Reversible Sterilization of Channel Catfish via Overexpression of Glutamic Acid Decarboxylase Gene

Author:

Ye Zhi123ORCID,Elaswad Ahmed14ORCID,Su Baofeng1ORCID,Alsaqufi Ahmed15,Shang Mei1,Bugg William S.16,Qin Guyu17,Drescher David18,Li Hanbo1,Qin Zhenkui13ORCID,Odin Ramjie19,Makhubu Nonkonzo1,Abass Nermeen110ORCID,Dong Sheng111ORCID,Dunham Rex1

Affiliation:

1. School of Fisheries, Aquaculture, and Aquatic Sciences, Auburn University, Auburn, AL 36849, USA

2. Key Laboratory of Tropical Aquatic Germplasm of Hainan Province, Sanya Oceanographic Institution, Ocean University of China, Sanya 572024, China

3. MOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao 266100, China

4. Center of Excellence in Marine Biotechnology, Sultan Qaboos University, Muscat 123, Oman

5. Department of Aquaculture and Animal Production, College of Agriculture and Food Sciences, King Faisal University, Al-Ahsa 31982, Saudi Arabia

6. Department of Forest and Conservation Sciences, University of British Columbia, Vancouver, BC V6T 1Z4, Canada

7. Division of Genetics, Department of Medicine, Brigham & Women’s Hospital, Harvard Medical School, Boston, MA 02115, USA

8. Fisheries Department, Muckleshoot Indian Tribe, Auburn, WA 98092, USA

9. College of Fisheries, Mindanao State University-Maguindanao, Datu Odin Sinsuat 9601, Philippines

10. Department of Agricultural Botany, Faculty of Agriculture Saba-Basha, Alexandria University, Alexandria 21531, Egypt

11. Department of Biological and Environmental Engineering, Cornell University, Ithaca, NY 14853, USA

Abstract

The confinement of transgenic fish is essential to prevent their escape and reproduction in natural ecosystems. Reversible transgenic sterilization is a promising approach to control the reproduction of transgenic fish. Therefore, the present study was conducted to develop a reversibly sterile channel catfish (Ictalurus punctatus) via the transgenic overexpression of the goldfish (Carassius auratus) glutamic acid decarboxylase (GAD) gene driven by the common carp (Cyprinus carpio) β-actin promoter to disrupt normal gamma-aminobutyric acid (GABA) regulation. Three generations of GAD-transgenic fish were produced. All studied generations showed repressed reproductive performance; however, this was not always statistically significant. In F1, 5.4% of the transgenic fish showed a sexual maturity score ≥ 4 (maximum = 5) at five years of age, which was lower (p = 0.07) than that of the control group (16.8%). In the spawning experiments conducted on F1 transgenic fish at six and nine years of age, 45.5% and 20.0% of fish spawned naturally, representing lower values (p = 0.09 and 0.12, respectively) than the percentages in the sibling control fish of the same age (83.3% and 66.7%, respectively). Four of six pairs of the putative infertile six-year-old fish spawned successfully after luteinizing hormone-releasing hormone analog (LHRHa) therapy. Similar outcomes were noted in the three-year-old F2 fish, with a lower spawning percentage in transgenic fish (20.0%) than in the control (66.7%). In one-year-old F2-generation transgenic fish, the observed mean serum gonadotropin-releasing hormone (GnRH) levels were 9.23 ± 2.49 and 8.14 ± 2.21 ng/mL for the females and males, respectively. In the control fish, the mean levels of GnRH were 11.04 ± 4.06 and 9.03 ± 2.36 ng/mL for the females and males, respectively, which did not differ significantly from the control (p = 0.15 and 0.27 for females and males, respectively). There was no significant difference in the estradiol levels of the female transgenic and non-transgenic fish in the one- and four-year-old F2-generation fish. The four-year-old F2-generation male transgenic fish exhibited significantly (p < 0.05) lower levels of GnRH and testosterone than the control fish. In conclusion, while overexpressing GAD repressed the reproductive abilities of channel catfish, it did not completely sterilize transgenic fish. The sterilization rate might be improved through selection in future generations.

Funder

US Department of Agriculture Biotechnology Risk Assessment Grant Program

Publisher

MDPI AG

Reference67 articles.

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