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Multiple vitellogenin genes (vtgs) in large yellow croaker (Larimichthys crocea): molecular characterization and expression pattern analysis during ovarian development

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Abstract

The large yellow croaker (Larimichthys crocea) is a marine fish that is economically important to Chinese fisheries, and its reproductive and developmental biology have been extensively investigated. However, the molecular mechanism of oogenesis in L. crocea is not clear. Here, we investigated the multiple vitellogenin (Vtg) system in large yellow croaker. Three different vtg cDNA sequences, including vtgAa, vtgAb and vtgC, were cloned, which indicate the existence of multiple Vtg proteins in large yellow croaker (Lc-Vtgs). Subsequently, the vtg cDNA sequences and predicted Vtg protein structures were analysed, and Vtg protein structures were found to be highly conserved. To research the expression of vtgs during the development of the ovaries, we examined ovarian development and oogenesis by histological analysis. Four stages of ovary development – stages II, III, IV and V – were observed and their boundaries were defined. Soon afterwards, the expression of vtgs in the liver (known as the main site of Vtg synthesis in teleosts) and ovary were analysed. The expression of vtgs was detected in the two tissues. Interestingly, in the early stages of development (stages II and III), there is little or no generation of yolk granules and the expression of vtgs in the liver is low. However, in the late stages (stages IV and V), yolk granules are generated rapidly and the expression of vtgs is significantly increased in the liver. These results support the hypothesis that the Vtgs were synthetized by the liver, and absorbed by the growing oocytes to promote oogenesis in large yellow croaker. We also detected the presence of vtg mRNA in the liver cells and oocytes by in situ hybridization, which indicated that vths were expressed both in the liver and ovaries. Importantly, we found that the distribution of vtgAa and vtgAb mRNA was close to the sites of yolk granule formation in oocytes.

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Abbreviations

Lc-Vtg:

Larimichthys crocea Vtg protein

Lc-vtg :

Larimichthys crocea vtg gene

RACE:

Rapid amplification of cDNA ends

ORF:

Open reading frame

RT-PCR:

Semi-quantitative reverse transcription polymerase chain reaction

qPCR:

Quantitative real-time polymerase chain reaction

ISH:

In situ hybridization

PBS:

Phosphate-buffered saline

O.C.T.:

Optimum cutting temperature

DEPC:

Diethylpyrocarbonate

SSC:

Sodium chloride

DIG:

Digoxigenin

PFA:

Paraformaldehyde

HE:

haematoxylin-eosin

vWF:

von Willebrand factor

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Acknowledgements

The authors wish to thank all the members from the Sperm Laboratory at Zhejiang University and the Fish Histology Laboratory at Ningbo University for fruitful discussions. This project was supported by the Scientific and Technical Project of Zhejiang Province (No. 2016C02055-7), the Scientific and Technical Project of Ningbo City (No. 2015C110005, 2016A610081), the National Natural Science Foundation of China (No. 31602140), and the Collaborative Innovation Center for Zhejiang Marine High-efficiency and Healthy Aquaculture, the K.C. Wong Magna Fund in Ningbo University.

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  1. Key Laboratory of Applied Marine Biotechnology by the Ministry of Education, School of Marine Sciences, Ningbo University, Ningbo, Zhejiang, 315211, People’s Republic of China

    Xin-Ming Gao, Yang Zhou, Dan-Dan Zhang, Cong-Cong Hou & Jun-Quan Zhu

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  1. Xin-Ming Gao
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Table S1

Information on L. crocea used in this report. (DOC 19 kb)

Table S2

The accession numbers of teleost Vtgs amino acid sequences in the NJ phylogenetic tree. (DOC 33 kb)

Fig. S1a

Full-length cDNA of vtgAa. Nucleotide residues are numbered from 5′ to 3′ direction. The deduced amino acid sequence is shown above the nucleotide sequence. The 16 amino acids starting from the first amino acid make up the signal peptide (underlined). The yellow shade indicates the binding domain of the Vtg receptor. The grey shades show the serine polymers in the Pv domain. The total of 14 cysteines in the β′ and CT domain are shown in red. The conserved CGLC motif is marked by a black box. (PNG 15553 kb)

High resolution image (TIF 48818 kb)

Fig. S1b

Full-length cDNA of vtgAb. The 15 amino acids starting from the first amino acid make up the signal peptide (underlined). The yellow highlighting indicates the binding domain of the Vtg receptor. The grey shades show the serine polymers in the Pv domain. The total of 14 cysteines in the β′ and CT are shown in red. The conserved CGLC motif is marked by a black box. (PNG 15737 kb)

High resolution image (TIF 50531 kb)

Fig. S1c

Full-length cDNA of vtgC. The 15 amino acids starting from the first amino acid make up the signal peptide (underlined). The yellow highlighting indicates the binding domain of the Vtg receptor. (PNG 12182 kb)

High resolution image (TIF 39122 kb)

Fig. S2a

Multiple sequence alignment of Lc-VtgAa. The red box shows the signal peptide. The black box shows the Vtg receptor binding region. The blue box shows the conserved CGXC motif (X means any amino acid). The four solid black triangles with a black line show the sites of cleavage by cathepsin D. (PNG 34744 kb)

High resolution image (TIF 118444 kb)

Fig. S2b

Multiple sequence alignment of Lc-VtgAb. The red box shows the signal peptide. The black box shows the Vtg receptor binding region. The blue box shows the conserved CGXC motif (X means any amino acid). The four solid black triangles with a black line show the sites of cleavage by cathepsin D. (PNG 36179 kb)

High resolution image (TIF 126920 kb)

Fig. S2c

Multiple sequence alignment of Lc-VtgC. The red box shows the signal peptide. The black box shows the Vtg receptor binding region. The solid black triangles with a black line show the sites of cleavage by cathepsin D. (PNG 36061 kb)

High resolution image (TIF 129693 kb)

Fig. S3

Ovary sections incubated with sense probe. The control groups incubated with sense probe of Lc-vtgAa (A1-A3), vtgAb (B1-B3) and vtgC (C1-C3) mRNA were not detected the positive signals. (PNG 3107 kb)

High resolution image (TIF 42037 kb)

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Gao, XM., Zhou, Y., Zhang, DD. et al. Multiple vitellogenin genes (vtgs) in large yellow croaker (Larimichthys crocea): molecular characterization and expression pattern analysis during ovarian development. Fish Physiol Biochem 45, 829–848 (2019). https://doi.org/10.1007/s10695-018-0569-y

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