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Germ cells are the only carriers that can transmit genetic information in multicellular animals, and are the basis for
species continuation and breed expansion.
For sexually reproducing animals, the birth of life begins with the union
of sperm and egg.
Both sperm and eggs are derived from primordial germ cells (PGCs) in the embryonic stage and germline stem cells (GSCs) in larval or adult gonads, that is, reproductive stem progenitor cells ( germline stem and progenitor cells，GSPCs）
。 The self-renewal and differentiation of GSPCs is the key to gamete generation and gonadal differentiation, and innovative research on this mechanism is not only an important proposition in developmental biology and reproductive biology, but also a major demand
for seed industry innovation.
Mitochondria are known as the cell's "powerhouse" and produce adenosine triphosphate (ATP) through aerobic respiration and oxidative phosphorylation, which provides energy
for cellular activity.
Mitochondria are highly dynamic organelles that constantly undergo fusion and fission to form a dynamic equilibrium, which is essential
for mitochondrial homeostasis and its function.
Studies have shown that mitochondrial homeostasis is involved in regulating the maintenance and differentiation
of stem cell fate.
However, it is unclear whether there is a specific mitochondrial dynamic regulatory mechanism for GSPCs, and how mitochondrial dynamics play a role in determining the fate of GSPCs.
Sun Yonghua's team at the Institute of Hydrobiology, Chinese Academy of Sciences has long been engaged in research on the development of fish germ cells, and has revealed multiple new factors regulating gonadal development and gamete genesis in fish and their mechanisms of action (He et al.
2020; Zhang et al.
2020b; Wang et al.
2022; Xie et al.
2022), and established allo- or xenograft transplantation abdominal reproductive technology (Zhang et al.
2020a; Zhang et al.
2022)
。 Recently, Sun Yonghua's team and Chen Zhenxia's team from Huazhong Agricultural University used zebrafish as a model, and discovered a mitochondrial fusion regulator Pld6 specifically expressed in germ cells through bioinformatics mining and experimental biological verification.
The loss of HLD6 leads to the dynamic imbalance of mitochondria in germ cells, and serious defects in mitochondrial morphology and function, which further hinders the maintenance and differentiation of GSPCs, and eventually forms an empty nest seminal nest
lacking germ cells.
This study revealed the important role of germ cell-specific mitochondrial fusion events in the determination of germ cell fate, and provided new insights
into the regulatory mechanism of fish germ cell development.
The researchers first performed transcriptome analysis on the sperm ovaries in the gonadal differentiation stage, and found that the transcription levels of mitochondrial assembly and oxidative phosphorylation-related genes in the ovaries were significantly higher than those in the seminal nest, suggesting that GSPCs require stronger mitochondrial energy
supply to egg differentiation.
Further single-cell transcriptome analysis of sperm ovaries revealed that PLD6, a key factor regulating mitochondrial fusion, is not only highly expressed in ovarian tissue, but also specifically expressed in germ cells including GSPCs (Figure 1).
Fig.
1 It was found that the mitochondrial fusion regulator PLD6 was specifically expressed in the germ cell lineage
Subsequently, the researchers established a model of zebrafish mutants with PLD6 deletion, and the results showed that all homozygous mutants developed into infertile males, and histological and cell biology studies showed that germ cells in the gonads of homozygous mutants were completely lost
.
Timing tracking and study of the development of mutant gonads showed that GSPCs with pld6 deletion could neither proliferate by mitosis nor differentiate by meiosis, thus moving towards the apoptosis pathway
in the early stage of gonadal development.
Further research revealed that mitochondrial dynamic imbalance in mutant GSPCs, mitochondrial copy number and ATP synthesis were significantly reduced, and the unique mitochondria-nuage in germ cells was in mutant GSPCs , which in turn hinders the synthesis of piRNA (Figure 2).
Therefore, this study has identified a new mitochondrial fusion regulator specific to germ cells and revealed its molecular and cytological mechanisms
that regulate the fate maintenance and differentiation of fish GSPCs.
Fig.
2 The mechanism of action of PLD6 dynamically regulates the maintenance and differentiation of reproductive stem progenitor cells by regulating mitochondria
The study, titled "A germ cell-specific mitochondrial fusion factor regulates the maintenance and differentiation of reproductive stem progenitor cells", was published online in the international academic journal Advanced Science
.
Dr.
Zhang Ru from the Fish Development and Biotechnology Section of the Institute of Aquatic Sciences and Yixuan Tu, a doctoral student at Huazhong Agricultural University, were the joint first authors of the paper, researcher Sun Yonghua from the Institute of Aquatic Sciences was the corresponding author of the paper, and Professor Chen Zhenxia of Huazhong Agricultural University was the co-corresponding author
.
Ye Ding, associate researcher of the Institute of Aquatic Sciences, and Professor Gu Zhenglong, Institute of Precision Medicine, Guangdong-Hong Kong-Macao Greater Bay Area, Fudan University, participated in the research
.
The research was supported
by the National Science Foundation for Outstanding Young Scholars, the National Natural Science Foundation of China Innovative Research Group, the National Key Research and Development Program of China, and the Strategic Leading Science and Technology Special Project of the Chinese Academy of Sciences.
The PLD6 mutant constructed in this paper has been preserved in the National Zebrafish Resource Center
of the National Aquatic Germplasm Resource Bank.
Full text link: https://doi.
org/10.
1002/advs.
202203631
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2020.
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