Advantages, Factors, Obstacles, Potential Solutions, and Recent Advances of Fish Germ Cell Transplantation for Aquaculture—A Practical Review
Abstract
:Simple Summary
Abstract
1. Fish Germ Cell Transplantation in Aquaculture
2. Germ Cell Transplantation Methods in Fish
2.1. Blastula Cell Transplantation (BCT)
2.2. Primordial Germ Cell Transplantation (PGT)
2.3. Gonadal Germ Cell Transplantation into the Peritoneal Cavity of Larvae (GPT)
2.4. Gonadal Germ Cell Transplantation into Adult Recipients (GAT)
3. Advantages of Germ Cell Transplantation in Aquaculture
3.1. Shortening Generation Time
3.2. Achieving Gamete Production of Semelparous Fish Recurrently through Multiple Seasons
3.3. Solving Bottlenecks of Broodstock Maintenance
3.4. Preservation and Restoration of Superior Strains Using Cryopreserved Cells
4. Factors Affecting the Success of Germ Cell Transplantation
4.1. The Number of Donor Cells
4.2. Purity of Donor Cells (Enrichment)
4.2.1. Percoll Density Gradient Centrifugation (PDGC)
4.2.2. Differential Plating (DP)
4.2.3. Centrifugal Elutriation (CE)
4.2.4. Fluorescence-Activated Cell Sorting (FACS)
4.2.5. Magnetic-Activated Cell Sorting (MACS)
4.2.6. Applications
4.3. Age of Recipients
4.4. Prevention of Endogenous Germ Cell Development in Recipient Gonads
4.4.1. Interspecific Hybridization
4.4.2. Triploidization
4.4.3. Dnd-Knockdown
4.4.4. Dnd-Knockout
4.4.5. Co-Treatment of High Temperature and Busulfan
4.4.6. Other Aspects
4.4.7. Applications
5. Obstacles and Potential Solutions of Germ Cell Transplantation in Aquaculture
5.1. Practical Acceleration of Selective Breeding Process
5.2. Securing Enough Donor Cells for Transplantation via In Vivo or In Vitro Propagation
5.3. Enhancing Transplantation Efficiency with Vulnerable Recipients during Early Development
5.4. Choice of Compatible Recipient Species for Xenotransplantation
6. Advanced Applications of Germ Cell Transplantation
6.1. Production of Mono-Sex Populations
6.2. Production of Sterile Fish through Transplantation of Germ Cells Carrying Mutated Somatic Genes
7. Future Perspectives
Author Contributions
Funding
Institutional Review Board Statement
Data Availability Statement
Conflicts of Interest
Appendix A
Donor | Recipient | % of Recipients with Gonadal Incorporation of Donor Cells | % of Recipients Producing Donor-Derived Gametes | Survival of Recipients (%) | % of Donor-Derived Offspring | Ref | |||||
---|---|---|---|---|---|---|---|---|---|---|---|
Species | Fish | Cells | Species | Fish | Total | Male | Female | ||||
C. auratus | All-female (XX) | A lower part of BD | Hybrid | ♂ C. carpio × ♀ C. auratus, all-male | N/A | N/A | 100 at SM | N/A | Con: 79.9 TP: 72.3 at 4 d | N/A | [11] |
WT | BMs | C. auratus langsdorfii | 3N | 3.1 at 4 d | N/A | N/A | N/A | Con: 65.8 CP + TP: 35.6 at 4 d | N/A | [9] | |
WT | 50–100 BMs | D. rerio | WT | 7.3 at 24 h | N/A | N/A | N/A | 73.3 at 24 h | N/A | [13] | |
C. auratus langsdorfii | 3N | A lower part of BD | C. auratus | WT | N/A | N/A | N/A | 100 at 3–4 y | Con: 91.4 TP: 98.4 at 3 d | 3.1–89.3 | [10] |
D. albolineatus | WT | 50–100 BMs | D. rerio | WT | 6.6 at 24 h | N/A | N/A | N/A | 96.8 at 24 h | N/A | [13] |
D. rerio | WT or TG:pRSV-LacZ (LacZ/-) | 20–100 BMs | D. rerio | Albino | N/A | 17.9 at 2–3 mo | N/A | N/A | 16.7 at SM | 1.0–40.0 | [6] |
WT | 50–100 BMs | D. rerio | WT | 9.0 at 24 h | N/A | N/A | N/A | 86.7 at 24 h | N/A | [13] | |
TG:pvasa-DsRed2-vasa;pβact-EGFP | A whole BD | D. rerio | Dnd-KD | 94.7 at prim-5 St | N/A | N/A | N/A | Con: 62.9 Dnd-KD: 50.3 TP: 26.1 at adult | N/A | [8] | |
M. anguillicaudatus | WT | 50–100 BMs | D. rerio | WT | 1.5 at 24 h | N/A | N/A | N/A | 75.8 at 24 h | N/A | [13] |
O. mykiss | WT, mid-blastula (2.5 d) | ~80 BMs | O. mykiss | WT, early blastula (1.5 d) | N/A | 31.6 at 2 y | 55.6 at 2 y | 10.0 at 2 y | 8.0 at 2 y | 0.3–14.6 | [7] |
O. latipes | TG:pLFABP-rfp;pvasa-GFP | 30 BMs | O. latipes | WT | 47.2 at St 18–23 | N/A | N/A | N/A | N/A | 4.3 | [64] |
TG:pLFABP-rfp;pvasa-GFP, dnd mRNA injected | WT | 81.2 at St 18–23 | N/A | N/A | N/A | N/A | 31.4 | ||||
TG:pLFABP-rfp;pvasa-GFP, dnd mRNA injected | Dnd-KD | 81.1 at St 18–23 | 91.4 at SM | N/A | N/A | N/A | 96.5 | ||||
TG:pLFABP-rfp;pvasa-GFP, dnd mRNA injected | γ-irradiated | 79.2 at St 18–23 | N/A | N/A | N/A | N/A | N/A |
Donor | Enrichment | Recipient | % of Recipients with Gonadal Incorporation of Donor Cells | % of Recipients Producing Donor-Derived Gametes | Survival of Recipients (%) | % of Donor-Derived Offspring | Ref | ||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Species | Fish | Age | Cells | Method | Purity | Species | Fish | Age | Total | Male | Female | ||||
A. japonica | WT | Somito-genesis | 1 PGC | MC | N/A | D. rerio | WT | Blastula | 42.7 at 2 d | N/A | N/A | N/A | Con: 92.7 TP: 92.6 at 2 d | N/A | [161] |
C. auratus | WT | 10–15 somite St | 1 PGC | MC | N/A | D. rerio | Dnd-KD | Blastula | N/A | N/A | Y at 10–12 mo | N | N/A | N/A | [16] |
WT | 10–15 somite St | 1 PGC | MC | N/A | D. rerio | Dnd-KD | Blastula | 63.5 at 2 d | N/A | N/A | N/A | 69.0 at 2 d | N/A | [13] | |
Albino | 10–15 somite St | 1 PGC | MC | N/A | C. auratus | Dnd-KD | Blastula | 42.7 at 3 d | 42.9 at 5 mo–2 y | 62.5 at 5 mo–2 y | 30.1 at 5 mo–2 y | Dnd-KD: 88.3 TP: 84.9 | 92.5–100 | [65] | |
D. albolineatus | WT | 10–15 somite St | 1 PGC | MC | N/A | D. rerio | Dnd-KD | Blastula | 45.1 at 2 d | 89.5 at SM | 93.8 at SM | 66.7 at SM | Dnd-KD: 59.2 TP: 74.7 at 2 d | 100 | [16] |
WT | 10–15 somite St | 1 PGC | MC | N/A | D. rerio | Dnd-KD | Blastula | 40.2 at 2 d | N/A | N/A | N/A | 76.8 at 2 d | N/A | [13] | |
D. rerio | WT | 10–15 somite St | 1 PGC | FACS | 87.8–100 | D. rerio | Dnd-KD | Blastula | 31.5 at 1 dpt | N/A | N/A | N/A | Dnd-KD: 92.9 Dnd-KD + TP: 81.4 at 1 dpt | N/A | [17] |
WT | 10–15 somite St | 1 PGC | MC | N/A | D. rerio | Dnd-KD | Blastula | 30.0 at 2 d | N/A | N/A | N/A | 89.7 at 2 d | N/A | [13] | |
21–25 somite St | 10.1 at 2 d | N/A | N/A | N/A | 82.4 at 2 d | N/A | |||||||||
Prim-5 St | 5.3 at 2 d | N/A | N/A | N/A | 78.4 at 2 d | N/A | |||||||||
Prim-15 St | 4.5 at 2 d | N/A | N/A | N/A | 87.3 at 2 d | N/A | |||||||||
WT | 10–15 somite St | 1 PGC | MC | N/A | D. rerio | Dnd-KD | Blastula | 20.7 at prim-5 St | N/A | N/A | N/A | Con: 74.1 Dnd-KD: 59.4 TP: 66.7 | N/A | [8] | |
M. anguillicaudatus | WT | 10–15 somite St | 1 PGC | MC | N/A | D. rerio | Dnd-KD | Blastula | N/A | N/A | Y at 10–12 mo | N | N/A | N/A | [16] |
WT | 10–15 somite St | 1 PGC | MC | N/A | D. rerio | Dnd-KD | Blastula | 43.1 at 2 d | N/A | N/A | N/A | 85.7 at 2 d | N/A | [13] | |
O. masou | WT | 40 d | 5–10 PGCs | MC | N/A | O. mykiss | WT | Newly hatched | 24.4 at 10 dpt | N/A | N/A | N/A | N/A | N/A | [66] |
O. mykiss | TG:pvasa-GFP | 35 d | 5–10 PGCs | MC | N/A | O. mykiss | WT | 2.5 d | 0 at 30 dpt | N/A | N/A | N/A | 26 at 30 dpt | ♂: 3.9 ♀: 4.2–6.1 | [15] |
35 d | 6 d | 0 at 30 dpt | N/A | N/A | N/A | 62 at 30 dpt | |||||||||
35 d | 35 d | 21.6 at 30 dpt | 15.4 at 1–2 y | 16.7 at 1 y | 14.3 at 2 y | 94 at 30 dpt | |||||||||
35 d | 35 d | 10–20 * at 30 dpt | N/A | N/A | N/A | N/A | |||||||||
40 d | 35 d | 10–20 * at 30 dpt | N/A | N/A | N/A | N/A | |||||||||
45 d | 35 d | 0–10 * at 30 dpt | N/A | N/A | N/A | N/A | |||||||||
35 d | 40 d | 10–20 * at 30 dpt | N/A | N/A | N/A | N/A | |||||||||
40 d | 40 d | 0–10 * at 30 dpt | N/A | N/A | N/A | N/A | |||||||||
45 d | 40 d | 0 * at 30 dpt | N/A | N/A | N/A | N/A | |||||||||
35 d | 45 d | 0 * at 30 dpt | N/A | N/A | N/A | N/A | |||||||||
40 d | 45 d | 0 * at 30 dpt | N/A | N/A | N/A | N/A | |||||||||
45 d | 45 d | 0 * at 30 dpt | N/A | N/A | N/A | N/A | |||||||||
TG:pvasa-GFP | 35 d | 20 PGCs | MC | N/A | O. masou | WT | Newly hatched | 16.7 at 30 dpt | N/A | 13.5 at 1 y | Y at 17 mo | N/A | ♂: 0.4 | [154] | |
WT | 32 d | 5–10 PGCs | MC | N/A | O. mykiss | WT | Newly hatched | 12.3 at 10 dpt | N/A | N/A | N/A | N/A | N/A | [66] | |
TG:pvasa-GFP | 30 dpf | 15–20 PGCs | MC | N/A | O. mykiss | WT | 32–34 dpf | Fresh: 12.5 CP (d1): 10.1 at 30 dpt | Fresh: 10.9 CP (d1): 8.3 at 3 y | Fresh: 10.3 CP (d1): 7.8 at 3 y | Fresh: 12.1 CP (d1): 9.1 at 3 y | Fresh: 98.5 CP (d1): 86.5 at 30 dpt | Fresh ♂: 0.2–16.3 Fresh ♀: 0.2–7.6 CP (d1) ♂: 2.0–13.5 CP (d1) ♀: 0.1–3.3 | [53] | |
S. trutta | WT | 40 d | 5–10 PGCs | MC | N/A | O. mykiss | WT | Newly hatched | 9.4 at 10 dpt | N/A | N/A | N/A | N/A | N/A | [66] |
Hybrid | H. huso × A. ruthenus | Late-neural St | 1 PGC | MC | N/A | C. auratus | WT | Blastula | 9.1 at 3 d | N/A | N/A | N/A | 95.7 at 3 d | N/A | [162] |
Donor | Enrichment | Recipient | % of Recipients with Gonadal Incorporation of Donor Cells | % of Recipients Producing Donor-Derived Gametes | Survival of Recipients (%) | % of Donor-Derived Offspring | Ref | ||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Species | Fish | Age (Size) | Cells | Method | Purity | Species | Fish | Age (Size) | Total | Male | Female | ||||
A. baerii | WT | 4 y | TCs | PDGC | 79.4 | A. ruthenus | WT | 1 wph | 60.0 at 90 dpt | N/A | N/A | N/A | Con: 96.7 TP: 95.8 | N/A | [39] |
WT | 4 y | TCs | N/C | N/A | A. ruthenus | WT | Newly hatched | Fresh: 55.0 CP: 65.0 at 90 dpt | N/A | N/A | N/A | N/A | N/A | [195] | |
WT | 4 y | OCs | PDGC | 70.8 | A. ruthenus | WT | 1 wph | 60.0 at 90 dpt | N/A | N/A | N/A | Con: 96.7 TP: 95.8 | N/A | [39] | |
WT | 4 y | OCs | N/C | N/A | A. ruthenus | WT | Newly hatched | Fresh: 70.0 CP: 55.0 at 90 dpt | N/A | N/A | N/A | N/A | N/A | [195] | |
A. dabryanus | WT | 2 y | 50,000 TCs | N/C | N/A | A. dabryanus | WT | 7–8 dph | 70.0 at 51 dpt | N/A | N/A | N/A | Con: 86.2 TP: 76.7 at 51 dpt | N/A | [196] |
A. sinensis | WT | 11.5 y | 50,000 OCs | N/C | N/A | A. dabryanus | WT | 7–8 dph | 20.0 at 51 dpt | N/A | N/A | N/A | Con: 86.2 TP: 68.6 at 51 dpt | N/A | [196] |
C. carpio | WT | 2 y | 30,000–50,000 TCs | PDGC | N/A | C. auratus | Dnd-KD | 7 d | 62.5 at 1 mo | 43.7 at 3 y | 32.4 at 3 y | 11.2 at 3 y | Con: 74 Dnd-KD: 79 Dnd-KD + TP: 72 at 18 mpf | 100 | [29] |
D. rerio | TG:ppiwil1-DsRed | 2–3 mo | 10–60 SG | PDGC | N/A | D. rerio | Dnd-KD | 2 w | N/A | N/A | Cult (3 w): 19 Cult (6 w): 18 at SM | N/A | Cult (3 w): 72.2 Cult (6 w): 64.9 at SM | 100 | [126] |
TG:pvasa-EGFP | Adult | 3000 GFP+ TCs | N/C | N/A | D. rerio | WT | 9–10 d | 6.7 at 50 dpt | N/A | 6.7 at SM | N/A | N/A | 3.9–7.3 | [101] | |
Dnd-KO | 5.0 at 50 dpt | N/A | 5.0 at SM | N/A | N/A | 100 | |||||||||
TG:pvasa-EGFP | 2 mo | 3000–5000 TCs | N/C | N/A | D. rerio | 3N | 7 d | 53.2 at adult | N/A | 43.5 at adult | N/A | 2N Con: 83.3 3N Con: 75.6 3N TP: 68.9 at adult | 100 | [145] | |
TG:pvasa-EGFP or TG:pβact-YFP | 3–6 mo | 3000 GFP+ TCs | N/C | N/A | D. rerio | WT | 7 d | Fresh: 31.1 CP: 24.4 VF: 22.2 at 50 dpt | N/A | N/A | N/A | Contro: 80 TP: 85 at 50 dpt | N/A | [135] | |
Dnd-KD | Fresh:58.3 CP: 47.4 VF: 50.0 at 50 dpt | N/A | 43 at 6 mo | N/A | N/A | 100 | |||||||||
TG:pvasa-DsRed2- vasa;pβact-EGFP | 3 mo | OCs | PDGC | N/A | Hybrid | ♂ D. albolineatus × ♀ D. rerio | 2 w | 20.0 at 8 w | 17.9 at 6 mo | 17.9 at 6 mo | 0 at 6 mo | 52.7 at 6 mo | 100 | [69] | |
TG:pziwi-Neo;pziwi-DsRed | 10–12 w | 20–40 FGSCs | PDGC | N/A | D. rerio | Dnd-KD | 2 w | N/A | N/A | Cult (3 w): 20.0 Cult (6 w): 16.0 at SM | N/A | Cult (3 w): 73.5 Cult (6 w): 71.7 at SM | 100 | [123] | |
TG:pvasa-EGFP | 2 mo | 500 OCs | N/C | N/A | D. rerio | 3N | 7 d | 43.6 at adult | N/A | 34.5 at adult | N/A | 2N Con: 83.3 3N Con: 75.6 3N TP: 61.1 at adult | 100 | [145] | |
N. mitsukurii | WT | 3 mo | 10,000 TCs | N/C | N/A | S. japonicus | WT | 5 d | 33.5 at 21 dpt | N/A | N/A | N/A | 20.3 at 21 dpt | N/A | [99] |
7 d | 70.0 at 21 dpt | N/A | N/A | N/A | 20.6 at 21 dpt | N/A | |||||||||
9 d | 4.4 at 21 dpt | N/A | N/A | N/A | 27.6 at 21 dpt | N/A | |||||||||
WT | 3 mo | 3000 TCs | FACS | Unsort: 18.8 Sort: 94.0 | N. mitsukurii | WT | 12 d | Unsort: 7.6 Sort: 60.0 at 20 dpt | N/A | N/A | N/A | N/A | N/A | [19] | |
TG:pHSC-GFP | 3 mo | 10,000 TCs | N/C | N/A | N. mitsukurii | 3N (<100% incidence) | 12 dph | 2N: 63.3 3N: 56.0 at 18 dpt | 2N: 6.1 3N: 31.4 at 6 mo | 2N: 5.3 3N: 36.8 at 6 mo | 2N: 6.8 3N: 28.9 at 6 mo | 41.1 at 18 dpt | 2N ♂: 6.8–89.2 3N ♂: 100 2N ♀: 2.2–25.0 3N ♀: 100 | [63] | |
TG:pHSC-GFP | 3 mo | 10,000 TCs | N/C | N/A | N. mitsukurii | WT | 12 d | 58.3 at 2 wpt | N/A | N/A | N/A | 68.1 at 2 wpt | N/A | [27] | |
Hybrid | ♂ P. argentata × ♀ N. mitsukurii, 3N | 12 d | 58.6 at 2 wpt | 34.4 at 6 mo | 34.4 at 6 mo | 0 at 6 mo | 34.7 at 2 wpt | ♂: 100 | |||||||
O. masou | WT | 12–13 mo | 3000 TCs | FACS | Unsort: 16.4 Sort: 75.6 | O. mykiss | WT | Newly hatched | Unsort: 0–25 * Sort: 80.0 at 20 dpt | N/A | N/A | N/A | N/A | N/A | [19] |
WT, black | 8 mo | 50,000 TCs | N/C | N/A | O. masou | 3N | 40–42 d | Fresh: 50–60 * CP: 58.2 at 50 dpt | CP: 39.1 at 2 y | CP: 43.5 at 2 y | CP: 34.8 at 2 y | N/A | 100 | [28] | |
WT, black | 8 mo | 50,000 OCs | N/C | N/A | O. masou | 3N | 40–42 d | Fresh: 40–60 * CP: 41.2 at 50 dpt | CP: 25.8 at 2 y | CP: 29.3 at 2 y | CP: 23.1 at 2 y | N/A | 100 | [28] | |
O. mykiss | Albino, TG:pvasa-GFP | 9 mo | 18,000 TCs (10,000 GFP+ cells) | FACS | N/A | O. mykiss | WT | Newly hatched | ♂: 38.8 ♀: 57.8 at 2 mpt | N/A | 50 at 1 y | 40 at 2 y | N/A | ♂: 5.5 (0.2–40.5) ♀: 2.1 (0.1–9.9) | [37] |
TG:pvasa-GFP | Adult | TCs | N/C | N/A | O. masou | 3N | Newly hatched | N/A | N/A | 34.5 at 2 y | 50.0 at 17 mo; 10.0 at 2–3 y | N/A | ♂: 100 ♀: 100 | [146] | |
TG:pvasa-GFP | 8–10 mo | 10,000 TCs | DP | 95–99 | O. mykiss | WT | Newly hatched | Sort: 77.7 Sort + Cult (1 mo): 52.2 at 30 dpt | N/A | N/A | N/A | N/A | N/A | [75] | |
TG:pvasa-GFP | 16 mo | 3000 TCs | FACS | N/A | O. mykiss | WT | Newly hatched | Sort-A: 51.0 Sort-B: 0 at 60 dpt | N/A | N/A | N/A | N/A | N/A | [67] | |
7 mo | 3000 ASG | N/C | N/A | 53.6 at 60 dpt | N/A | N/A | N/A | N/A | N/A | ||||||
WT | 8–12 mo | 3000 TCs | FACS | N/A | O. mykiss | WT | Newly hatched | Unsort: 23.0 Sort: 78.3 at 20 dpt | N/A | N/A | N/A | N/A | N/A | [19] | |
TG:pvasa-GFP | 8–12 mo | Unsort: 35.9 Sort: 93.2 | Unsort: 29.0 Sort: 82.0 at 20 dpt | N/A | N/A | N/A | N/A | N/A | |||||||
TG:pvasa-GFP | 16 or 24 mo | Sort: 90.0–96.2 | N/A | N/A | N/A | N/A | N/A | N/A | |||||||
TG:pvasa-GFP | 11–12 mo | 5000 TCs | DP | >90 | O. mykiss | WT | 25–27 d | Fresh: 59.7 Cult + Sort: 94.5 Cult + Sort + Tryp-2 h: 43.9 at 20 dpt | N/A | N/A | N/A | N/A | N/A | [73] | |
TG:pMlc2-GFP | 6 mo | 10,000 ASG | PDGC + CE | >90 | O. mykiss | WT | Peri-hatching | 90 at 6 mo | N/A | 90 at 1–2 y | N/A | N/A | 1–56 | [23] | |
1 y | >90 | 78 at 6 mo | N/A | N/A | N/A | N/A | N/A | ||||||||
Mature | >70 | 42 at 6 mo | N/A | N/A | N/A | N/A | N/A | ||||||||
TG:pvasa-GFP | 11 mo | 500 GFP+ TCs | N/C | N/A | O. mykiss | 3N | 32 d | Fresh: 30–40 * CP (F371): 30–40 * at 50 dpt | Fresh: 32.4 CP (F371): 28.6 at 2 y | Fresh: 35.0 CP (F371): 40.0 at 2 y | Fresh: 29.4 CP (F371): 15.4 at 2 y | N/A | 100 | [61] | |
18 mo | O. mykiss | 32 d | Fresh: 40–60 * CP (F371): 40–60 * at 30 dpt | N/A | N/A | N/A | N/A | N/A | |||||||
11 mo | O. masou | 37 d | Fresh: 20–30 * CP (F371): 20–30 * at 50 dpt | Fresh: 27.6 CP (F371): 24.0 at 2 y | Fresh: 33.3 CP (F371): 30.8 at 2 y | Fresh: 23.5 CP (F371): 16.7 at 2 y | N/A | 100 | |||||||
TG:pvasa-GFP | 8 mo | 30,000 TCs | N/C | N/A | O. masou | WT | 38–40 d | 63.2 at 20 dpt | N/A | N/A | N/A | N/A | N/A | [124] | |
Dnd-KD | 70 at 20 dpt | 54.5 at 2 y | 46.7 at 2 y | 71.4 at 2 y | N/A | ♂: 100 (6 Inds); 72.3 (1 Ind) ♀: 100 (2 Inds); 21.1 (3 Inds) | |||||||||
TG:pvasa-GFP | 9–11 mo | 1000 TCs | FACS (AB No. 80 or No. 95) | Unsort: <20 * Sort (No. 80): 70.7 Sort (No. 95): 80.9 | O. mykiss | WT | Newly hatched | Unsort: 1.1 Sort (No. 80): 19.2 Sort (No. 95): 18.4 at 20 dpt | N/A | N/A | N/A | N/A | N/A | [20] | |
TG:pvasa-GFP | 13–14 mo | <2000 TCs | MACS (AB No. 172) | Unsort: 49.8 Sort: 81.7 | O. mykiss | WT | Newly hatched | Unsort: 10–20 * Sort: 30–40 * at 20 dpt | N/A | N/A | N/A | N/A | N/A | [62] | |
TG:pvasa-GFP | 12–15 mo | 15,000 SG | DP | N/A | O. mykiss | 3N | 30 d | Fresh: 60–80 * Cult: 60–80 * at 20 dpt | Fresh: 89.2 Cult: 65.0 at 1 y | Fresh: 88.0 Cult: 77.6 at 1 y | Fresh: 73.3 Cult: 36.8 at 2 y | N/A | ♂: 100 ♀: 100 | [147] | |
TG:pvasa-GFP | 6–9 mo | 15,000 OCs | N/C | N/A | O. mykiss | 3N | 25 d | ♂: 50.0 ♀: 47.1 at 5 mo | 10.0 at 2 y | 15.0 at 2 y | 5.0 at 2 y | N/A | ♂: 100 ♀: 100 | [21] | |
TG:pvasa-GFP | 9 mo | <10,000 GPF+ OCs | N/C | N/A | O. mykiss | 3N | 33 d | Fresh: 60–80 * CP: 57.1 at 50 dpt | Fresh: 25.0 CP: 24.0 at 2.5 y | Fresh: 30.8 CP: 28.0 at 2.5 y | Fresh: 18.2 CP: 20.0 at 2.5 y | N/A | Fresh: 100 CP: 100 | [56] | |
TG:pvasa-GFP | 12–14 mo | <10,000 OCs | MACS (AB No. 172) | Unsort: 5.2 Sort: 54.8 | O. mykiss | WT | Newly hatched | Unsort: 0–20 * Sort: 60–80 * at 20 dpt | N/A | N/A | N/A | N/A | N/A | [62] | |
O. nerka | WT | 15 mo | <5000 TCs | MACS (AB No. 172) | Unsort: 16.4 Sort: 68.6 | O. mykiss | WT | Newly hatched | Unsort: 0–20 * Sort: 40–60 * at 20 dpt | N/A | N/A | N/A | N/A | N/A | [62] |
O. niloticus | TG:pβact-EGFP | 5–12 mo | 20,000 TCs | N/C | N/A | O. niloticus | WT | 6 d | 0 at 5 mo | N/A | N/A | N/A | N/A | N/A | [137] |
7 d | 6.7 at 5 mo | 37.5 at 1 y | 40.0 at 1 y | 33.3 at 1 y | N/A | 2.4 | |||||||||
8 d | 0 at 5 mo | N/A | N/A | N/A | N/A | N/A | |||||||||
O. latipes | TG:pvasa-GFP | 2–4 mo | 15,000 TCs | N/C | N/A | O. latipes | WT | 7 d | >50 * at 1 mpt | N/A | N/A | N/A | 20.0 at 1 mpt | N/A | [55] |
15,000 TCs | WT | 11 d | >50 * at 1 mpt | N/A | N/A | N/A | 90 at 1 mpt | N/A | |||||||
15,000 TCs | WT | 14 d | <50 * at 1 mpt | N/A | N/A | N/A | 90 at 1 mpt | N/A | |||||||
15,000 TCs | WT | 19 d | 0 * at 1 mpt | N/A | N/A | N/A | 90 at 1 mpt | N/A | |||||||
15,000 TCs | WT | 23 d | 0 * at 1 mpt | N/A | N/A | N/A | 90 at 1 mpt | N/A | |||||||
300 TCs | WT | 11 d | 10 at 1 mpt | N/A | N/A | N/A | N/A | N/A | |||||||
1000 TCs | WT | 11 d | 10 at 1 mpt | N/A | N/A | N/A | N/A | N/A | |||||||
3000 TCs | WT | 11 d | 60 at 1 mpt | N/A | N/A | N/A | N/A | N/A | |||||||
10,000 TCs | WT | 11 d | 60 at 1 mpt | N/A | N/A | N/A | N/A | N/A | |||||||
30,000 TCs | WT | 11 d | 60 at 1 mpt | N/A | N/A | N/A | N/A | N/A | |||||||
15,000 TCs | 3N | 11 d | N/A | Fresh: 63.6 CP: 70.0 at 2–3 mo | N/A | N/A | N/A | 100 | |||||||
Wnt4b (-/-) mutant | - | 15,000 TCs | N/C | N/A | O. latipes | 3N | 11 d | N/A | CP: 83.3 at 2–3 mo | N/A | N/A | N/A | 100 | [55] | |
Tokyo-medaka (endangered) | 1 y | TG:pvasa-GFP, 3N | N/A | CP: 63.9 at 2–3 mo | N/A | N/A | N/A | 100 | |||||||
Kaga (inbred) | - | TG:pvasa-GFP, 3N | N/A | CP: 58.6 at 2–3 mo | N/A | N/A | N/A | 100 | |||||||
Fshr mutant (-/-), XX male | 3 mo | 3000–9000 TCs | N/C | N/A | Hybrid | ♂ O. curvinotus × ♀ O. latipes or ♂ O. latipes × ♀ O. curvinotus | Newly hatched | N/A | N/A | N/A | 35.3 at 3 mo | N/A | 100 | [144] | |
TG:pvasa-GFP | 2 mo | 12,000 TCs | N/A | N/A | N/A | 48.3 at 3 mo | N/A | N/A | |||||||
WT | Adult | 1000 OCs | PDGC + DP | N/A | O. latipes | WT | 11 d | [Cult (10 d)] Con: 15.0 On pDA: 25.0 On pDA/PLL: 0 at 20 d | N/A | N/A | N/A | 50.0–80.0 at 20 d | N/A | [197] | |
WT | Adult | 1000 OCs | PDGC + DP | N/A | O. latipes | WT | 11 d | Con: 14.3 Sort: 32.1 at 20 d | N/A | N/A | N/A | 57.1–72.4 at 20 d | N/A | [70] | |
P. dentatus | WT | N/A | TCs | PDGC | N/A | P. olivaceus | 3N | 17 dph | 100 at 14 dpt | N/A | Merged: 100 at 2 y | N/A | [Merged] Con: 27.1 at 3 y TP: 4.0 at 2 y | Merged: Y | [148] |
20 dph | 90.0 at 14 dpt | N/A | N/A | ||||||||||||
P. olivaceus | WT | N/A | TCs | PDGC | N/A | P. olivaceus | 3N | 16 dph | 100 at 14 dpt | N/A | Merged: 100 at 2 y | N/A | [Merged] Con: 27.1 at 3 y TP: 6.8 at 2 y | Merged: Y | [148] |
19 dph | 100 at 14 dpt | N/A | N/A | ||||||||||||
22 dph | 100 at 14 dpt | N/A | N/A | ||||||||||||
P. spathula | WT | 2.5 y | 50,000 TCs | PDGC | N/A | A. dabryanus | WT | 7–8 dph | 80.6 at 2 mo | N/A | N/A | N/A | Con: 76.5 TP: 68.5 at 2 mo | N/A | [198] |
S. salar | WT | 1 y | 2000–5000 TCs | N/C | N/A | O. mykiss | 3N (Shasta/ Shasta/albino) | Newly hatched | 61.1 at 4 wpt | 11.0 at 1–2 y | 10.0 at 1–2 y | 12.1 at 2 y | N/A | ♂: 100 ♀: N/A | [150] |
S. trutta | WT | 9–12 mo | 4000–5000 TCs | FACS (AB No. 95) | Unsort: 21.2 Sort: 80.6 | O. mykiss | WT | Newly hatched | Con: 15.8 Sort: 34.7 at 20 dpt | N/A | N/A | N/A | N/A | N/A | [86] |
S. leucomaenis | WT | 12–13 mo | 3000 TCs | FACS | Unsort: 10.1 Sort: 79.9 | O. mykiss | WT | Newly hatched | Unsort: 0 Sort: 48.8 at 20 dpt | N/A | N/A | N/A | N/A | N/A | [19] |
S. maximus | WT | N/A | TCs | PDGC | N/A | P. olivaceus | 3N | 15 dph | 60.0 at 14 dpt | N/A | Merged: 40.0 at 2 y | N/A | [Merged] Con: 27.1 at 3 y TP: 10.0 at 2 y | Merged: Y | [148] |
18 dph | 40.0 at 14 dpt | N/A | N/A | ||||||||||||
21 dph | 30.0 at 14 dpt | N/A | N/A | ||||||||||||
S. quinqueradiata | WT | 10 mo | 20,000 TCs | N/C | N/A | S. quinqueradiata | WT | 6 dph | 100 at 28 dpt | N/A | N/A | N/A | 8.0 at 28 dpt | N/A | [155] |
8 dph | 100 at 28 dpt | N/A | N/A | N/A | 10.9 at 28 dpt | N/A | |||||||||
10 dph | 85.7 at 28 dpt | N/A | N/A | N/A | 15.9 at 28 dpt | N/A | |||||||||
12 dph | 85.7 at 28 dpt | N/A | N/A | N/A | 29.6 at 28 dpt | N/A | |||||||||
Merged | N/A | N/A | 100 at 1.5–2.5 y | 100 at 2.5 y | 5.08 at SM | ♂: 66.6 (19.6–98.8) ♀: 63.2 (17.0–97.5) | |||||||||
T. rubripes | WT | 1 y | 4000–6000 TCs | N/C | N/A | T. alboplumbeus | 3N (<100% incidence) | 1 dph | 50 at 4 wpt | N/A | 38.3 at 11 mo | 31.3 at 2 y | 47 at 72 wpt | ♂: 100 ♀: 5–95 | [138] |
5 dph | 33.3 at 4 wpt | N/A | 23.7 at 11 mo | 23.1 at 2 y | 41.4 at 72 wpt | ||||||||||
WT | 10–12 mo | 5000 TCs | N/C | N/A | T. alboplumbeus | 3N (<100% incidence) | 1 dph | Fresh: 39.1 CP: 38.9 at 40 dph | N/A | [CP] 2N: 36.4 3N: 64.2 at 10 mph | [CP] 2N: 0 3N: 1.6 at 2 y | Con: 41.4 Fresh: 21.8 CP: 14.5 at 40 dph | 2N ♂: 3.2–87.5 (3 Inds) 2N ♀: 0 (10 Inds) 3N ♂: 100 (11 Inds); 62.5 (1 Ind) 3N ♀: 100 (1 Ind) | [120] | |
WT | 1 y | 5000 TCs | N/C | N/A | T. alboplumbeus | WT | 1 dph | 40.0 at 40 dph | N/A | N/A | N/A | Con: 23.8 at 40 dph; 45.3 at 12 mph TP: 14.8 at 40 dph | N/A | [127] | |
Dnd-KD | 40.5 at 40 dph | N/A | 91.7 at 10 mo | 26.7 at 2 y | Dnd-KD: 20.3 and 35.0 Dnd-KD + TP: 15.8 and 16.9 at 40 dph and 12 mph | ♂: 100 (7 Inds); 12.5–87.5 (2 Inds) ♀: 100 (3 Inds) | |||||||||
T. maccoyii | WT | 57.0 kg | TCs | PDGC | N/A | S. lalandi | WT | 6–7 dph | 33.3 at 18 dpt | N/A | N/A | N/A | 9.1 at 64 dph | N/A | [47] |
9–10 dph | 37.5 at 18 dpt | N/A | N/A | N/A | 9.2 at 64 dph | N/A | |||||||||
T. orientalis | WT | 0 y | TCs | N/C | N/A | S. japonicus | WT | 7 d | 0 at 21 dpt | N/A | N/A | N/A | N/A | N/A | [22] |
1 y | 5.4 at 21 dpt | N/A | N/A | N/A | N/A | N/A | |||||||||
3 y | 0 at 21 dpt | N/A | N/A | N/A | N/A | N/A | |||||||||
WT | 2–4 y | >10,000 TCs | FACS (AB No. 152) | Unsort: 16.6 Sort: 77.3 | N. mitsukurii | WT | 12 dph | PDGC Sort (PKH26 labled): 33.3 PDGC Sort (No. 152 AB labeled): 63.3 at 14 dpt | N/A | N/A | N/A | N/A | N/A | [45] | |
WT | 3 y | >10,000 TCs | PDGC | N/A | Hybrid | ♂ S. japonicus × ♀ S. australasicus | 10 d | 100 at 14 dpt | N/A | N/A | N/A | N/A | N/A | [48] | |
WT | 2 y | >30,000 TCs | N/C | N/A | S. japonicus | WT | 7 dph | Y at 14 dpt and 4 mpt | N/A | N/A | N/A | N/A | N/A | [46] | |
E. affinis | WT | 10 dph | Y at 14 dpt and 3 mpt | N/A | N/A | N/A | N/A | N/A |
Donor | Enrichment | Recipient | % of Recipients with Gonadal Incorporation of Donor Cells | % of Recipients Producing Donor-Derived Gametes | Survival of Recipients (%) | % of Donor-Derived Offspring | Ref | |||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Species | Fish | Age (Size) | Cells | Method | Purity | Species | Fish | Sex | Age (Size) | Total | Male | Female | ||||
D. rerio | TG:pvasa -EGFP | Adult | TCs | FACS | Unsort: 10–20 * Sort: 60–70 * | D. rerio | WT, HT + B treated | ♂ | Adult | 30 at 3 wpt | N/A | N/A | N/A | N/A | N/A | [128] |
♀ | Adult | Y at 3 wpt | N/A | N/A | N/A | N/A | N/A | |||||||||
I. furcatus | WT | 2 y | 2 × 104–1.43 × 106 TCs | PDGC | N/A | I. punctatus | 3N | ♂ | 2 y | 87.5 at 10 mpt | N/A | Y at 2 ypt | N/A | N/A | Y | [199] |
N. mitsukurii | TG:pHSC -GFP | 3 mo | 2 × 106 TCs | N/C | N/A | Hybrid | ♂ P. argentata × ♀ N. mitsukurii | ♂ | 6 mo | 37.5 at 6 wpt | N/A | 10 at 25 wpt | N/A | 77.0 at 1 dpt | 100 | [31] |
TG:pHSC -GFP | 3 mo | 2 × 106 OCs | N/C | N/A | Hybrid | ♂ P. argentata × ♀ N. mitsukurii, 3N | ♀ | 6 mo | N/A | 33.3 at 9 mpt | 16.6 at 9 mpt | 16.6 at 9 mpt | 75 at mpt | 100 | [104] | |
O. bonariensis | WT | 4–5 mo | 4 × 104 TCs (for each lobe, surgery) | PDGC | N/A | O. hatcheri | WT, HT + B treated | ♂ | 1 y | 33.3 at 6 wpt | N/A | 20.0 at 6 mpt | N/A | N/A | 1.2–13.3 | [149] |
WT | 4–5 mo | 3.75 × 106 TCs | PDGC | N/A | O. hatcheri | WT, HT + B treated | ♂ | 1 y | 80.0 at 8 wpt | N/A | 17.6 at 7 mpt | N/A | N/A | 12.6–39.7 | [100] | |
WT | 4–5 mo | 3.75 × 106 Ocs | PDGC | N/A | O. hatcheri | WT, HT + B treated | ♀ | 1 y | 60.0 at 8 wpt | N/A | N/A | 5.0 at 7 mpt | N/A | 39.7–52.2 | [100] | |
O. niloticus | WT | Adult | 1 × 107 TCs | PDGC + DP | N/A | O. niloticus | WT, HT + B treated | ♂ | Adult | 89.5 at 8–9 wpt | N/A | Y at 9 wpt | N/A | N/A | 6.3 | [32] |
P. olivaceus | WT | 1 y | OCs | PDGC | Unsort: 37.8 Sort: 83.6 | P. olivaceus | WT, HT + B treated | ♂ | 2 y | Y at 123 dpt | N/A | 11.7 at 10 mpt | N/A | 100 at 10 mpt | 43.0–45.5 | [72] |
R. quelen | WT | 289 g | 1 × 107 TCs | PDGC + DP | N/A | O. niloticus | WT, HT + B treated | ♂ | 208 g | 100 at 2 mpt | N/A | N/A | N/A | N/A | N/A | [163] |
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Method | Principle | Advantage | Disadvantage | Enrichment of Fish GSCs |
---|---|---|---|---|
PDGC | Fractionating cells by their density with centrifugation | Simple procedure No need for special materials, techniques, and equipment | Low purity | The most frequently used method 60–83.6% purity [39,71,72] |
DP | Positive or negative selection based on adherence of cells by in vitro culture | Simple procedure No need for special materials, techniques, and equipment | Low purity Relatively long procedure Potential risks of spontaneous differentiation during in vitro culture | Frequently used >90% purity by serial DPs [73,75] No available commercial molecules for positive selection |
CE | Aligning and eluting cells by their physical characteristics with centrifugation | High purity expected Not requiring TGs or ABs | Requiring special sorting conditions and equipment | >90% purity by combining with PDGC [23] |
FACS | Isolation of cells based on light-scattering properties | High purity expected Flexible sorting condition by customizing gates based on size, granularity, and fluorescent intensity of cells | Requiring special skills and equipment Requiring specific ABs against the surface protein of target cells, TGs carrying germ cells expressing FPs, or other specific sorting conditions Not suitable for large scales | Up to 100% purity of PGCs labeled with mRNA-nanos3 3′ UTR encoded FP [17] 93.2–99% purity with TGs [18,19,85] 70.7–80.9% purity using ABs [20,45,86] 75.6–94.9% purity without using TGs or ABs [19,87] Limitation of using TG fish for commercial application No available commercial fish ABs |
MACS | Affinity based cell sorting with magnetic particles-conjugated ABs against cell surface proteins | High purity expected No need for special techniques or equipment Simpler than FACS Applicable to large scales | Requiring specific ABs against the surface protein of target cells | 54.8–81.7% purity [62] No available commercial fish ABs |
Method | Principle | Advantage | Disadvantage | Recipient Case |
---|---|---|---|---|
Interspecific hybridization | Preventing normal meiosis by a chromosomal mismatch or arresting mitosis of PGCs | Simple preparation by breeding without any treatment Complete germ cell elimination (in germ cell-less hybrids) | Unpredictable reproductive phenotypes depending on species/sex combination | ♂ D. albolineatus × ♀ D. rerio [69], O. curvinotus × O. latipes [144], ♂ P. argentata × ♀ N. mitsukurii [27,31,104] |
Triploidization | Preventing normal meiosis by a chromosomal mismatch | Relatively simple procedure | Potential risks of endogenous germ cell-derived gamete production Unstable efficiency depending on species and method | D. rerio [145], N. mitsukurii [63], O. masou [28,146], O. mykiss [21,56,147], O. latipes [55], P. olivaceus [148], T. alboplumbeus [120,138] |
Dnd-knockdown | Disrupting PGC development by MO-mediated inhibition of Dnd expression | High efficiency expected Possibility of complete germ cell elimination | Requiring special techniques, apparatus, or materials Not guaranteed 100% sterility | C. auratus [29,65], D. rerio [16,123,126], O. masou [124], O. latipes [64], T. alboplumbeus [127] |
Dnd-knockout | Disrupting germ cell development by blocking Dnd expression through gene editing | Guaranteed 100% sterility in homozygous mutants Complete germ cell elimination | Requiring genetic knowledge, techniques, apparatus, and time to establish mutant lines Only 25% sterile fish of total | D. rerio [101], O. mykiss [38] |
High temperature + busulfan co-treatment | Arresting meiosis and inducing apoptosis of germ cells | Preparable in a few weeks with wild-type adults | Incomplete germ cell ablation Requiring optimized conditions to achieve low mortality and successful germ cell ablation | O. hatcheri [100,149], O. niloticus [32], P. olivaceus [72] |
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Ryu, J.H.; Xu, L.; Wong, T.-T. Advantages, Factors, Obstacles, Potential Solutions, and Recent Advances of Fish Germ Cell Transplantation for Aquaculture—A Practical Review. Animals 2022, 12, 423. https://doi.org/10.3390/ani12040423
Ryu JH, Xu L, Wong T-T. Advantages, Factors, Obstacles, Potential Solutions, and Recent Advances of Fish Germ Cell Transplantation for Aquaculture—A Practical Review. Animals. 2022; 12(4):423. https://doi.org/10.3390/ani12040423
Chicago/Turabian StyleRyu, Jun Hyung, Lan Xu, and Ten-Tsao Wong. 2022. "Advantages, Factors, Obstacles, Potential Solutions, and Recent Advances of Fish Germ Cell Transplantation for Aquaculture—A Practical Review" Animals 12, no. 4: 423. https://doi.org/10.3390/ani12040423
APA StyleRyu, J. H., Xu, L., & Wong, T.-T. (2022). Advantages, Factors, Obstacles, Potential Solutions, and Recent Advances of Fish Germ Cell Transplantation for Aquaculture—A Practical Review. Animals, 12(4), 423. https://doi.org/10.3390/ani12040423