Abnormal meiosis in fertile and sterile triploid cyprinid fish

Chun, Zhang; Li, Qi; Zhu, La; He, Wangchao; Yang, Chungang; Zhang, Hui; Sun, Yu; Zhou, Li; Sun, Yuena; Zhu, Shurun; Wu, Chang; Tao, Min; Zhou, Yi; Zhao, Rurong; Tang, Chenchen; Liu, Shaojun

doi:10.1007/s11427-020-1900-7

Cited by 20 publications

(17 citation statements)

References 21 publications

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“…The 4nAT has 200 chromosomes, and its kidney cells also show two strong signals and a few weak signals (Figure 2a). Here, the two strong signals indicated two homologous chromosomes from the genomes of RCC, as CC with no major signals has been reported in a previous study (Zhang et al, 2015; Zhang et al, 2021), which further verified the chromosome constitution of 4nAT with two sets of genomes of RCC and two sets of genomes of CC. 5S rDNA localization on the pachytene stage of meiosis I cells in 4nAT showed two strong signals that appeared in pairs (Figure 2b), which indicated that pairing of homologous chromosomes in 4nAT occurred between the two identical RCC genomes, and between the two identical CC genomes.…”

Section: Resultssupporting

confidence: 84%

Localization of 5S rDNA analysis of homologous pairing in tetraploid hybrids of red crucian carp (♀) × common carp (♂)

Zhang

Sun

Zhu

et al. 2021

J World Aquaculture Soc

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Interspecies crossing and allopolyploidization increase the opportunity for generating new breeding resources for fish farming. Allotetraploid hybrid fish (4nAT) were created by crossing red crucian carp (RCC, Carassius auratus red var., ♀) with common carp (CC, Cyprinus carpio L., ♂). However, the genetic pattern of the heterogeneous genomes during gametogenesis in 4nAT is still unclear, which hinders the understanding of the mechanism of generation of new phenotypes during allopolyploidization in fish breeding. In the present study, fluorescence in situ hybridization of 5S rDNA was employed to track homologous pairing, and the characteristics of bivalents were observed using air-drying preparation technology and electron microscopy. The results showed two strong signals of 5S rDNA localization from the RCC genome, paired in the pachytene stage and metaphase stage of meiosis I cells in 4nAT, suggesting pairing of homologous chromosomes in 4nAT occurred between identical chromosomes. Furthermore, all bivalent pairs possessed one Hui Zhang and Yu Sun contributed equally to this work.

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Section: Resultssupporting

confidence: 84%

Localization of 5S rDNA analysis of homologous pairing in tetraploid hybrids of red crucian carp (♀) × common carp (♂)

Zhang

Sun

Zhu

et al. 2021

J World Aquaculture Soc

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“…One of the major challenges for triploids is their difficulty during meiosis, as the pairing and equal segregation of three homologous chromosomes is impossible ( Comai 2005 ). Chromosome pairing failure often results in meiotic arrest at pachytene–metaphase I, followed by apoptosis, or aneuploid gamete production ( Kuroda et al 2019 ; Zhang et al 2021 ). However, unisexual vertebrates develop unique mechanisms, such as oogonial fusion or premeiotic endoreplication in parthenogenetic lizards ( Aspidoscelis tesselata ) ( Lutes et al 2010 ) and Cobitis triploid females ( Dedukh et al 2020 ), as well as suppression of homolog synapsis and the first meiotic division in P. formosa ( Schultz 1979 ), to bypass these barriers in meiosis.…”

Section: Discussionmentioning

confidence: 99%

Changes in Ploidy Drive Reproduction Transition and Genomic Diversity in a Polyploid Fish Complex

Zhu

et al. 2022

Molecular Biology and Evolution

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Unisexual animals are commonly found in some polyploid species complexes, and most of these species have had a long evolutionary history. However, their method for avoiding genomic decay remains unclear. The polyploid Carassius complex naturally comprises the sexual amphidiploid C. auratus (crucian carp or goldfish) (AABB) and the gynogenetic amphitriploid C. gibelio (gibel carp) (AAABBB). Recently, we developed a fertile synthetic amphitetraploid (AAAABBBB) male from C. gibelio by incorporating a C. auratus genome. In this study, we generated novel amphitriploids (AAABBB) by backcrossing the amphitetraploid male with the amphidiploid C. auratus. Whole-genome resequencing revealed the genomic changes, including recombination and independent assortment between homologs of C. gibelio and C. auratus. The fertility, sex determination system, oocyte development, and fertilization behaviors of the novel amphitriploids were investigated. Approximately 80% of the novel amphitriploid females recovered the unisexual gynogenesis ability. Intriguingly, two types of primary oocyte (with and without homolog synapsis) were discovered, and their distinct development fates were observed. Type I oocytes entered apoptosis due to improper synaptonemal complex assembly and incomplete double-strand break repair, whereas subsequent type II oocytes bypassed meiosis through an alternative ameiotic pathway to develop into mature eggs. Moreover, gynogenesis was stabilized in their offspring, and a new array of diverse gynogenetic amphitriploid clones was produced. These revealed genomic changes and detailed cytological data provide comprehensive evidence that changes in ploidy drive unisexual and sexual reproduction transition, thereby resulting in genomic diversity and allowing C. gibelio avoid genomic decay.

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“…The spermatozoa of the 3nDTCC mostly activate triploid ova and do not participate in the genetic makeup of offspring ( Xiao et al, 2011 ). Furthermore, 3nDTCC possessed a complete spermatogenesis process to produce viable 1.5n sperm ( Zhang et al, 2021 ), and the breeding test of 3nDTCC (♀) ×3nDTCC (♂) showed that the 1.5n spermatozoa only activated the eggs, not involved in the genetic composition of the offspring or only inserted a few of the paternal DNA fragments, which were speculated by the progeny were triploid and all-female. Do the spermatozoa of 3nDTCC possess the complete structure as that in bisexual reproductive diploid fish?…”

Section: Discussionmentioning

confidence: 99%

“…The artificial breeding experiment showed that the male and female 3nDTCC were all fertile and produced triploid offspring when mating with each other ( Xiao et al, 2011 ). The recent research studies have showed that 3nDTCC males presented a relative regular meiotic prophase I with complete conjugate chromosome pairs and finally formed mature sperms ( Zhang et al, 2021 ). The 3nDTCC males are fertile and can produce spermatozoa with “normal morphology” and possess normal swimming ability, but the genetic material of them is rejected by gynogenetic progeny.…”

Section: Introductionmentioning

confidence: 99%

Structural Abnormalities of Spermatozoa in Triploid Gynogenetic Crucian Carp (Carassius auratus)

Sun

Qiang

et al. 2021

Front. Genet.

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The spermatozoa of triploid gynogenetic crucian carp (Carassius auratus) (3nDTCC) possess a spermatogenesis process with a normal genetic background. However, the genetic materials of these spermatozoa do not completely inherit gynogenetic progeny in general. Understanding the intrinsic mechanism may be helpful for developing breeding strategies of gynogenetic fishes. In this study, the spermatozoa ultrastructure was systematically studied in diploid red crucian carp and 3nDTCC to demonstrate their cytological structural differences. In addition, the artificial breeding tests of 3nDTCC(♀) with different ploidy spermatozoa were performed to verify the contributions of genetic materials from 3nDTCC spermatozoa to the gynogenesis progeny. Furthermore, the mRNA expression of centriole-related genes (i.e., cep57, cetn1, rootletin, and nek2) involved in spermatozoa packaging was also determined by quantitative real-time PCR (qPCR) to illustrate the molecular expression characteristics of the spermatozoa packaging process in 3nDTCC. The results reveal the adaptive features of spermatozoa in 3nDTCC, including the loose midpiece structure, abnormal head structure, and abnormal expression of centriole-related genes, which may influence the motility of spermatozoa and make it not involved normally in the genetic composition of the gynogenesis offspring.

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Abnormal meiosis in fertile and sterile triploid cyprinid fish

Cited by 20 publications

References 21 publications

Localization of 5S rDNA analysis of homologous pairing in tetraploid hybrids of red crucian carp (♀) × common carp (♂)

Localization of 5S rDNA analysis of homologous pairing in tetraploid hybrids of red crucian carp (♀) × common carp (♂)

Changes in Ploidy Drive Reproduction Transition and Genomic Diversity in a Polyploid Fish Complex

Structural Abnormalities of Spermatozoa in Triploid Gynogenetic Crucian Carp (Carassius auratus)

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