On some structural and evolutionary aspects of rDNA amplification in oogenesis of Trachemys scripta turtles

Davidian, Asya; Koshel, Elena I.; Dyomin, Alexander; Galkina, Svetlana; Saifitdinova, Alsu; Gaginskaya, Elena

doi:10.1007/s00441-020-03282-x

Cited by 9 publications

(12 citation statements)

References 84 publications

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“…In turtles, the rDNA amplification and formation of extrachromosomal nucleoli during oogenesis are well characterized ( Callebaut et al 1997 ; Davidian et al 2021 ). Figure 7 A shows the content of the oocyte nucleus (germinal vesicle, GV) manually dissected from T. scripta oocyte with a diameter of ∼2 mm.…”

Section: Resultsmentioning

confidence: 99%

“…The ability to amplify the NOR rDNA to create extrachromosomal rDNA copies forming amplified nucleoli is a feature of oocytes in many animals with the so-called hypertranscriptional oogenesis ( Dondua 2018 ). Among vertebrates, the phenomenon of ribosomal gene amplification during oogenesis is found in fish ( Vincent et al 1969 ; Raikova 1976 ; Thiry and Poncin 2005 ; Locati, Pagano, Ensink, et al 2017 ; Locati, Pagano, Girard, et al 2017 ), amphibians ( Brown and Dawid 1968 ; Gall 1968 ; Macgregor 1968 , 1972 , 1982 ; Gall and Pardue 1969 ; Ficq and Brachet 1971 ; Gall et al 2004 ), and some reptiles ( Macgregor 1982 ; Guraya 1989 ; Callebaut et al 1997 ; Uribe and Guillette 2000 ; Moore et al 2008 ; Pérez-Bermúdez et al 2012 ; Davidian et al 2021 ). The strategy of amplified nucleoli provides early embryos with a sufficient number of ribosomes and thereby supports the protein synthesis until the zygotic transcription is activated ( Davidson 1986 ; Tafuri and Wolffe 1993 ).…”

Section: Introductionmentioning

confidence: 99%

“…There are only a few data available on chromosomal localization and copy number of 5S rRNA genes in reptile genomes ( Sochorová et al 2018 ; Cavalcante et al 2020 ). The existing evidence of distinctive rDNA amplification strategy in turtle oogenesis ( Macgregor 1982 ; Davidian et al 2021 ) prompted us to study the molecular and evolutionary mechanisms underlying the phenomenon of rRNA gene amplification in oocytes of these animals in more detail.…”

Section: Introductionmentioning

confidence: 99%

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45S rDNA Repeats of Turtles and Crocodiles Harbor a Functional 5S rRNA Gene Specifically Expressed in Oocytes

Davidian

Dyomin

Galkina

et al. 2021

Molecular Biology and Evolution

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In most eukaryotic genomes, tandemly repeated copies of 5S rRNA genes are clustered outside the nucleolus organizer region (NOR), which normally encodes three other major rRNAs: 18S, 5.8S, and 28S. Our analysis of turtle rDNA sequences has revealed a 5S rDNA insertion into the NOR intergenic spacer in antisense orientation. The insertion (hereafter called NOR-5S rRNA gene) has a length of 119 bp and coexists with the canonical 5S rDNA clusters outside the NOR. Despite the ∼20% nucleotide difference between the two 5S gene sequences, their internal control regions for RNA polymerase III are similar. Using the turtle Trachemys scripta as a model species, we showed the NOR-5S rDNA specific expression in oocytes. This expression is concurrent with the NOR rDNA amplification during oocyte growth. We show that in vitellogenic oocytes, the NOR-5S rRNA prevails over the canonical 5S rRNA in the ribosomes, suggesting a role of modified ribosomes in oocyte-specific translation. The orders Testudines and Crocodilia seem to be the only taxa of vertebrates with such a peculiar rDNA organization. We speculate that the amplification of the 5S rRNA genes as a part of the NOR DNA during oogenesis provides a dosage balance between transcription of all the four ribosomal RNAs while producing a maternal pool of extra ribosomes. We further hypothesize that the NOR-5S rDNA insertion appeared in the Archelosauria clade during the Permian period and was lost later in the ancestors of Aves.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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45S rDNA Repeats of Turtles and Crocodiles Harbor a Functional 5S rRNA Gene Specifically Expressed in Oocytes

Davidian

Dyomin

Galkina

et al. 2021

Molecular Biology and Evolution

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“…Subsequent experiments using equilibrium density gradient centrifugation in CsCl and comparative hybridization between germinal vesicle and somatic cell DNA definitively showed that the oocytes of Sedum mexicanum and Necturus maculosus contained extra-chromosomal copies of rDNA. Others went on to show that extra-chromosomal rDNA can be found in the oocytes produced by a variety of organisms ( Gall, 1968 , 1969 ; Gall et al, 1969 ; Macgregor, 1972 ; Gall and Rochaix, 1974 ; Davidian et al, 2021 ). Despite their occurrence across several vertebrate species, prevailing evidence indicates that placental mammals do not amplify rDNA within their oocytes using this mechanism ( Bachvarova, 1985 ; Tian et al, 2001 ).…”

Section: Regulation Of Translation Machinery During Germ Cell Developmentmentioning

confidence: 99%

“…Knowledge regarding the formation of extra-chromosomal nucleoli comes mostly from the study of amphibian oocytes. A recent paper by Davidian et al (2021) provides a thoughtful description of the current state of the field. Briefly, the extra synthesis of rDNA begins at the pachytene stage of meiotic prophase, through a gene amplification process.…”

Section: Regulation Of Translation Machinery During Germ Cell Developmentmentioning

confidence: 99%

The Dynamic Regulation of mRNA Translation and Ribosome Biogenesis During Germ Cell Development and Reproductive Aging

Mercer

Jang

et al. 2021

Front. Cell Dev. Biol.

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The regulation of mRNA translation, both globally and at the level of individual transcripts, plays a central role in the development and function of germ cells across species. Genetic studies using flies, worms, zebrafish and mice have highlighted the importance of specific RNA binding proteins in driving various aspects of germ cell formation and function. Many of these mRNA binding proteins, including Pumilio, Nanos, Vasa and Dazl have been conserved through evolution, specifically mark germ cells, and carry out similar functions across species. These proteins typically influence mRNA translation by binding to specific elements within the 3′ untranslated region (UTR) of target messages. Emerging evidence indicates that the global regulation of mRNA translation also plays an important role in germ cell development. For example, ribosome biogenesis is often regulated in a stage specific manner during gametogenesis. Moreover, oocytes need to produce and store a sufficient number of ribosomes to support the development of the early embryo until the initiation of zygotic transcription. Accumulating evidence indicates that disruption of mRNA translation regulatory mechanisms likely contributes to infertility and reproductive aging in humans. These findings highlight the importance of gaining further insights into the mechanisms that control mRNA translation within germ cells. Future work in this area will likely have important impacts beyond germ cell biology.

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First discovered, long out of sight, finally visible: ribosomal DNA

2022

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On some structural and evolutionary aspects of rDNA amplification in oogenesis of Trachemys scripta turtles

Cited by 9 publications

References 84 publications

45S rDNA Repeats of Turtles and Crocodiles Harbor a Functional 5S rRNA Gene Specifically Expressed in Oocytes

45S rDNA Repeats of Turtles and Crocodiles Harbor a Functional 5S rRNA Gene Specifically Expressed in Oocytes

The Dynamic Regulation of mRNA Translation and Ribosome Biogenesis During Germ Cell Development and Reproductive Aging

First discovered, long out of sight, finally visible: ribosomal DNA

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