Ribosomal Intergenic Spacers Are Filled with Transposon Remnants

Overview

Journal Genome Biol Evol

Publisher Oxford University Press

Specialties Biology
Genetics
Molecular Biology

Date 2023 Jun 21

PMID 37341531

Authors

Arnold J Bendich

Scott O Rogers

Affiliations

Soon will be listed here.

Abstract

Eukaryotic ribosomal DNA (rDNA) comprises tandem units of highly conserved coding genes separated by rapidly evolving spacer DNA. The spacers of all 12 species examined were filled with short direct repeats (DRs) and multiple long tandem repeats (TRs), completing the rDNA maps that previously contained unannotated and inadequately studied sequences. The external transcribed spacers also were filled with DRs and some contained TRs. We infer that the spacers arose from transposon insertion, followed by their imprecise excision, leaving short DRs characteristic of transposon visitation. The spacers provided a favored location for transposon insertion because they occupy loci containing hundreds to thousands of gene repeats. The spacers' primary cellular function may be to link one ribosomal RNA transcription unit to the next, whereas transposons flourish here because they have colonized the most frequently used part of the genome.

Citing Articles

Direct repeats found in the vicinity of intron splice sites.

Rogers S, Bendich A Naturwissenschaften. 2025; 112(1):14.

PMID: 39883174 PMC: 11782384. DOI: 10.1007/s00114-025-01966-4.

Stress-Induced Evolution of the Nucleolus: The Role of Ribosomal Intergenic Spacer (rIGS) Transcripts.

Gavrilova A, Neklesova M, Zagryadskaya Y, Kuznetsova I, Turoverov K, Fonin A Biomolecules. 2024; 14(10).

PMID: 39456266 PMC: 11505599. DOI: 10.3390/biom14101333.

Structure and Evolution of Ribosomal Genes of Insect Chromosomes.

Gokhman V, Kuznetsova V Insects. 2024; 15(8).

PMID: 39194798 PMC: 11354594. DOI: 10.3390/insects15080593.

Origin and maintenance of large ribosomal RNA gene repeat size in mammals.

Macdonald E, Whibley A, Waters P, Patel H, Edwards R, Ganley A Genetics. 2024; 228(1).

PMID: 39044674 PMC: 11373518. DOI: 10.1093/genetics/iyae121.

The Dynamic Interplay Between Ribosomal DNA and Transposable Elements: A Perspective From Genomics and Cytogenetics.

Garcia S, Kovarik A, Maiwald S, Mann L, Schmidt N, Pascual-Diaz J Mol Biol Evol. 2024; 41(3).

PMID: 38306580 PMC: 10946416. DOI: 10.1093/molbev/msae025.

References

Ingle J, Timmis J, Sinclair J . The Relationship between Satellite Deoxyribonucleic Acid, Ribosomal Ribonucleic Acid Gene Redundancy, and Genome Size in Plants. Plant Physiol. 1975; 55(3):496-501. PMC: 541645. DOI: 10.1104/pp.55.3.496. View

Fleurier S, Dapa T, Tenaillon O, Condon C, Matic I . rRNA operon multiplicity as a bacterial genome stability insurance policy. Nucleic Acids Res. 2022; 50(22):12601-12620. PMC: 9825170. DOI: 10.1093/nar/gkac332. View

Rogers S, Bendich A . Ribosomal RNA genes in plants: variability in copy number and in the intergenic spacer. Plant Mol Biol. 2013; 9(5):509-20. DOI: 10.1007/BF00015882. View

Saini N, Gordenin D . Hypermutation in single-stranded DNA. DNA Repair (Amst). 2020; 91-92:102868. PMC: 7234795. DOI: 10.1016/j.dnarep.2020.102868. View

Bendich A, McCarthy B . Ribosomal RNA homologies among distantly related organisms. Proc Natl Acad Sci U S A. 1970; 65(2):349-56. PMC: 282909. DOI: 10.1073/pnas.65.2.349. View

Havlova K, Dvorackova M, Peiro R, Abia D, Mozgova I, Vansacova L . Variation of 45S rDNA intergenic spacers in Arabidopsis thaliana. Plant Mol Biol. 2016; 92(4-5):457-471. DOI: 10.1007/s11103-016-0524-1. View

Casacuberta E . Drosophila: Retrotransposons Making up Telomeres. Viruses. 2017; 9(7). PMC: 5537684. DOI: 10.3390/v9070192. View

Berger S, Schweiger H . Ribosomal DNA in different members of a family of green algae (Chlorophyta, Dasycladaceae): an electron microscopisal study. Planta. 2014; 127(1):49-62. DOI: 10.1007/BF00388862. View

Thakur J, Packiaraj J, Henikoff S . Sequence, Chromatin and Evolution of Satellite DNA. Int J Mol Sci. 2021; 22(9). PMC: 8122249. DOI: 10.3390/ijms22094309. View

10.

Agrawal S, Ganley A . The conservation landscape of the human ribosomal RNA gene repeats. PLoS One. 2018; 13(12):e0207531. PMC: 6281188. DOI: 10.1371/journal.pone.0207531. View

11.

Abraham K, Khosraviani N, Chan J, Gorthi A, Samman A, Zhao D . Nucleolar RNA polymerase II drives ribosome biogenesis. Nature. 2020; 585(7824):298-302. PMC: 7486236. DOI: 10.1038/s41586-020-2497-0. View

12.

Kobayashi T, Horiuchi T, Tongaonkar P, Vu L, Nomura M . SIR2 regulates recombination between different rDNA repeats, but not recombination within individual rRNA genes in yeast. Cell. 2004; 117(4):441-53. DOI: 10.1016/s0092-8674(04)00414-3. View

13.

Kirchberger P, Schmidt M, Ochman H . The Ingenuity of Bacterial Genomes. Annu Rev Microbiol. 2020; 74:815-834. DOI: 10.1146/annurev-micro-020518-115822. View

14.

Garcia S, Panero J, Siroky J, Kovarik A . Repeated reunions and splits feature the highly dynamic evolution of 5S and 35S ribosomal RNA genes (rDNA) in the Asteraceae family. BMC Plant Biol. 2010; 10:176. PMC: 3095306. DOI: 10.1186/1471-2229-10-176. View

15.

Hori Y, Engel C, Kobayashi T . Regulation of ribosomal RNA gene copy number, transcription and nucleolus organization in eukaryotes. Nat Rev Mol Cell Biol. 2023; 24(6):414-429. DOI: 10.1038/s41580-022-00573-9. View

16.

Eickbush D, Eickbush T . Vertical transmission of the retrotransposable elements R1 and R2 during the evolution of the Drosophila melanogaster species subgroup. Genetics. 1995; 139(2):671-84. PMC: 1206373. DOI: 10.1093/genetics/139.2.671. View

17.

Gao L, Altae-Tran H, Bohning F, Makarova K, Segel M, Schmid-Burgk J . Diverse enzymatic activities mediate antiviral immunity in prokaryotes. Science. 2020; 369(6507):1077-1084. PMC: 7985843. DOI: 10.1126/science.aba0372. View

18.

Osia B, Twarowski J, Jackson T, Lobachev K, Liu L, Malkova A . Migrating bubble synthesis promotes mutagenesis through lesions in its template. Nucleic Acids Res. 2022; 50(12):6870-6889. PMC: 9262586. DOI: 10.1093/nar/gkac520. View

19.

Burton R, Metz E, Flowers J, Willett C . Unusual structure of ribosomal DNA in the copepod Tigriopus californicus: intergenic spacer sequences lack internal subrepeats. Gene. 2005; 344:105-13. DOI: 10.1016/j.gene.2004.09.001. View

20.

Kasselimi E, Pefani D, Taraviras S, Lygerou Z . Ribosomal DNA and the nucleolus at the heart of aging. Trends Biochem Sci. 2022; 47(4):328-341. DOI: 10.1016/j.tibs.2021.12.007. View