Characterization of eyes, photoreceptors and opsins in developmental stages of the arrow worm Spadella cephaloptera (Chaetognatha)

The phylogenetic position of chaetognaths, or arrow worms, has been debated for decades, however recently they have been grouped into the Gnathifera, a sister clade to all other Spiralia. Chaetognath photoreceptor cells are anatomically unique by exhibiting a highly modified cilium and are arranged differently in the eyes of the various species. Studies investigating eye development and underlying gene regulatory networks are so far missing. To gain insights into the development and the molecular toolkit of chaetognath photoreceptors and eyes a new transcriptome of the epibenthic species Spadella cephaloptera was searched for opsins. Our screen revealed two copies of xenopsin and a single copy of peropsin. Gene expression analyses demonstrated that only xenopsin1 is expressed in photoreceptor cells of the developing lateral eyes. Adults likewise exhibit two xenopsin1+ photoreceptor cells in each of their lateral eyes. Beyond that, a single cryptochrome gene was uncovered and found to be expressed in photoreceptor cells of the lateral developing eye. In addition, cryptochrome is also expressed in the cerebral ganglia in a region in which also peropsin expression was observed. This condition is reminiscent of a non-visual photoreceptive zone in the apical nervous system of the annelid Platynereis dumerilii that performs circadian entrainment and melatonin release. Cryptochrome is also expressed in cells of the corona ciliata, an organ in the posterior dorsal head region, indicating a role in circadian entrainment. Our study highlights the importance of the Gnathifera for unraveling the evolution of photoreceptors and eyes in Spiralia and Bilateria.

毛颚动物（chaetognaths，又名箭虫（arrow worms））的系统发育位置已争论数十年，近期它们被归入颚胃动物（Gnathifera）——一类与所有其他螺旋动物（Spiralia）互为姊妹群的类群。毛颚动物的感光细胞在解剖学上独具特色：其纤毛经高度特化，且在不同物种的眼部中排布方式各异。目前针对其眼部发育及潜在基因调控网络的相关研究仍属空白。为探究毛颚动物感光细胞与眼部的发育过程及分子工具包，本研究对表底栖物种头翼锄虫（Spadella cephaloptera）的全新转录组（transcriptome）进行了视蛋白（opsins）筛选。本次筛选共发现两份异视蛋白（xenopsin）拷贝与一份周视蛋白（peropsin）拷贝。基因表达分析结果显示，仅异视蛋白1（xenopsin1）在发育中的侧眼感光细胞中表达。成体的每一侧眼同样存在2个表达异视蛋白1的感光细胞。除此之外，本研究还发现了一份隐花色素（cryptochrome）基因拷贝，其在发育中的侧眼感光细胞中表达。此外，隐花色素还在脑神经节的特定区域表达，该区域同时存在周视蛋白的表达信号。这一表达模式与环节动物（annelid）杜氏阔沙蚕（Platynereis dumerilii）顶神经系统中的非视觉感光区类似——该区域负责昼夜节律同步与褪黑素释放。隐花色素还在头部后背部区域的纤毛冠（corona ciliata）细胞中表达，提示其可能参与昼夜节律同步过程。本研究突显了颚胃动物在解析螺旋动物与两侧对称动物（Bilateria）感光系统及眼部演化历程中的关键价值。