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

Wei Wang,Tingting Zhou,Chenggui Wang,Siuming Chan,Amankwah Beatrice Kyei,Bin Li,Lili Shi

doi:10.3389/fendo.2020.577745

Wei Wang, Tingting Zhou + Show 5 more

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https://doi.org/10.3389/fendo.2020.577745

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Journal: Frontier in Endocrinology	Publication Date: Nov 19, 2020
Citations: 7	License type: CC BY 4.0

Affiliation: Guangdong Ocean University

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.

Highlights

Growth and reproduction are two energy-requiring processes important for the species’ continuation
A total of 15 transcripts encoding for full-length or partial Vg or Vg-like cDNAs were identified from the hepatopancreas and ovary transcriptomes of the whiteleg shrimp L. vannamei
Since the transcriptomes were constructed using cDNAs from more than one shrimp and the presence of seven transcripts of LvVg1 suggested that multiple LvVg1 isoforms may exist in the whiteleg shrimp L. vannamei

Summary

Introduction

Growth and reproduction are two energy-requiring processes important for the species’ continuation. During female maturation of shrimp, the ovary undergoes rapid vitellogenesis from the synthesis of a large quantity of the major egg yolk protein or vitellogenin (Vg). Research on Vg in decapod crustaceans began with the purification of Vg from maturing ovary, followed by amino acid sequence determination of the protein [3, 7, 8]. The RACE and RT-PCR cloning approaches were used to obtain the fulllength sequence of Vg [3, 7]. Previous studies using molecular cloning approaches resulted in the identification of one shrimp vitellogenin gene. In subsequent studies based on genomic PCR cloning, genome walking and genomic library screening, the vitellogenin genes of several decapods have been reported (Figure 1B) [3, 4, 8,9,10]

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