Investigation of Gene Sequence Divergence, Expression Dynamics, and Endocrine Regulation of the Vitellogenin Gene Family in the Whiteleg Shrimp Litopenaeus vannamei

Abstract

In this report, we studied the vitellogenin gene family in the whiteleg shrimp Litopenaeus vannamei by transcriptomics, bioinformatics, and molecular biology methods. At least three moderately homologous vitellogenin (Vg) genes (i.e. LvVg1, LvVg2, and LvVg3) were identified in the genome. The deduced LvVg proteins consisted of a vitellogenin_N domain, a DUF1943 domain, and a VWD domain typical of most vitellogenins from oviparous animals. LvVg1 was the most abundant Vg expressed in the hepatopancreas and ovary of maturing females. Furthermore, multiple isoforms of LvVg1 were evolved presumably due to the need for rapid Vg production during the rapid phase of vitellogenesis. LvVg transcripts were detected in different larval stages, juveniles, and subadults. During the non-reproductive cycle, LvVg expression in the hepatopancreas peaked at the intermolt stages. During the female vitellogenesis cycle, a two-phase expression pattern of LvVg1 gene was observed in the hepatopancreas and ovary. Moreover, the eyestalk optic nerve, brain, and thoracic ganglion consisted of factors that differentially regulated the expression of the three Vg genes. In addition to their reproduction-related roles, Vg may also be involved in growth and molt-related processes. Phylogenetic analysis revealed the early expansion and separation of these Vg genes, and it is most likely correlated with the expansion of Vg’s function. In conclusion, the evolution of multiple LvVg1 isoforms and the acquisition of different Vg genes (i.e. LvVg2 and LvVg3) may occur universally in most decapods. Full information on the total number of Vg genes and precise knowledge on the expression pattern and endocrine regulation of each Vg during all life cycle stages are crucial for us to understand the roles of this emerging gene family in the control of shrimp reproduction and other non-reproductive processes.

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

“…v a n n a m e i g e n o m e a n d XR_003475567.1 and XM_027379601.1, respectively, as previously reported (Dai et al, 2021). Different Vg genes and multiple Vg isoforms with different expression patterns have been found in L. vannamei (Wang et al, 2020). However, their contribution to vitellin accumulation in oocytes is unclear.…”

“…Interestingly, the results of the current study showed that the signal peptide was only found in the a.a. sequences of Ov-Vg but not Hp-Vg (Figure 6B). It is speculated that Hp-Vg is transported from the hepatopanscreas to the ovary via the vitellogenin apolipoprotein, which does not require a signal peptide (Wang et al, 2020). In contrast, Ov-Vg is secreted and absorbed by ovaries independently via a paracrine pathway.…”

Suppression of a Novel Vitellogenesis-Inhibiting Hormone Significantly Increases Ovarian Vitellogenesis in the Black Tiger Shrimp, Penaeus monodon

“…Moreover, a certain amount of Vg protein could also be detected in hemolymph of subadult shrimp, however, the levels were lower than in adults ( 27 , 61 ). Hepatopancreas and ovary have been known as the site of vitellogenesis ( 62 – 64 ), and multiple Vg genes have been reported in some species, including Pandalopsis japonica ( 65 ), Metapenaeus ensis ( 66 ) and L. vannamei ( 67 ). In M. ensis , expression level of MeVg1 was relatively high in HP but low in ovary ( 66 ).…”

Examination of the Effects of Thoracic Ganglion and Brain Extracts on Vitellogenin Gene Expression in the Ovary of Whiteleg Shrimp, Litopenaeus vannamei, and Possible Vitellogenesis-Stimulating Activity

“…Transcriptional expression of L. vannamei Vg mRNA in the incubated ovarian explants was determined using QuantiFast Probe RT-PCR + ROX Vial Kit (Qiagen, Hilden, Germany) according to the manufacturer's instructions. For the design of primers and probes, we utilized a cDNA sequence by encoding the Vg gene that was frst reported by Raviv et al [15] (GenBank ID: AY321153), which also corresponds to LvVg1b and LvVg1e of the LvVg1 gene group, as reported by [16]. Total RNAs extracted from the incubated ovarian explants with RNeasy Mini Kit (250) (Qiagen, Hilden, Germany) were used as templates.…”