Transcriptomic analysis reveals yolk accumulation mechanism from the hepatopancreas to ovary in the pacific white shrimp Litopenaeus vannamei

Abstract

The Pacific white shrimp Litopenaeus vannamei is an economically important penaeid species worldwide. Under farming conditions, the full ovarian maturation of L. vannamei generally depends on the combination of artificial ablation of unilateral eyestalk and feeding high-quality natural diets, suggesting that nutrient accumulation is important to ovarian maturation. In this study, we aimed to investigate the gene expression related to nutritional accumulation in L. vannamei during ovarian development by transcriptomic analysis. A total of 52.45 Gb of high-quality transcriptome data were obtained from 8 samples from the hepatopancreas and ovaries from shrimp in gonadal developmental stages I-IV. A total of 23,149 expressed genes were detected, of which 19,852 were known genes and 3,297 were novel genes. Our study found that genes related to amino acid, carbohydrate and lipid metabolism were expressed at higher levels in the hepatopancreas than in the ovary. The genes for most lipoproteins and their receptors were predominantly expressed in the hepatopancreas, while vitellogenin receptor (VgR) was specifically expressed in the ovary. Moreover, two vitellogenin (Vg) genes were identified, in which one was specifically expressed in the hepatopancreas and defined as Hp-Vg, and the other was specifically expressed in the ovary and defined as Ov-Vg. In addition, genes related to carotenoid metabolism were enriched in the hepatopancreas. This study provides solid evidence that the hepatopancreas is the major exogenous vitellogenesis site for ovarian maturation of L. vannamei. Two distinct Vg genes perform exogenous and endogenous vitellogenesis in the hepatopancreas and ovary in L. vannamei, respectively. The results of this study also presented some new insights for understanding the nutritional dynamics from the hepatopancreas to ovary during ovarian maturation in penaeids.

Genome-Wide Identification of Vitellogenin Gene Family and Comparative Analysis of Their Involvement in Ovarian Maturation in Exopalaemon carinicauda

“…Unilateral eyestalk ablation in female shrimp is commonly practiced to induce ovarian maturation [64,65]. Removal of the eyestalk, observed in both Pleocyamata and Dendrobranchiata, has been shown to accelerate ovarian development and elevate the gonadosomatic index [66][67][68]. In the Dendrobranchiata shrimp species P. japonicus, mRNA expression of Vtg1 notably increased in the ovaries while remaining unchanged in the hepatopancreas following eyestalk ablation, whereas Vtg2 expression differed [28].…”

Metabolome and Transcriptome Association Analysis Reveals the Link Between Pigmentation and Nutrition Utilization in the Juveniles of Sea Cucumber Holothuria leucospilota

“…For instance, in birds and sh (Hiramatsu et al, 2015, Tian et al, 2010, yolk is derived from the liver (Hiramatsu et al, 2015), while in insects, it is synthesized by the fat body (Tufail and Takeda, 2008). Molluscs produce yolk directly in the ovary (Ni et al, 2014), whereas crustaceans primarily synthesize it in the hepatopancreas (Li et al, 2022. Interestingly, the MYP gene is expressed in both male and female sea urchins (Shyu et al, 1986).…”

Evaluation of common natural diets used in female orange mud crab, Scylla olivacea (Herbst, 1796) reared in captivity

“…This is probably due to high nutrients transported from the hepatopancreas, thereby initiating the increasing size of the oocyte diameter of the crabs. The dynamic changes of the nutrient levels in both hepatopancreas and ovary has been well explained in a study conducted by Li et al (2022), which used the transcriptomic analysis to analyse the expression of relevant genes. In their study, genes related to nutrient metabolism were expressed at higher levels in the hepatopancreas than in the ovary, proving that hepatopancreas as the major lipid metabolism centre that supplied more lipids to the developing ovaries during ovarian development which explains this occurrence.…”

“…explained in a study conducted by Li et al (2022), which used the transcriptomic analysis to analyse the expression of relevant genes.…”