Abstract
BackgroundOocyte maturation in fish involves numerous cell signaling cascades that are activated or inhibited during specific stages of oocyte development. The objectives of this study were to characterize molecular pathways and temporal gene expression patterns throughout a complete breeding cycle in wild female largemouth bass to improve understanding of the molecular sequence of events underlying oocyte maturation.MethodsTranscriptomic analysis was performed on eight morphologically diverse stages of the ovary, including primary and secondary stages of oocyte growth, ovulation, and atresia. Ovary histology, plasma vitellogenin, 17β-estradiol, and testosterone were also measured to correlate with gene networks.ResultsGlobal expression patterns revealed dramatic differences across ovarian development, with 552 and 2070 genes being differentially expressed during both ovulation and atresia respectively. Gene set enrichment analysis (GSEA) revealed that early primary stages of oocyte growth involved increases in expression of genes involved in pathways of B-cell and T-cell receptor-mediated signaling cascades and fibronectin regulation. These pathways as well as pathways that included adrenergic receptor signaling, sphingolipid metabolism and natural killer cell activation were down-regulated at ovulation. At atresia, down-regulated pathways included gap junction and actin cytoskeleton regulation, gonadotrope and mast cell activation, and vasopressin receptor signaling and up-regulated pathways included oxidative phosphorylation and reactive oxygen species metabolism. Expression targets for luteinizing hormone signaling were low during vitellogenesis but increased 150% at ovulation. Other networks found to play a significant role in oocyte maturation included those with genes regulated by members of the TGF-beta superfamily (activins, inhibins, bone morphogenic protein 7 and growth differentiation factor 9), neuregulin 1, retinoid X receptor, and nerve growth factor family.ConclusionsThis study offers novel insight into the gene networks underlying vitellogenesis, ovulation and atresia and generates new hypotheses about the cellular pathways regulating oocyte maturation.
Highlights
Female teleost fishes show remarkable diversity in reproductive strategies
Vtg is characterized as the initial uptake of Vtg into oocytes (C), while late Vtg is marked by significant Vtg deposition surrounded by the formation of multiple oil droplets (D)
It is important to identify the signaling cascades that correspond to atresia to better understand how these molecular changes relate to gonad morphology
Summary
Female teleost fishes show remarkable diversity in reproductive strategies. Some reproductive strategies include continuous and semi-synchronous spawning, sex reversal, and synchronous or simultaneous hermaphroditism. Despite the wide diversity in reproductive strategies, there are characteristic morphological and physiological changes that occur as the oocytes grow and mature. One can discern the beginning of formation of oocyte microvilli, extending towards the granulosa layer, followed by extensions of microvilli from the granulosa layer towards the oocyte. During this phase, meiosis is arrested at the diplotene stage of prophase I and the oocyte is characterized by intensive mRNA transcription [1]. Primary oocytes progress into secondary growth phase and are characterized by active uptake of nutritional resources including the egg yolk precursor protein vitellogenin (Vtg) and lipids and active deposition of the zona radiata interna. The objectives of this study were to characterize molecular pathways and temporal gene expression patterns throughout a complete breeding cycle in wild female largemouth bass to improve understanding of the molecular sequence of events underlying oocyte maturation
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