Domestication of rice has reduced the occurrence of transposable elements within gene coding regions

Li, Xukai; Guo, Kai; Zhu, Xiaobo; Chen, Peng; Liu, Ying; Xie, Guosheng; Wang, Lingqiang; Wang, Yanting; Persson, Staffan; Peng, Liangcai

doi:10.1186/s12864-016-3454-z

Cited by 26 publications

(24 citation statements)

References 56 publications

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“…A recent study showed that wild rice genomes tend to accumulate TEs in genic regions, while cultivated rice genomes show depletion of TEs from genic regions including introns [103]. This has likely occurred independently in the genomes of several cultivars [103]. This convergent loss of genic TE sequences in cultivar genomes may be a result of selective pressure against long heterochromatic TEs in the genic regions during domestication and selection (Fig 3).…”

Section: Plos Geneticsmentioning

confidence: 96%

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Transcriptional regulation of genes bearing intronic heterochromatin in the rice genome

Espinas

Furci

et al. 2020

PLoS Genet

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Intronic regions of eukaryotic genomes accumulate many Transposable Elements (TEs). Intronic TEs often trigger the formation of transcriptionally repressive heterochromatin, even within transcription-permissive chromatin environments. Although TE-bearing introns are widely observed in eukaryotic genomes, their epigenetic states, impacts on gene regulation and function, and their contributions to genetic diversity and evolution, remain poorly understood. In this study, we investigated the genome-wide distribution of intronic TEs and their epigenetic states in the Oryza sativa genome, where TEs comprise 35% of the genome. We found that over 10% of rice genes contain intronic heterochromatin, most of which are associated with TEs and repetitive sequences. These heterochromatic introns are longer and highly enriched in promoter-proximal positions. On the other hand, introns also accumulate hypomethylated short TEs. Genes with heterochromatic introns are implicated in various biological functions. Transcription of genes bearing intronic heterochromatin is regulated by an epigenetic mechanism involving the conserved factor OsIBM2, mutation of which results in severe developmental and reproductive defects. Furthermore, we found that heterochromatic introns evolve rapidly compared to non-heterochromatic introns. Our study demonstrates that heterochromatin is a common epigenetic feature associated with actively transcribed genes in the rice genome.

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Section: Plos Geneticsmentioning

confidence: 96%

Section: Plos Geneticsmentioning

confidence: 99%

Transcriptional regulation of genes bearing intronic heterochromatin in the rice genome

Espinas

Furci

et al. 2020

PLoS Genet

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“…Several other genes related mostly to japonica rice domestication, including qSH1, PLOG1, qSW5, GIF1, and Rc, have been cloned and functionally characterized (Kovach et al, 2007;Izawa, 2008). In such instances, simple changes in the promoter sequences of these genes altered their expression (Huo et al, 2017), while in some cases insertion of a transposon was responsible (Li et al, 2017). There were also SNPs that likely alter the key amino acids in important proteins such as enzymes (Kharabian-Masouleh et al, 2012;Ma et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

Major Domestication-Related Phenotypes inIndicaRice Are Due to Loss of miRNA-Mediated Laccase Silencing

et al. 2018

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Domestication of rice (Oryza sativa) included conversion of perennial wild species with few seeds to short plants that produced abundant seeds. Most domestication-associated changes were due to variations in transcription factors and other key proteins such as enzymes. Here, we show that multiple yield-related traits associated with indica rice domestication are linked to micro (mi) RNA-mediated regulation. Analysis of small (s) RNA data sets from cultivated indica rice lines, a few landraces, and two wild relatives of rice revealed the presence of abundant 22-nucleotide (nt) reads in wild relatives that mapped to miR397 precursors. miR397 was expressed at very high levels in wild relatives and at negligible levels in high-yielding cultivated lines. In its genera-specific form of 22-nt, miR397 targeted mRNAs encoding laccases that decayed and induced robust secondary cascade silencing in wild species that required RNA-dependent RNA polymerase 6. In wild species of rice, reduced expression of laccases resulted in low lignification. As expected, overexpression of miR397 induced de-domestication phenotypes. At least 26 uncharacterized QTLs previously implicated in rice yield overlapped with laccases and miR397 genes. These results suggest that miRNAs contribute to rice domestication-associated phenotypes.

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“…Cultivation and plant breeding reduces genetic diversity and tness to environmental stresses (Roger et al, 2012). A recent whole-genome comparison of wild and cultivated rice species revealed depletion of intronic TE insertions in cultivated species (Li et al, 2017b). Gymnosperms are outcrossing species that produce large quantities of pollen and seeds, generating a genetically diverse germplasm pool for subsequent natural selection of highly adaptable seedlings.…”

Section: Discussionmentioning

confidence: 99%

Comparative study of pine reference genomes reveals transposable element interconnected gene networks

Voronova

Rendón-Anaya

Ingvarsson

et al. 2020

Preprint

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Background: Sequencing the giga-genomes of several pine species belonging to the ancient gymnosperm clade has enabled comparative genomic analyses of these widely distributed outcrossing tree species. Initial sequence studies have revealed the wide distribution and extraordinary diversity of transposable elements (TEs) that occupy the large intergenic spaces. Our previous investigations revealed significant variations of class I TEs within pine subpopulations, but inoculation with pathogen induced correlated expression of TE families in pine seedlings, suggesting TE co-localisation with stress-responsive genes. In this study, we analyzed the distribution of TEs in gene regions of the assembled genomes of Pinus taeda and Pinus lambertiana using high-performance computing resources.Results: The quality of draft genomes and the genome annotation have significant consequences for the investigation of TEs and these aspects are discussed. Several TE families were identified in both species genomes frequently inserted into genes or their flanks. The non-autonomous MITE3321 family found in gene flanking regions and provide TATA boxes, several ARR1, DOF, WRKY and GT-binding sites, which are important signals in plant transcription activation and stress-response regulation. Distribution of MITE3321 across gene non-coding regions suggests action of selective pressure on this sequences and formation of gene sub-networks, depending on the location of MITE insertions. DNA TE DTX184 could potentially form microRNAs or provide its target site, thereby connect about 200 important stress-responsive genes in both pine species. Several retrotransposons propagated in gene regions were also identified, such as Copia-1813 containing important light-responsive regulative sequences, however full- length structures of low-copy-number TEs couldn’t be verified in the current genome assemblies. Only rare gene homologs carried similar insertions, indicating that most transposition events occurred after separation of investigated pine species. Node genes that contain many types of interspersed repeats were identified and observed in multiple potential transposable element associated networks.Conclusions: This study demonstrated the increased accumulation of TEs in the introns of stress-responsive genes of pines and the probability of rewiring them in responsive networks and sub-networks interconnected with node genes containing multiple TEs. Many such regulatory influences could lead to the adaptive environmental response clines that are characteristic of naturally spread pine populations.

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Domestication of rice has reduced the occurrence of transposable elements within gene coding regions

Cited by 26 publications

References 56 publications

Transcriptional regulation of genes bearing intronic heterochromatin in the rice genome

Transcriptional regulation of genes bearing intronic heterochromatin in the rice genome

Major Domestication-Related Phenotypes inIndicaRice Are Due to Loss of miRNA-Mediated Laccase Silencing

Comparative study of pine reference genomes reveals transposable element interconnected gene networks

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