanism in the pineal color opponency are conserved throughout non-mammalian vertebrates. / Results: We found that in the lamprey pineal organ, the two opsins are conserved but that, in contrast to the situation in other vertebrate pineal-related organs, they are expressed in separate photoreceptor cells. Intracellular electrophysiological recordings demonstrated that the parietopsin-expressing photoreceptor cells with Go-type G protein evoke a depolarizing response to visible light. Additionally, spectroscopic analyses revealed that parietopsin with 11-cis 3-dehydroretinal has an absorption maximum at ~570 nm, which is in approximate agreement with the wavelength (~560 nm) that produces the maximum rate of neural firing in pineal ganglion cells exposed to visible light. The vesicular glutamate transporter is localized at both the parietopsin- and parapinopsin-expressing photoreceptor terminals, suggesting that both types of photoreceptor cells use glutamate as a transmitter. Retrograde tracing of the pineal ganglion cells revealed that the terminal of the parietopsin-expressing cells is located close enough to form a neural connection with the ganglion cells, which is similar to our previous observation for the parapinopsin-expressing photoreceptor cells and the ganglion cells. In sum, our observations point to a "two-cell system" in which parietopsin and parapinopsin, expressed separately in two different types of photoreceptor cells, contribute to the generation of color opponency in the pineal ganglion cells. / Conclusion: Our results indicate that the jawless vertebrate, lamprey, employs a system for color opponency that differes from that described previously in jawed vertebrates. From a physiological viewpoint, we propose an evolutionary insight, the emergence of pineal "one-cell system" from the ancestral "multiple (two)-cell system," showing the opposite evolutionary direction to that of the ocular color opponency.

This work was supported by the Japanese Ministry of Education, Culture, Sports, Science and Technology Grants-in-Aid for Scientific Research 15H05777 and 20K21434 (to A.T.), 16KT0074 and 17H06015 (to M.K.), 14J40094 (to E.K.-Y.), and 13J05782 and 18K14751 (to S.W.).

eng

188

光受容 / 松果体 / 色検出 / ヤツメウナギ

Opsin / Pineal organ / Color opponency / Lamprey

publisher

Osaka City University / Osaka City University, Nara Women's University / Osaka City University / Nara Women's University / Osaka City University / Osaka City University

2021-09-16

BioMed Central

1741-7007

AA1203472X

Journal Article

https://doi.org/10.1186/s12915-021-01121-1

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