Domestication of High-Copy Transposons Underlays the Wheat Small RNA Response to an Obligate Pathogen

Abstract Plant genomes have evolved several evolutionary mechanisms to tolerate and make use of transposable elements (TEs). Of these, transposon domestication into cis-regulatory and microRNA (miRNA) sequences is proposed to contribute to abiotic/biotic stress adaptation in plants. The wheat genome is derived at 85% from TEs, and contains thousands of miniature inverted-repeat transposable elements (MITEs), whose sequences are particularly prone for domestication into miRNA precursors. In this study, we investigate the contribution of TEs to the wheat small RNA immune response to the lineage-specific, obligate powdery mildew pathogen. We show that MITEs of the Mariner superfamily contribute the largest diversity of miRNAs to the wheat immune response. In particular, MITE precursors of miRNAs are wide-spread over the wheat genome, and highly conserved copies are found in the Lr34 and QPm.tut-4A mildew resistance loci. Our work suggests that transposon domestication is an important evolutionary force driving miRNA functional innovation in wheat immunity.

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A miniature inverted-repeat transposable element, AddIn-MITE, located inside a WD40 gene is conserved in Andropogoneae grasses

PeerJ ◽

10.7717/peerj.6080 ◽

2019 ◽

Vol 7 ◽

pp. e6080

Author(s):

Clicia Grativol ◽

Flavia Thiebaut ◽

Sara Sangi ◽

Patricia Montessoro ◽

Walaci da Silva Santos ◽

...

Keyword(s):

Transposable Elements ◽

Transposable Element ◽

Small Rna ◽

Genome Assembly ◽

Inverted Repeat ◽

Small Rnas ◽

Distribution Patterns ◽

Plant Genomes ◽

Sugarcane Genome

Miniature inverted-repeat transposable elements (MITEs) have been associated with genic regions in plant genomes and may play important roles in the regulation of nearby genes via recruitment of small RNAs (sRNA) to the MITEs loci. We identified eight families of MITEs in the sugarcane genome assembly with MITE-Hunter pipeline. These sequences were found to be upstream, downstream or inserted into 67 genic regions in the genome. The position of the most abundant MITE (Stowaway-like) in genic regions, which we call AddIn-MITE, was confirmed in a WD40 gene. The analysis of four monocot species showed conservation of the AddIn-MITE sequence, with a large number of copies in their genomes. We also investigated the conservation of the AddIn-MITE’ position in the WD40 genes from sorghum, maize and, in sugarcane cultivars and wild Saccharum species. In all analyzed plants, AddIn-MITE has located in WD40 intronic region. Furthermore, the role of AddIn-MITE-related sRNA in WD40 genic region was investigated. We found sRNAs preferentially mapped to the AddIn-MITE than to other regions in the WD40 gene in sugarcane. In addition, the analysis of the small RNA distribution patterns in the WD40 gene and the structure of AddIn-MITE, suggests that the MITE region is a proto-miRNA locus in sugarcane. Together, these data provide insights into the AddIn-MITE role in Andropogoneae grasses.

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Faculty Opinions recommendation of Epigenetic reprogramming and small RNA silencing of transposable elements in pollen.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.1157170.617284 ◽

2009 ◽

Author(s):

Elizabeth Dennis

Keyword(s):

Transposable Elements ◽

Small Rna ◽

Rna Silencing ◽

Epigenetic Reprogramming

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Evolutionary rewiring of the wheat transcriptional regulatory network by lineage-specific transposable elements

Genome Research ◽

10.1101/gr.275658.121 ◽

2021 ◽

pp. gr.275658.121

Author(s):

Yuyun Zhang ◽

Zijuan Li ◽

Yu'e Zhang ◽

Kande Lin ◽

Yuan Peng ◽

...

Keyword(s):

Transposable Elements ◽

Genome Evolution ◽

Regulatory Networks ◽

Transcriptional Regulatory Network ◽

Sequence Similarity ◽

Purifying Selection ◽

Wheat Genome ◽

Specific Gene ◽

High Sequence Similarity ◽

Wheat Genome Evolution

More than 80% of the wheat genome consists of transposable elements (TEs), which act as one major driver of wheat genome evolution. However, their contributions to the regulatory evolution of wheat adaptations remain largely unclear. Here, we created genome-binding maps for 53 transcription factors (TFs) underlying environmental responses by leveraging DAP-seq in Triticum urartu, together with epigenomic profiles. Most TF-binding sites (TFBS) located distally from genes are embedded in TEs, whose functional relevance is supported by purifying selection and active epigenomic features. About 24% of the non-TE TFBS share significantly high sequence similarity with TE-embedded TFBS. These non-TE TFBS have almost no homologous sequences in non-Triticeae species and are potentially derived from Triticeae-specific TEs. The expansion of TE-derived TFBS linked to wheat-specific gene responses, suggesting TEs are an important driving force for regulatory innovations. Altogether, TEs have been significantly and continuously shaping regulatory networks related to wheat genome evolution and adaptation.

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Histone H1 prevents non-CG methylation-mediated small RNA biogenesis in Arabidopsis heterochromatin

10.1101/2021.07.31.454434 ◽

2021 ◽

Author(s):

Jaemyung Choi ◽

David Bruce Lyons ◽

Daniel Zilberman

Keyword(s):

Dna Methylation ◽

Transposable Elements ◽

Small Rna ◽

Histone H3 ◽

Histone H1 ◽

Dna Methyltransferases ◽

Flowering Plants ◽

Genomic Sequences ◽

Rna Molecules ◽

Rna Biogenesis

Flowering plants utilize small RNA molecules to guide DNA methyltransferases to genomic sequences. This RNA-directed DNA methylation (RdDM) pathway preferentially targets euchromatic transposable elements. However, RdDM is thought to be recruited by methylation of histone H3 at lysine 9 (H3K9me), a hallmark of heterochromatin. How RdDM is targeted to euchromatin despite an affinity for H3K9me is unclear. Here we show that loss of histone H1 enhances heterochromatic RdDM, preferentially at nucleosome linker DNA. Surprisingly, this does not require SHH1, the RdDM component that binds H3K9me. Furthermore, H3K9me is dispensable for RdDM, as is CG DNA methylation. Instead, we find that non-CG methylation is specifically required for small RNA biogenesis, and without H1 small RNA production quantitatively expands to non-CG methylated loci. Our results demonstrate that H1 enforces the separation of euchromatic and heterochromatic DNA methylation pathways by excluding the small RNA-generating branch of RdDM from non-CG methylated heterochromatin.

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Multigenome analysis implicates miniature inverted-repeat transposable elements (MITEs) in metabolic diversification in eudicots

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1721318115 ◽

2018 ◽

Vol 115 (28) ◽

pp. E6650-E6658 ◽

Cited By ~ 12

Author(s):

Alexander M. Boutanaev ◽

Anne E. Osbourn

Keyword(s):

Transposable Elements ◽

Inverted Repeat ◽

Cluster Formation ◽

Gene Clusters ◽

Biosynthetic Gene Cluster ◽

Terpene Synthase ◽

Biosynthetic Gene ◽

Biosynthetic Gene Clusters ◽

Systematic Analysis ◽

Plant Genomes

Plants produce a plethora of natural products, including many drugs. It has recently emerged that the genes encoding different natural product pathways may be organized as biosynthetic gene clusters in plant genomes, with >30 examples reported so far. Despite superficial similarities with microbes, these clusters have not arisen by horizontal gene transfer, but rather by gene duplication, neofunctionalization, and relocation via unknown mechanisms. Previously we reported that two Arabidopsis thaliana biosynthetic gene clusters are located in regions of the genome that are significantly enriched in transposable elements (TEs). Other plant biosynthetic gene clusters also harbor abundant TEs. TEs can mediate genomic rearrangement by providing homologous sequences that enable illegitimate recombination and gene relocation. Thus, TE-mediated recombination may contribute to plant biosynthetic gene cluster formation. TEs may also facilitate establishment of regulons. However, a systematic analysis of the TEs associated with plant biosynthetic gene clusters has not been carried out. Here we investigate the TEs associated with clustered terpene biosynthetic genes in multiple plant genomes and find evidence to suggest a role for miniature inverted-repeat transposable elements in cluster formation in eudicots. Through investigation of the newly sequenced Amborella trichopoda, Aquilegia coerulea, and Kalanchoe fedtschenkoi genomes, we further show that the “block” mechanism of founding of biosynthetic gene clusters through duplication and diversification of pairs of terpene synthase and cytochrome P450 genes that is prevalent in the eudicots arose around 90–130 million years ago, after the appearance of the basal eudicots and before the emergence of the superrosid clade.

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

10.21203/rs.3.rs-236927/v1 ◽

2021 ◽

Author(s):

Juan Manuel Crescente ◽

Diego Zavallo ◽

Mariana del Vas ◽

Sebastian Asurmendi ◽

Marcelo Helguera ◽

...

Keyword(s):

Gene Expression ◽

Triticum Aestivum ◽

Transposable Elements ◽

Small Rna ◽

Translational Repression ◽

High Homology ◽

Genome Wide ◽

Target Sites ◽

The Common ◽

Non Coding Rnas

Abstract Plant microRNAs (miRNAs) are a class of small non-coding RNAs that are 20–24 nucleotides length and can repress gene expression at post-transcriptional levels by target degradation or translational repression. There is increasing evidence that some microRNAs can be derived from a group of non-autonomous class II transposable elements called Miniature Inverted-repeat Transposable Elements (MITEs) in plants. We used public small RNA, degradome libraries and the common wheat (Triticum aestivum) genome to screen miRNAs production and target sites. We also created a comprehensive wheat MITE database using known and identifying novel elements. We found high homology between MITEs and 14% of all the miRNAs production sites in wheat. Furthermore, we show that MITE-derived miRNAs have preference for target degradation sites with MITE insertions in 3' UTR regions in wheat.

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