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

Although both are salient features of genomes, at first glance ribosomal DNAs and transposable elements are genetic elements with not much in common: whereas ribosomal DNAs are mainly viewed as housekeeping genes that uphold all prime genome functions, transposable elements are generally portrayed as selfish and disruptive. These opposing characteristics are also mirrored in other attributes: organization in tandem (ribosomal DNAs) versus organization in a dispersed manner (transposable elements); evolution in a concerted manner (ribosomal DNAs) versus evolution by diversification (transposable elements); and activity that prolongs genomic stability (ribosomal DNAs) versus activity that shortens it (transposable elements). Re-visiting relevant instances in which ribosomal DNA–transposable element interactions have been reported, we note that both repeat types share at least four structural and functional hallmarks: (1) they are repetitive DNAs that shape genomes in evolutionary timescales, (2) they exchange structural motifs and can enter co-evolution processes, (3) they are tightly controlled genomic stress sensors playing key roles in senescence/aging, and (4) they share common epigenetic marks such as DNA methylation and histone modification. Here, we give an overview of the structural, functional, and evolutionary characteristics of both ribosomal DNAs and transposable elements, discuss their roles and interactions, and highlight trends and future directions as we move forward in understanding ribosomal DNA–transposable element associations.

This research was supported by the Agencia Estatal de Investigación, Government of Spain (PID2020-119163GB-I00 and PRE2021-097873, granted to S.G. and J.P.P.D., respectively, all funded by MCIN/AEI/10.13039/501100011033). T.H. receives grants from the Bundesministerium für Bildung und Forschung (BMBF) for the EpicBeet project (FKZ 031B1221A) and the German Research Foundation (DFG) for the project 433081887/HE7194/2-1. S.M. is funded by a Back-to-Research Grant financed by the Ministry of Research, Culture and Tourism of the Free State of Saxony (SMWK). Interactions between the Dresden, Graz, and Barcelona labs are enabled by an EMBO short-term fellowship (Ref. 8989) and a Dresden Senior Fellowship to S.G. The research of A.K. is supported by the Czech Science Foundation (grant no. 22-16826S)

Ribosomal DNAs and Transposable Elements: Two Opposing Faces of Repetitive DNAs Ribosomal DNAs: Conserved and Heavily Transcribed, These Housekeepers Are In Charge of Cell Maintenance TEs: Hyperdiverse and Mostly Repressed, These Evolutionary Drivers Bring Genomic Novelty rDNA and TEs: Bridging the Differences and Coming Together? Methods to Detect rDNA, TEs, and Their Associations TEs in Ribosomal DNA Are rDNAs TE Insertion Hotspots? Do TE Insertions in rDNA Simply Occupy a Niche for Their Own Profit or May They Even Be Beneficial to the Host? Ribosomal DNA in TEs Future Perspectives What to Expect From Current and Next Technical Advancements Biological Roles and Consequences of the rDNA–TE Interplay Conclusion Acknowledgments Data Availability References