Long-read direct RNA sequencing reveals epigenetic regulation of chimeric gene-transposon transcripts in <i>Arabidopsis thaliana</i>

Berthelier, Jérémy; Furci, Leonardo; Asai, Shuji; Sadykova, Munissa; Shimazaki, Tomoe; Shirasu, Ken; Saze, Hidetoshi

doi:10.1101/2022.09.21.507229

Cited by 6 publications

(11 citation statements)

References 123 publications

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“…The ONT data further allowed us to unambiguously discriminate between read-out transcription and the indirect upregulation of genes via the cis-regulatory effect mediated by the recruitment of the transcription machinery to the TE (Zhao et al 2018;Fagny et al 2020;Deneweth et al 2022). The formation of TE-gene fusion transcripts is a common phenomenon in Arabidopsis (Lockton and Gaut 2009;Berthelier et al 2023) and we indeed detected read-out transcription originating from the 3` LTRs of both ONSEN and Copia-35 TE families under heatstress. However, our data suggests that the cis-regulatory effect is the main driver of TE-mediated expression of the flanking genes.…”

Section: Both Onsen and Copia-35 Confer Heat Responsiveness To Their ...mentioning

confidence: 63%

Natural diversity of heat-induced transcription of retrotransposons inArabidopsis thaliana

Xu,

Thieme,

Roulin

2024

Preprint

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Transposable elements (TEs) are major components of plant genomes, profoundly impacting the fitness of their hosts. However, technical bottlenecks have long hindered our mechanistic understanding of TEs. Using RNA-Seq and long-read sequencing with Oxford Nanopore Technologies direct cDNA sequencing, we analyzed the heat-induced transcription of TEs in three natural accessions of Arabidopsis thaliana (Cvi-0, Col-0, and Ler-1). In addition to the well-studied ONSEN retrotransposon family, we identified Copia-35 as a second heat-responsive retrotransposon family with particularly high activity in the relict accession Cvi-0. Our analysis revealed distinct expression patterns of individual TE copies and suggest different mechanisms regulating the GAG protein production in the ONSEN versus Copia-35 families. In addition, analogously to ONSEN, Copia-35 activation led to the upregulation of flanking genes such as AMUP9 and potentially to the quantitative modulation of flowering time. Unexpectedly, our results indicate that for both families, the upregulation of flanking genes is not directly initiated by transcription from their 3 LTRs. These findings highlight the inter- and intraspecific expressional diversity linked to retrotransposon activation under stress, providing insights into their potential roles in plant adaptation and evolution at elevated temperatures.

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Section: Both Onsen and Copia-35 Confer Heat Responsiveness To Their ...mentioning

confidence: 63%

Natural diversity of heat-induced transcription of retrotransposons inArabidopsis thaliana

Xu,

Thieme,

Roulin

2024

Preprint

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“…Experimental loss of heterochromatin modifications, including DNA methylation, can affect the expression of TE-containing genes (Saze et al 2013; Berthelier et al 2023). However, whether HS-induced reactivation of ONSEN is associated with its hypomethylation is still unclear (Tittel-Elmer et al 2010; Sun et al 2020), likely due to the difficulty to investigate DNA methylation of such repetitive sequences.…”

Section: Resultsmentioning

confidence: 99%

“…Experimental loss of heterochromatin modifications, including DNA methylation, can affect the expression of TE-containing genes (Saze et al 2013;Berthelier et al 2023).…”

Section: Flowering Locus T (Ft) Suppressor Of Overexpression Of Constansmentioning

confidence: 99%

Retrotransposon-driven environmental regulation ofFLCleads to adaptive response to herbicide

Raingeval,

Leduque,

Baduel

et al. 2023

Preprint

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The mobilization of retrotransposons yields major-effect mutations. Here, we report an adaptive retrotransposon insertion within the first intron of the Arabidopsis floral-repressor locus FLOWERING LOCUS C (FLC). The insertion-mutation augments the environmental sensitivity of FLC by affecting the balance between coding and non-coding transcript isoforms in response to environmental threads. We show that this balance is modulated epigenetically by DNA methylation and orchestrated by IBM2, a factor involved in the processing of intronic heterochromatin. The stress-sensitive allele of FLC has recently spread across populations subjected to recurrent chemical weeding, and we demonstrate that retrotransposon-driven acceleration of life cycle represents a rapid response to herbicide. Our findings illustrate how retrotransposition can create environmentally-sensitive alleles that facilitate adaptation to anthropogenic disturbances of the environment.

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“…Altogether, these results demonstrate the high specificity of our de novo transcript annotation. We next characterized the transcripts generated exclusively by TEs, as opposed to chimeric transcripts that span both TEs and cellular genes (Berthelier et al 2023). In total we identified 3,410 TE-derived transcripts, 76.8% of which contain at least two exons.…”

Section: High Quality Functional Annotation Of Transposable Element-e...mentioning

confidence: 99%

Transposable element products, functions, and regulatory networks in Arabidopsis

Borredá,

Leduque,

Colot

et al. 2024

Preprint

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Transposable elements (TEs) are DNA sequences with the ability to propagate themselves within genomes. Their mobilization is catalyzed by self-encoded factors, yet these factors have been poorly investigated. Here, we leveraged extensive long- and short-read transcriptome data, structural predictions, and regulatory networks analyses, to construct a comprehensive atlas of TE transcripts and their encoded products in the model organism Arabidopsis thaliana. We uncovered hundreds of transcriptionally competent TEs, each potentially encoding multiple proteins either through distinct genes, alternative splicing, or post-translational processing. Structural-based protein analyses revealed hitherto unidentified domains, uncovering proteins with multimerization and DNA binding domains forming macromolecular complexes. Furthermore, we demonstrate that TE expression is highly intertwined with the transcriptional network of cellular genes, and identified transcription factors and cis-regulatory elements associated with their coordinated expression during development or in response to environmental cues. This comprehensive functional atlas provides a valuable resource for studying the mechanisms involved in transposition and their consequences for genome and organismal function.

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Long-read direct RNA sequencing reveals epigenetic regulation of chimeric gene-transposon transcripts in Arabidopsis thaliana

Cited by 6 publications

References 123 publications

Natural diversity of heat-induced transcription of retrotransposons inArabidopsis thaliana

Natural diversity of heat-induced transcription of retrotransposons inArabidopsis thaliana

Retrotransposon-driven environmental regulation ofFLCleads to adaptive response to herbicide

Transposable element products, functions, and regulatory networks in Arabidopsis

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