Abstract

Genetic information of reproduction and growth is essential for sustainable molluscan fisheries and aquaculture management. However, there is limited knowledge regarding the reproductive activity of the commercially important Pacific abalone Haliotis discus hannai. We performed de novo transcriptome sequencing of the ganglia in sexually immature and mature female Pacific abalone to better understand the sexual maturation process and the underlying molecular mechanisms. Of the ~305 million high-quality clean reads, 76,684 transcripts were de novo-assembled with an average length of 741 bp, 28.54% of which were annotated and classified according to Gene Ontology terms. There were 256 differentially expressed genes between the immature and mature abalone. Tandem mass spectrometry analysis, as compared to the predicted-peptide database of abalone ganglia transcriptome unigenes, identified 42 neuropeptide precursors, including 29 validated by peptidomic analyses. Label-free quantification revealed differential occurrences of 18 neuropeptide families between immature and mature abalone, including achatin, FMRFamide, crustacean cardioactive peptide, and pedal peptide A and B that were significantly more frequent at the mature stage. These results represent the first significant contribution to both maturation-related transcriptomic and peptidomic resources of the Pacific abalone ganglia and provide insight into the roles of various neuropeptides in reproductive regulation in marine gastropods.

Highlights

  • The reproductive success of animals depends on diverse physiological and behavioral processes that take place in a timely and orderly manner

  • In contrast to the hypothalamic regulation of the brain, the neural ganglia of ecdysozoan invertebrates produces several neuropeptides, which include insulin-like peptides, neuroparsins, neuropeptide F (NPF)/short NPF, allatoregulatory peptides, corticotropin-releasing factor-like diuretic hormone, gonad-stimulating factor, crustacean hyperglycemic hormone, vitellogenesis inhibiting hormone, and gonad inhibitory hormone, which have been reported to act as reproductive regulators [4,5]

  • With the goal of identifying and quantifying endogenous ganglionic signaling molecules in the abalone related to sexual maturation, we adopted a two-step approach: the construction of a transcriptome dataset to identify Differentially expressed genes (DEGs) and pathways playing important roles in sexual maturation, followed by a detailed investigation of the expression of specific neuropeptide families using peptidomic analysis

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Summary

Introduction

The reproductive success of animals depends on diverse physiological and behavioral processes that take place in a timely and orderly manner. In addition to the importance of successful coordination among these processes, each step requires continuous adjustment according to the external factors of abiotic and biotic natures. In both vertebrates and invertebrates, neuroendocrine factors, such as neurotransmitters and neurohormones, are responsible for communicating cell signals, and they play crucial roles in the regulation, formation, maturation, and release of gametes [1,2]. In contrast to the hypothalamic regulation of the brain, the neural ganglia of ecdysozoan invertebrates produces several neuropeptides, which include insulin-like peptides, neuroparsins, neuropeptide F (NPF)/short NPF, allatoregulatory peptides, corticotropin-releasing factor-like diuretic hormone, gonad-stimulating factor, crustacean hyperglycemic hormone, vitellogenesis inhibiting hormone, and gonad inhibitory hormone, which have been reported to act as reproductive regulators [4,5]

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