Abstract

Low egg quality and embryonic survival are critical challenges in aquaculture, where assisted reproduction procedures and other factors may impact egg quality. This includes European eel (Anguilla anguilla), where pituitary extract from carp (CPE) or salmon (SPE) is applied to override a dopaminergic inhibition of the neuroendocrine system, preventing gonadotropin secretion and gonadal development. The present study used either CPE or SPE to induce vitellogenesis in female European eel and compared impacts on egg quality and offspring developmental competence with emphasis on the maternal-to-zygotic transition (MZT). Females treated with SPE produced significantly higher proportions of floating eggs with fewer cleavage abnormalities and higher embryonic survival. These findings related successful embryogenesis to higher abundance of mRNA transcripts of genes involved in cell adhesion, activation of MZT, and immune response (dcbld1, epcam, oct4, igm) throughout embryonic development. The abundance of mRNA transcripts of cldnd, foxr1, cea, ccna1, ccnb1, ccnb2, zar1, oct4, and npm2 was relatively stable during the first eight hours, followed by a drop during MZT and low levels thereafter, indicating transfer and subsequent clearance of maternal mRNA. mRNA abundance of zar1, epcam, and dicer1 was associated with cleavage abnormalities, while mRNA abundance of zar1, sox2, foxr1, cldnd, phb2, neurod4, and neurog1 (before MZT) was associated with subsequent embryonic survival. In a second pattern, low initial mRNA abundance with an increase during MZT and higher levels persisting thereafter indicating the activation of zygotic transcription. mRNA abundance of ccna1, npm2, oct4, neurod4, and neurog1 during later embryonic development was associated with hatch success. A deviating pattern was observed for dcbld1, which mRNA levels followed the maternal-effect gene pattern but only for embryos from SPE treated females. Together, the differences in offspring production and performance reported in this study show that PE composition impacts egg quality and embryogenesis and in particular, the transition from initial maternal transcripts to zygotic transcription.

Highlights

  • The aquaculture sector has expanded rapidly and further development relies on diversification and on closing the life cycle for aquatic species in captivity [1,2]

  • High variability in egg quality and low survival during embryonic development pose a challenge to captive offspring production in fish aquaculture [3,4,5,6]

  • While the influence of maternal nutrition and egg nutrient composition on offspring quality is well established, studies of embryogenesis continue to uncover vital functions of different cytoplasmic factors such as messenger RNAs that are incorporated into the developing oocyte [5,9]

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Summary

Introduction

The aquaculture sector has expanded rapidly and further development relies on diversification and on closing the life cycle for aquatic species in captivity [1,2]. While the influence of maternal nutrition and egg nutrient composition on offspring quality is well established, studies of embryogenesis continue to uncover vital functions of different cytoplasmic factors such as messenger RNAs (mRNAs) that are incorporated into the developing oocyte [5,9]. These maternal mRNA transcripts deposited into the egg during oocyte development have proven to be essential drivers of zygotic and early embryonic development until the mid-blastula transition [7,9,10]. The maternal mRNA abundance and activation of the maternal-to-zygotic transition (MZT) are vital for the molecular ontogeny and development of the embryo, including the activation of zygotic transcription and the clearance of maternal mRNA [13,14,15,16,17]

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