Genome-wide identification of MITE-derived microRNAs and their targets in bread wheat

Crescente, Juan Manuel; Zavallo, Diego; Vas, Mariana del; Asurmendi, Sebastián; Helguera, Marcelo; Fernández, Elmer; Vanzetti, Leonardo Sebastián

doi:10.21203/rs.3.rs-236927/v1

Cited by 3 publications

(4 citation statements)

References 38 publications

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“…In wheat, TamiR113, which has dynamic expression under adverse conditions, was found to be derived from a MITE (Yu et al, 2014). Recently, a genome‐wide study revealed that among a total of 270 miRNAs, 38 miRNAs, including 10 24‐nt miRNAs, are derived from MITEs in wheat (Crescente et al, 2022). Here we found that more than half of lmiRNAs are derived from MITEs in rice seedlings, further supporting that MITEs are an important origin of small RNAs.…”

Section: Discussionmentioning

confidence: 99%

Evolution of lmiRNAs and their targets from MITEs for rice adaptation

Huang

Wang

et al. 2022

JIPB

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Twenty‐four nucleotide long microRNAs (lmiRNAs) direct DNA methylation at target genes and regulate their transcription. The evolutionary origin of lmiRNAs and the range of lmiRNA‐mediated regulation remain obscure. Here, we reannotated lmiRNAs and their targets in rice by applying stringent criteria. We found that the majority of lmiRNAs are derived from Miniature Inverted‐repeat Transposable Elements (MITEs) and most sites targeted by MITE‐derived lmiRNAs reside within MITEs, suggesting co‐evolution of lmiRNAs and their targets through MITE amplification. lmiRNAs undergo dynamically changes under stress conditions and the genes targeted by lmiRNAs show an enrichment for stress‐responsive genes, suggesting that lmiRNAs are widely involved in plant responses to stresses. We constructed the evolutionary histories of lmiRNAs and their targets. Nearly half of lmiRNAs emerged before or when the AA genome was diverged, while the emergence of lmiRNA targets coincided with or followed the emergence of lmiRNAs. Furthermore, we found that the sequences of a lmiRNA target site underwent variations, coincident with the divergence of rice accessions and the distribution of rice accessions in different geographical locations and climatic conditions. Our findings highlight MITEs as an important origin of lmiRNAs and suggest that the evolution of lmiRNA‐target regulatory modules may contribute to rice adaptation to environmental changes.

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Section: Discussionmentioning

confidence: 99%

Evolution of lmiRNAs and their targets from MITEs for rice adaptation

Huang

Wang

et al. 2022

JIPB

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“…Furthermore, TEs contain regulatory sequences such as promoters, transcription factors binding sits, and target sites for post-transcriptional degradation, which might affect adjacent gene expression or even modulate gene expression through complex transcriptional regulatory networks ( Bourque et al., 2018 ; Dubin et al., 2018 ; Qiu and Köhler, 2020 ; Zhang et al., 2021 ). Additionally, the insertion of TE into a gene body might result in the creation of new isoforms through exonization, truncation, alternative splicing, or even by the domestication of TE-derived coding sequences into host genes, potentially altering the gene function ( Keidar et al., 2018 ; Poretti et al., 2019 ; Crescente et al., 2022 ).…”

Section: Introductionmentioning

confidence: 99%

“…This observation led Ramírez-González et al., 2018 to suggest a possible role for TEs in gene regulation as cis-regulatory elements or through other epigenetic mechanisms in a tissue-specific manner. Moreover, recent studies showed that TEs, specifically MITEs (Miniature Inverted repeat TEs), which are prevalent in the vicinity of wheat genes, might act as miRNAs precursors in wheat and thus can potentially shape regulatory gene networks ( Poretti et al., 2019 ; Crescente et al., 2022 ). While the effect of TE insertions into promoter regions in wheat has been well-investigated, very little is known about the possible effect of TE insertions within gene bodies ( Li et al., 2014 ; Xi et al., 2016 ; Keidar et al., 2018 ; Keidar-Friedman et al., 2018 ; Domb et al., 2019 ; Jiang et al., 2019 ).…”

Section: Introductionmentioning

confidence: 99%

Transposable elements are associated with genome-specific gene expression in bread wheat

2023

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IntroductionRecent studies in wheat emphasized the importance of TEs, which occupy ~85% of the wheat genome, as a major source of intraspecific genetic variation due to their recent activity and involvement in genomic rearrangements. The contribution of TEs to structural and functional variations in bread wheat genes is not fully understood.MethodsHere, publicly available RNA-Seq databases of bread wheat were integrated to identify TE insertions within gene bodies (exons\ introns) and assess the impact of TE insertions on gene expression variations of homoeologs gene groups. Overall, 70,818 homoeologs genes were analyzed: 55,170 genes appeared in each one of the three subgenomes (termed ABD), named triads; 12,640 genes appeared in two of the three subgenomes (in A and B only, termed AB; or in A and D only, termed AD; or in B and D only, termed BD);, named dyads; and 3,008 genes underwent duplication in one of the three subgenomes (two copies in: subgenome A, termed AABD; subgenome B, termed ABBD; or subgenome D, termed ABDD), named tetrads.ResultsTo this end, we found that ~36% of the 70,818 genes contained at least one TE insertion within the gene body, mostly in triads. Analysis of 14,258 triads revealed that the presence of TE insertion in at least one of the triad genes (7,439 triads) was associated with balanced expression (similar expression levels) between the homoeolog genes. TE insertions within the exon or in the untranslated regions (UTRs) of one or more of the homoeologs in a triad were significantly associated with homoeolog expression bias. Furthermore, we found a statistically significant correlation between the presence\absence of TEs insertions belonging to six TE superfamilies and 17 TE subfamilies and the suppression of a single homoeolog gene. A significant association was observed between the presence of TE insertions from specific superfamilies and the expression of genes that are associated with biotic and abiotic stress responses.ConclusionOur data strongly indicate that TEs might play a prominent role in controlling gene expression in a genome-specific manner in bread wheat.

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“…One key feature of MITEs is that their transcripts can fold into hairpin-shaped dsRNAs due to the extensive sequence complementarity between IR arms. These dsRNA secondary structures are recognized and processed by DCL3 to produce 24-nt siRNAs that trigger DNA methylation without the need for RNAPIV/RDR2 activity (Ariel and Manavella, 2021;Crescente et al, 2022;Cuerda-Gil and Slotkin, 2016;Gagliardi et al, 2019;Sasaki et al, 2014). Thus, transcripts of these MITEs can be initiated from promoters of adjacent genes, triggering their RNA Polymerase II (RNAPII)dependent DNA methylation.…”

Section: Introductionmentioning

confidence: 99%

Polymorphic Inverted Repeats near coding genes impact chromatin topology and phenotypic traits in Arabidopsis thaliana

Arce

Mencia

Cambiagno

et al. 2022

Preprint

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Transposons are mobile elements that are commonly silenced to protect eukaryotic genome integrity. In plants, transposable elements (TEs) can be activated during stress conditions and subsequently insert into gene-rich regions. TE-derived inverted repeats (IRs) are commonly found near plant genes, where they affect host gene expression with potentially positive effects on adaptation. However, the molecular mechanisms by which these IRs control gene expression is unclear in most cases. Here, we identify in the Arabidopsis thaliana genome hundreds of IRs located near genes that are transcribed by RNA Polymerase II, resulting in the production of 24-nt small RNAs that trigger methylation of the IRs. The expression of these IRs is associated with drastic changes in the local 3D chromatin organization, which alter the expression pattern of the hosting genes. Notably, the presence and structure of many IRs differ between A. thaliana accessions. Capture-C sequencing experiments revealed that such variation changes short-range chromatin interactions, which translates into changes in gene expression patterns. CRISPR/Cas9-mediated disruption of two of such IRs leads to a switch in genome topology and gene expression, with phenotypic consequences. Our data demonstrate that the insertion of an IR near a gene provides an anchor point for chromatin interactions that can profoundly impact the activity of neighboring loci. This turns IRs into powerful evolutionary agents that can contribute to rapid adaptation.

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Genome-wide identification of MITE-derived microRNAs and their targets in bread wheat

Cited by 3 publications

References 38 publications

Evolution of lmiRNAs and their targets from MITEs for rice adaptation

Evolution of lmiRNAs and their targets from MITEs for rice adaptation

Transposable elements are associated with genome-specific gene expression in bread wheat

Polymorphic Inverted Repeats near coding genes impact chromatin topology and phenotypic traits in Arabidopsis thaliana

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