Mechanisms of Egg Yolk Formation and Implications on Early Life History of White Perch (Morone americana)

Abstract

The three white perch (Morone americana) vitellogenins (VtgAa, VtgAb, VtgC) were quantified accurately and precisely in the liver, plasma, and ovary during pre-, early-, mid-, and post-vitellogenic oocyte growth using protein cleavage-isotope dilution mass spectrometry (PC-IDMS). Western blotting generally mirrored the PC-IDMS results. By PC-IDMS, VtgC was quantifiable in pre-vitellogenic ovary tissues and VtgAb was quantifiable in pre-vitellogenic liver tissues however, neither protein was detected by western blotting in these respective tissues at this time point. Immunohistochemistry indicated that VtgC was present within pre-vitellogenic oocytes and localized to lipid droplets within vitellogenic oocytes. Affinity purification coupled to tandem mass spectrometry using highly purified VtgC as a bait protein revealed a single specific interacting protein (Y-box binding protein 2a-like [Ybx2a-like]) that eluted with suramin buffer and confirmed that VtgC does not bind the ovary vitellogenin receptors (LR8 and Lrp13). Western blotting for LR8 and Lrp13 showed that both receptors were expressed during vitellogenesis with LR8 and Lrp13 expression highest in early- and mid-vitellogenesis, respectively. The VtgAa within the ovary peaked during post-vitellogenesis, while VtgAb peaked during early-vitellogenesis in both white perch and the closely related striped bass (M. saxatilis). The VtgC was steadily accumulated by oocytes beginning during pre-vitellogenesis and continued until post-vitellogenesis and its composition varies widely between striped bass and white perch. In striped bass, the VtgC accounted for 26% of the vitellogenin-derived egg yolk, however in the white perch it comprised only 4%. Striped bass larvae have an extended developmental window and these larvae have yolk stores that may enable them to survive in the absence of food for twice as long as white perch after hatch. Thus, the VtgC may play an integral role in providing nutrients to late stage fish larvae prior to the onset of exogenous feeding and its composition in the egg yolk may relate to different early life histories among this diverse group of animals.

Oogenesis and Egg Quality in Finfish: Yolk Formation and Other Factors Influencing Female Fertility

“…They also provide a programmed provisioning of protein, carbohydrate, and lipid nutrition to developing embryos and yolk sac larvae at different developmental time points. A disparate accumulation by the oocyte of different vitellogenin type has also been reported in several species of fishes including grey mullet (Mugil cephalus) [55], barfin flounder (Verasper moseri) [26,27], striped bass (Morone saxatilis) [28,151], white perch [29,54], mosquitofish (Gambusia affinis) [30], red seabream (Pagrus major) [31], goldsinny wrasse (Ctenolabrus rupestris) [152], haddock (Melanogrammus aeglefinus) [32], Atlantic halibut (Hippoglossus hippoglossus) [33,153], and zebrafish (Danio rerio) [34]. This indicates that the final egg yolk composition may vary considerably between fish species.…”

“…Vitellogenin receptors cluster into clathrin coated vesicles that are endocytosed and vitellogenins are processed into yolk proteins for storage in yolk granules located throughout the ooplasm (Yolk Deposition). The figure summarizes data from: [5][6][7][8][9][10][11][12][13][14][15][16][17][18][19][20][21][22]25,[28][29][30][31]134].…”

The observed oogenesis impairment in greater amberjack Seriola dumerili (Risso, 1810) reared in captivity is not related to an insufficient liver transcription or oocyte uptake of vitellogenin

“…Multiple vitellogenins have been described in a number of fish species including the white perch Morone americana (Gmelin, 1789) (Schilling et al., ), the Atlantic bluefin tuna Thunnus thynnus (Linnaeus, 1758) (Pousis et al., ), the grey mullet Mugil cephalus (Linnaeus, 1758) (Amano et al., ), the zebrafish Danio rerio (Hamilton, 1822) (Wang, Tan, Emelyanov, Korzh & Gong, ) and the red seabream Pagrus major (Temminck & Schlegel, 1843) (Sawaguchi et al., ). During oocyte maturation in marine fish that spawn floating eggs, the yolk protein domains of these three Vtgs undergo varying degrees of proteolysis into lipids and free amino acids (FAAs), causing oocyte hydration (Cerdà, Fabra & Raldúa, ; Schilling, Loziuk, Muddiman, Daniels & Reading, ).…”

Two vitellogenins in the loliginid squidUroteuthis edulis: Identification and specific expression in ovarian follicles

“…At present, whether the two ue‐ VTG s have distinct or redundant functions is unknown but, as in G . affinis (Sawaguchi et al, ) and perhaps in the white perch Morone americana (Schilling, Loziuk, Muddiman, Daniels, & Reading, ), distinct, unequal utilization of multiple VTGs may occur in U . edulis .…”

“…edulis occurs over 14 days (at 25°C) to 37 days (at 15°C) (Natsukari & Tashiro, 1991), which suggests the need for a long-term supply of yolk proteins as nutrients. At present, whether the two ue-VTGs have distinct or redundant functions is unknown but, as in G. affinis (Sawaguchi et al, 2005) and perhaps in the white perch Morone americana (Schilling, Loziuk, Muddiman, Daniels, & Reading, 2015), distinct, unequal utilization of multiple VTGs may occur in U. edulis. Detailed investigation of the amount and proportion of yolk proteins derived from two ue-VTGs in each embryonic stage will resolve this question.…”