Measuring and interpreting transposable element expression

Lanciano, Sophie; Cristofari, Gaël

doi:10.1038/s41576-020-0251-y

Cited by 250 publications

(283 citation statements)

References 220 publications

(267 reference statements)

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“…The estimation of the transcript levels derived from different TE genomic copies remains partially biased with such transcriptomic analyses. In particular, single-mapping will retain more reads on older sequences that have accumulated more SNPs than younger elements [41]. To precisely evaluate the global impact of the Nup84 complex on distinct copies of Ty1, we used integrated Ty1- lacZ fusions previously designed to study the transcription of individual Ty1 copies at their genomic location [55].…”

Section: Resultsmentioning

confidence: 99%

“…RNA polymerase III-transcribed genes [39,40]). In line with the difficulties associated with the analysis of repetitive sequences [41], little is known about the influence of NPCs on the RNA polymerase II (RNAP II)-dependent transcription of transposable elements (TEs). TEs are ubiquitous in eukaryotes and represent a significant fraction of their genomes (reviewed in [42]).…”

Section: Introductionmentioning

confidence: 99%

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A nuclear pore sub-complex restricts the propagation of Ty retrotransposons by limiting their transcription

Bonnet

Chaput

Palancade

et al. 2021

Preprint

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Beyond their canonical function in nucleocytoplasmic exchanges, nuclear pore complexes (NPCs) regulate the expression of protein-coding genes. Here, we have implemented transcriptomic and molecular methods to specifically address the impact of the NPC on retroelements, which are present in multiple copies in genomes. We report a novel function for the Nup84 complex, a core NPC building block, in specifically restricting the transcription of LTR-retrotransposons in yeast. Nup84 complex-dependent repression impacts both Copia and Gypsy Ty LTR-retrotransposons, all over the S. cerevisiae genome. Mechanistically, the Nup84 complex restricts the transcription of Ty1, the most active yeast retrotransposon, through the tethering of the SUMO-deconjugating enzyme Ulp1 to NPCs. Strikingly, the modest accumulation of Ty1 RNAs caused by Nup84 complex loss-of-function is sufficient to trigger an important increase of Ty1 cDNA levels, resulting in massive Ty1 retrotransposition. Altogether, our studies expand our understanding of the complex interactions between retrotransposons and the NPC, and highlight the importance for the cells to keep retrotransposon under tight transcriptional control.AUTHOR SUMMARYRetroelements, which replicate by reverse transcription of their RNA into a cDNA that is integrated into the host genetic material, play an important role in the plasticity of eukaryotic genomes. The study of yeast retrotransposons has led to the identification of host factors that limit retroelement mobility, including components of the nuclear pore complex (NPC), most of them still awaiting mechanistic characterization. Here, we investigated the contribution of the Nup84 complex, a core NPC scaffold, to retrotransposon biology in budding yeast. Our findings uncover that the Nup84 complex restricts the transcription of phylogenetically-distinct Ty retroelements. By focusing on Ty1 retrotransposons, we provide evidence that repression by the Nup84 complex depends on the maintenance at the NPC of the SUMO-protease Ulp1, an essential enzyme of the SUMO pathway with multiple targets in the transcription machinery. We finally show that this transcriptional control is critical for genome dynamics, since a small increase in the accumulation of Ty1 RNAs leads to massive retrotransposition. Our data reveal that although relatively abundant, Ty transcripts are limiting for retrotransposition, underscoring the importance of a tight control of their expression. They also characterize a new non-canonical function of NPCs, confirming their connection with genome expression and stability.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

A nuclear pore sub-complex restricts the propagation of Ty retrotransposons by limiting their transcription

Bonnet

Chaput

Palancade

et al. 2021

Preprint

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“…However, it is unclear how chimeric transcripts from these loci contribute to the overall pool of transposon mRNAs in somatic cells. Reliable measurement of autonomous-and non-autonomous transposon expression in somatic tissue, is hampered by repetitive sequences being difficult to map and germline transposons being polymorphic (Lanciano and Cristofari, 2020). Hence, many somatic transposon expression studies have analyzed single transposon families or have used bulk sequencing of tissues or cultured Cold Spring Harbor Laboratory Press on October 30, 2020 -Published by genome.cshlp.org Downloaded from 4 cells (Babaian et al, 2019;Chung et al, 2019;Faulkner et al, 2009;Li et al, 2013;Philippe et al, 2016;Pinson et al, 2018;Rangwala et al, 2009;Wang et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

Transposon expression in the Drosophila brain is driven by neighboring genes and diversifies the neural transcriptome

Treiber

Waddell

2020

Genome Res.

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Somatic transposon expression in neural tissue is commonly considered as a measure of mobilization and has therefore been linked to neuropathology and organismal individuality. We combined genome sequencing data with single-cell mRNA sequencing of the same, inbred fly strain to map transposon expression in the Drosophila midbrain and found that transposon expression patterns are highly stereotyped. Every detected transposon is resident in at least one cellular gene with a matching expression pattern. Bulk RNA sequencing from fly heads of the same strain revealed that coexpression is a physical link in the form of abundant chimeric transposon-gene mRNAs. We identified 264 genes where transposons introduce cryptic splice sites into the nascent transcript and thereby significantly expand the neural transcript repertoire. Some genes exclusively produce chimeric mRNAs with transposon sequence and on average 11.6% of the mRNAs produced from a given gene are chimeric. Conversely, most transposon-containing transcripts are chimeric, which suggests that somatic expression of these transposons is largely driven by cellular genes. We propose that chimeric mRNAs produced by alternative splicing into polymorphic transposons, rather than transposon mobilization, may contribute to functional differences between individual cells and animals.

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“…For both 93-11 and Nip genomes, majority over 95% reads were mapped in gene coding regions, while few reads less than 0.5% were mapped in LTR/TE regions (Table 1). Further indicating the low transcription activities of LTR/TEs in rice species (33). Figure 6).…”

Section: Rice Ltr/te Transcription Activitiesmentioning

confidence: 92%

Comparative Evolution and Transcription Activity of Transposable Elements in Indica and Japonica Rice

Wang

et al. 2020

Preprint

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BackgroundTransposable elements (TEs) are able to diversify plant gene expression and function, sequentially promote plant variety and evolution. However, there is lack of efficient approach to investigate the evolution behavior and transcription activity of TEs in plants. Here we developed a pipeline Matrix-TE to comprehensively evaluate the super-families, differentiation and transcription activity of LTR/TEs in Indica and Japonica rice, the two considerable important and closely related monocots.ResultsSix LTR/TE super-families were identified by Matrix-TE in both Indica and Japonica rice genomes, in which the OS-type1 and OS-type2 super-families were unclassified. Indica rice specific TE peak P-Gypsy and Japonica rice specific TE peak P-Copia were observed separately. Then the two peaks were analyzed by Gaussian Probability Density Function (GPDF) fit. Significant TE transcription activities were observed in Indica and Japonica rice plants after stress treatments. Particularly, hot, cold and salt stresses induced the high expression level of LTR/TEs in rice plants.ConclusionsWe developed the approach Matrix-TE on the basis of BLASTN and GPDF algorithms, and applied it to comprehensively and quantitatively investigate LTR/TE types and contents in the close subspecies Indica and Japonica rice genomes. The individual TE burst events P-Copia and P-Gypsy were observed in Japonica and Indica rice, separately. RNA-seq and RT-PCR methods indicated that LTR/TE transcripts were induced by hot, cold and high salt stress conditions. The optimized Matrix-TE approach and procedures probably could be used in other plant species with big genomes like wheat and maize.

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Measuring and interpreting transposable element expression

Cited by 250 publications

References 220 publications

A nuclear pore sub-complex restricts the propagation of Ty retrotransposons by limiting their transcription

A nuclear pore sub-complex restricts the propagation of Ty retrotransposons by limiting their transcription

Transposon expression in the Drosophila brain is driven by neighboring genes and diversifies the neural transcriptome

Comparative Evolution and Transcription Activity of Transposable Elements in Indica and Japonica Rice

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