Abstract

The major inorganic and organic osmolytes responsible for hydrating the oocytes during pre-ovulatory meiotic maturation in autumn- and spring-spawning stocks of Atlantic herring are examined. Despite the ovulated eggs of spring-spawning herring being 1.6- to 2-fold larger than the autumn-spawning stock, the GSI (27 ± 3%) and degree of oocyte hydration (70–72% water) were similar. Normalising the data with respect to dry mass revealed that the physiological mechanisms underlying the maturational influx of water were the same for both classes of egg. Cl−, K+ and Pi together with a small pool of free amino acids (FAA) represented the driving forces for oocyte hydration. K+ (autumn and spring) and Pi (spring) maintained their concentrations in the ovulated eggs, while all other ions, including Cl−, Na+, NH4 + and Mg2+ were significantly diluted. In contrast the FAA concentration increased during the hydration process. Amongst the inorganic ions, Cl− showed the greatest increase in the ovulated eggs. The FAA content doubled from 1.5 to 3.3% of dry mass during oocyte hydration and accounted for 29% of the calculated ovoplasmic osmolality in the ovulated eggs from both autumn- and spring-spawners. This significant osmotic effect of the small pool of FAA was due to the low water content of the benthic eggs. The differential movement of the inorganic and organic osmolytes that underly oocyte hydration in Atlantic herring are discussed in relation to current models of transmembrane ion flux.

Highlights

  • In teleosts, the differential expression of multiple forms of vitellogenin and subsequent processing of the Vtg proteins following clathrin-mediated endocytosis has been shown to result in a complex suite of deposited yolk proteins (Yp) in the growing oocyte (Babin et al, 2007; Finn 2007a)

  • We found that unlike other teleosts, Atlantic herring expresses only a single form of vtg, with a deduced aa sequence conforming to the linear NH2-(LvH-Pv-LvL-ß-CT)COO- pentapartite structure of teleost complete Vtgs

  • A single vtg form in this group of teleosts is consistent with preliminary reports of only a single vtg transcript or a single eluted peak of Vtg in Pacific herring (Clupea pallasii) (Koya et al 2003; Matsubara et al 2003)

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Summary

Introduction

The differential expression of multiple forms of vitellogenin (vtg) and subsequent processing of the Vtg proteins following clathrin-mediated endocytosis has been shown to result in a complex suite of deposited yolk proteins (Yp) in the growing oocyte (Babin et al, 2007; Finn 2007a). Up to three forms (vtgAo1, vtgAo2 and vtgC) are recognized in Ostariophysi (Wang et al 2000, 2005, Mikawa et al 2006, Miracle et al 2006, Kang et al 2007) and two forms (three genes: vtgAe1-3) are known for the Elopomorpha (Okumura et al 2002, Wang et al 2006, Finn and Kristoffersen, 2007). As in all oviparous species of marine teleosts, the oocyte of Atlantic herring undergoes a pre-adaptive hydration prior to spawning in the hyperosmotic oceanic environment (Kristoffersen & Finn, 2008). In this latter study we have shown that inorganic ions are the major osmolytes that drive the maturational influx of water in this species. Since it is known that acanthomorph species rely on depolymerization of mainly the lipovitellin heavy chain of the VtgAa form to generate the osmotic driving force for oocyte hydration, we wanted to investigate whether a similar process occurs in more ancestral marine teleosts as exemplified by Atlantic herring

Materials and Methods
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