Meiotic Chromosome Dynamics in Zebrafish

Imai, Yukiko; Olaya, Ivan; Sakai, Noriyoshi; Burgess, Sean M.

doi:10.3389/fcell.2021.757445

Cited by 13 publications

(16 citation statements)

References 178 publications

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“…Cluster #2 includes genes that are specifically enriched in Symbrk and Nuc stages. Functionally enriched terms in this cluster included meiotic processes such as homologous recombination and mismatch repair ( Figure 2B ), consistent with the included leptotene-pachytene prophase oocytes in this sample, when DNA double-strand breaks are repaired through homologous recombination, as well as nonhomologous repair mechanisms ( Imai et al, 2021 ). Interestingly, enriched terms also included RNA transport and translation ( Figure 2B ), which are consistent with oocyte symmetry breaking and polarization of localized mRNA through Bb formation at these stages.…”

Section: Resultssupporting

confidence: 73%

Stage Specific Transcriptomic Analysis and Database for Zebrafish Oogenesis

Bogoch

Jamieson-Lucy

Vejnar

et al. 2022

Front. Cell Dev. Biol.

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Oogenesis produces functional eggs and is essential for fertility, embryonic development, and reproduction. The zebrafish ovary is an excellent model to study oogenesis in vertebrates, and recent studies have identified multiple regulators in oocyte development through forward genetic screens, as well as reverse genetics by CRISPR mutagenesis. However, many developmental steps in oogenesis, in zebrafish and other species, remain poorly understood, and their underlying mechanisms are unknown. Here, we take a genomic approach to systematically uncover biological activities throughout oogenesis. We performed transcriptomic analysis on five stages of oogenesis, from the onset of oocyte differentiation through Stage III, which precedes oocyte maturation. These transcriptomes revealed thousands of differentially expressed genes across stages of oogenesis. We analyzed trends of gene expression dynamics along oogenesis, as well as their expression in pair-wise comparisons between stages. We determined their functionally enriched terms, identifying uniquely characteristic biological activities in each stage. These data identified two prominent developmental phases in oocyte differentiation and traced the accumulation of maternally deposited embryonic regulator transcripts in the developing oocyte. Our analysis provides the first molecular description for oogenesis in zebrafish, which we deposit online as a resource for the community. Further, the presence of multiple gene paralogs in zebrafish, and the exclusive curation by many bioinformatic tools of the single paralogs present in humans, challenge zebrafish genomic analyses. We offer an approach for converting zebrafish gene name nomenclature to the human nomenclature for supporting genomic analyses generally in zebrafish. Altogether, our work provides a valuable resource as a first step to uncover oogenesis mechanisms and candidate regulators and track accumulating transcripts of maternal regulators of embryonic development.

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Section: Resultssupporting

confidence: 73%

Stage Specific Transcriptomic Analysis and Database for Zebrafish Oogenesis

Bogoch

Jamieson-Lucy

Vejnar

et al. 2022

Front. Cell Dev. Biol.

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“…This was coupled with the formation of DSBs (Zickler and Kleckner, 2015). In our target reptiles, chromosome axes were detected as short stretches of SYCP3 and SYCP1 signal adjacent to the telomes, mirroring the patterns previously described in zebrafish (Blokhina et al, 2019;Imai et al, 2021). Moreover, telomeres clustered to one side of the nucleus forming the bouquet, presumably promoting homologous pairing and synapsis.…”

Section: Meiosis Progression Is Highly Conserved In Reptilessupporting

confidence: 78%

“…It is not until pachytene that chromosomes are completely synapsed and COs are resolved as chiasmata (the points where genetic material is actually exchanged). The mechanisms underlying meiotic progression have been extensively studied in several model organisms, including yeast, fruit flies, nematodes, mice and zebrafish ( Zickler and Kleckner, 2015 ; Blokhina et al, 2019 ; Imai et al, 2021 ). However, our understanding of the dynamics of meiotic prophase I and recombination among non-mammalian amniote vertebrates (i.e., sauropsids–birds/reptiles) remains incomplete ( Segura et al, 2013 ; Marín-Gual et al, 2022 ).…”

Section: Introductionmentioning

confidence: 99%

Meiotic chromosome dynamics and double strand break formation in reptiles

Marín-Gual

González-Rodelas

Garcias

et al. 2022

Front. Cell Dev. Biol.

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During meiotic prophase I, tightly regulated processes take place, from pairing and synapsis of homologous chromosomes to recombination, which are essential for the generation of genetically variable haploid gametes. These processes have canonical meiotic features conserved across different phylogenetic groups. However, the dynamics of meiotic prophase I in non-mammalian vertebrates are poorly known. Here, we compare four species from Sauropsida to understand the regulation of meiotic prophase I in reptiles: the Australian central bearded dragon (Pogona vitticeps), two geckos (Paroedura picta and Coleonyx variegatus) and the painted turtle (Chrysemys picta). We first performed a histological characterization of the spermatogenesis process in both the bearded dragon and the painted turtle. We then analyzed prophase I dynamics, including chromosome pairing, synapsis and the formation of double strand breaks (DSBs). We show that meiosis progression is highly conserved in reptiles with telomeres clustering forming the bouquet, which we propose promotes homologous pairing and synapsis, along with facilitating the early pairing of micro-chromosomes during prophase I (i.e., early zygotene). Moreover, we detected low levels of meiotic DSB formation in all taxa. Our results provide new insights into reptile meiosis.

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“…In this section, the different subtypes of SPC during meiosis I were staged according to the previous article (Imai et al, 2021). Sycp3 was found with unique expression pattern in different subtypes of SPC-I.…”

Section: Resultsmentioning

confidence: 99%

“…However, the dynamic expression pattern of Pcna during meiosis is still missing. In this study, we carefully characterized the expression dynamic of Pcna during meiosis I in zebrafish, and found that Pcna was polarly localized in the nucleus of leptotene SPC-I just underneath the Sycp3, suggesting a potential role of Pcna during the initiation of meiotic recombination when Sycp3 was shown adjacent to the telomeres (Imai et al, 2021). During the leptotene stage, telomeres moved to one pole of the nucleus where Sycp3 aggregated and the accumulated (Saito et al, 2014).…”

Section: Discussionmentioning

confidence: 99%

Assessment of fish spermatogenesis through high-quality immunofluorescence against fish testicular samples with an antibody set

Liu

et al. 2022

Preprint

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A complete evaluation of the spermatogenetic status of a fish by accurately identifying different types of spermatogenic cells is useful not only for reproductive studies but also for genetic breeding. For this task, it is required to establish a simple and practical experimental procedure, to obtain repeatable, high-quality imaging data. Here, we have developed antibodies against the zebrafish (Danio rerio) spermatogenesis-related proteins, including Ddx4, Piwil1, Sycp3, and Pcna, and an integrated method for high-quality and high-through output immunofluorescence on testis sections of different fish species. We accurately identified different spermatogenic cells at different stages. Type-A spermatogonia can be identified by the highest expression of Ddx4 and Piwil1 among different spermatogenic cells. Type-B spermatogonia is identified by the second highest expression of Ddx4 and the highest expression of Pcna among different spermatogenic cells. Spermatids can be distinguished from spermatozoa by the expression of Piwil1. The different subtypes of primary spermatocytes (SPC-I) can be identified by co-staining of Sycp3 and Pcna. Leptotene SPC-I show polar expression of both Sycp3 and Pcna at the same side of the nucleus. All the antibodies were tested for practicality in four fish species, Chinese rare minnow (Gobiocypris rarus), common carp (Cyprinus carpio), blunt snout bream (Megalobrama amblycephala), and rice field eel (Monopterus albus). Using this method and the antibody sets, we were able to precisely and accurately evaluate the spermatogenetic status in different fish species.

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Meiotic Chromosome Dynamics in Zebrafish

Cited by 13 publications

References 178 publications

Stage Specific Transcriptomic Analysis and Database for Zebrafish Oogenesis

Stage Specific Transcriptomic Analysis and Database for Zebrafish Oogenesis

Meiotic chromosome dynamics and double strand break formation in reptiles

Assessment of fish spermatogenesis through high-quality immunofluorescence against fish testicular samples with an antibody set

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