Neuroendocrine transcriptomics in Eriocheir sinensis: Photoperiod-induced modulation of gonadal development and circadian clock genes in neural tissues

Abstract

Photoperiod is a critical environmental cue that orchestrates reproductive physiology and circadian biology in crustaceans, yet the neural gene networks linking photoperiod to ovarian maturation and clock regulation remain largely unknown. To elucidate the molecular mechanisms underlying photoperiod regulation of ovarian development and associated circadian rhythmicity, the eyestalk (SG) and brain ganglion (BG) of female Chinese mitten crab (Eriocheir sinensis) from two photoperiod groups (Light (L): Dark (D) = 0 h: 24 h (L0) and L: D = 18 h: 6 h (L18)) were used for transcriptome analysis. The analysis identified 298 differentially expressed genes (DEGs) in the brain and 109 DEGs in the eyestalk. KEGG enrichment analysis indicated these DEGs were primarily associated with ovarian development and circadian rhythm-related signaling pathways. Key ovarian development-related genes, including E3 ubiquitin-protein ligase lubel-like isoform X6, 5-hydroxytryptamine receptor-like, serine/threonine-protein phosphatase alpha-2, estrogen sulfotransferase, cytochrome P450 2 L1-like, follicle-stimulating hormone receptor-like isoform X1 and E3 ubiquitin-protein ligase CHIP (EULCHIP), exhibited significant upregulation or downregulation in the L18-BG group. Meanwhile, genes such as EULCHIP, E3 ubiquitin-protein ligase TRIM71-like, CREB-binding protein-like isoform X2, serine/threonine-protein phosphatase 6 regulatory ankyrin repeat subunit C, collagen alpha-5(IV) chain, integrin beta 1, ecdysone-induced protein 74EF-like, and insulin-like growth factor-binding protein complex acid labile subunit showed significant upregulation or downregulation in the L18-SG group. These findings suggest that prolonged photoperiods enhance ovarian development and modulate reproductive endocrine activity during ovarian maturation. Furthermore, circadian rhythm-related genes such as period circadian protein-like isoform X1, prostaglandin D synthase, and acetylcholine receptor subunit alpha-type acr-16 displayed marked differential expression between photoperiod groups, indicating disrupted molecular oscillations and gradual desynchronization of circadian rhythmicity under extended light exposure. This study provides critical, systems-level insights into the photoperiod-driven regulatory networks of ovarian development and endocrine dynamics in crustaceans, offering a molecular basis for optimizing aquaculture practices and advancing our understanding of crustacean reproductive physiology.