scholarly journals The plant mobile domain proteins MAIN and MAIL1 interact with the phosphatase PP7L to regulate gene expression and silence transposable elements in Arabidopsis thaliana

2019 ◽  
Author(s):  
Melody Nicolau ◽  
Nathalie Picault ◽  
Julie Descombin ◽  
Yasaman Jami-Alahmadi ◽  
Suhua Feng ◽  
...  

ABSTRACTTransposable elements (TEs) are DNA repeats that must remain silenced to ensure cell integrity. Several epigenetic pathways including DNA methylation and histone modifications are involved in the silencing of TEs, and in the regulation of gene expression. In Arabidopsis thaliana, the TE-derived plant mobile domain (PMD) proteins have been involved in TE silencing, genome stability, and control of developmental processes. Using a forward genetic screen, we found that the PMD protein MAINTENANCE OF MERISTEMS (MAIN) acts synergistically and redundantly with DNA methylation to silence TEs. We found that MAIN and its close homolog MAIN-LIKE 1 (MAIL1) interact together, as well as with the phosphoprotein phosphatase (PPP) PP7-like (PP7L). Remarkably, main, mail1, pp7l single and mail1 pp7l double mutants display similar developmental phenotypes, and share common subsets of upregulated TEs and misregulated genes. Finally, phylogenetic analyses of PMD and PP7-type PPP domains among the Eudicot lineage suggest neo-association processes between the two protein domains to potentially generate new protein function. We propose that, through this interaction, the PMD and PPP domains may constitute a functional protein module required for the proper expression of a common set of genes, and for silencing of TEs.AUTHOR SUMMARYThe plant mobile domain (PMD) is a protein domain of unknown function that is widely spread in the angiosperm plants. Although most PMDs are associated with repeated DNA sequences called transposable elements (TEs), plants have domesticated the PMD to produce genic versions that play important roles within the cell. In Arabidopsis thaliana, MAINTENANCE OF MERISTEMS (MAIN) and MAIN-LIKE 1 (MAIL1) are genic PMDs that are involved in genome stability, developmental processes, and silencing of TEs. The mechanisms involving MAIN and MAIL1 in these cellular processes remain elusive. Here, we show that MAIN, MAIL1 and the phosphoprotein phosphatase (PPP) named PP7-like (PP7L) interact to form a protein complex that is required for the proper expression of genes, and the silencing of TEs. Phylogenetic analyses revealed that PMD and PP7-type PPP domains are evolutionary connected, and several plant species express proteins carrying both PMD and PPP domains. We propose that interaction of PMD and PPP domains would create a functional protein module involved in mechanisms regulating gene expression and repressing TEs.

2021 ◽  
Vol 118 (35) ◽  
pp. e2107320118
Author(s):  
Li He ◽  
Cheng Zhao ◽  
Qingzhu Zhang ◽  
Gaurav Zinta ◽  
Dong Wang ◽  
...  

The CMT2 and RNA-directed DNA methylation (RdDM) pathways have been proposed to separately maintain CHH methylation in specific regions of the Arabidopsis thaliana genome. Here, we show that dysfunction of the chromatin remodeler DDM1 causes hundreds of genomic regions to switch from CMT2 dependency to RdDM dependency in DNA methylation. These converted loci are enriched at the edge regions of long transposable elements (TEs). Furthermore, we found that dysfunction in both DDM1 and RdDM causes strong reactivation of TEs and a burst of TE transposition in the first generation of mutant plants, indicating that the DDM1 and RdDM pathways together are critical to maintaining TE repression and protecting genomic stability. Our findings reveal the existence of a pathway conversion–based backup mechanism to guarantee the maintenance of DNA methylation and genome integrity.


2020 ◽  
Author(s):  
Rurika Oka ◽  
Mattijs Bliek ◽  
Huub C.J. Hoefsloot ◽  
Maike Stam

AbstractBackgroundDNA methylation is an important factor in the regulation of gene expression and genome stability. High DNA methylation levels are associated with transcriptional repression. In mammalian systems, unmethylated, low methylated and fully methylated regions (UMRs, LMRs, and FMRs, respectively) can be distinguished. UMRs are associated with proximal regulatory regions, while LMRs are associated with distal regulatory regions. Although DNA methylation is mainly limited to the CG context in mammals, while it occurs in CG, CHG and CHH contexts in plants, UMRs and LMRs were expected to occupy similar genomic sequences in both mammals and plants.ResultsThis study investigated major model and crop plants such as Arabidopsis thaliana, tomato (Solanum lycopersicum), rice (Oryza sativa) and maize (Zea mays), and shows that plant genomes can also be subdivided in UMRs, LMRs and FMRs, but that LMRs are mainly present in the CHG context rather than the CG context. Strikingly, the identified CHG LMRs were enriched in transposable elements rather than regulatory regions. Maize candidate regulatory regions overlapped with UMRs. LMRs were enriched for heterochromatic histone modifications and depleted for DNase accessibility and H3K9 acetylation. CHG LMRs form a distinct, abundant cluster of loci, indicating they have a different role than FMRs.ConclusionsBoth mammalian and plant genomes can be segmented in three distinct classes of loci, UMRs, LMRs and FMRs, indicating similar underlying mechanisms. Unlike in mammals, distal regulatory sequences in plants appear to overlap with UMRs instead of LMRs. Our data indicate that LMRs in plants have a different function than those in mammals.


PLoS ONE ◽  
2012 ◽  
Vol 7 (1) ◽  
pp. e30515 ◽  
Author(s):  
Andriy Bilichak ◽  
Yaroslav Ilnystkyy ◽  
Jens Hollunder ◽  
Igor Kovalchuk

2018 ◽  
Vol 35 (16) ◽  
pp. 2718-2723 ◽  
Author(s):  
Tamir Tuller ◽  
Alon Diament ◽  
Avital Yahalom ◽  
Assaf Zemach ◽  
Shimshi Atar ◽  
...  

Abstract Motivation The COP9 signalosome is a highly conserved multi-protein complex consisting of eight subunits, which influences key developmental pathways through its regulation of protein stability and transcription. In Arabidopsis thaliana, mutations in the COP9 signalosome exhibit a number of diverse pleiotropic phenotypes. Total or partial loss of COP9 signalosome function in Arabidopsis leads to misregulation of a number of genes involved in DNA methylation, suggesting that part of the pleiotropic phenotype is due to global effects on DNA methylation. Results We determined and analyzed the methylomes and transcriptomes of both partial- and total-loss-of-function Arabidopsis mutants of the COP9 signalosome. Our results support the hypothesis that the COP9 signalosome has a global genome-wide effect on methylation and that this effect is at least partially encoded in the DNA. Our analyses suggest that COP9 signalosome-dependent methylation is related to gene expression regulation in various ways. Differentially methylated regions tend to be closer in the 3D conformation of the genome to differentially expressed genes. These results suggest that the COP9 signalosome has a more comprehensive effect on gene expression than thought before, and this is partially related to regulation of methylation. The high level of COP9 signalosome conservation among eukaryotes may also suggest that COP9 signalosome regulates methylation not only in plants but also in other eukaryotes, including humans. Supplementary information Supplementary data are available at Bioinformatics online.


2020 ◽  
Vol 12 (11) ◽  
pp. 1994-2001 ◽  
Author(s):  
Michele Wyler ◽  
Christoph Stritt ◽  
Jean-Claude Walser ◽  
Célia Baroux ◽  
Anne C Roulin

Abstract Transposable elements (TEs) constitute a large fraction of plant genomes and are mostly present in a transcriptionally silent state through repressive epigenetic modifications, such as DNA methylation. TE silencing is believed to influence the regulation of adjacent genes, possibly as DNA methylation spreads away from the TE. Whether this is a general principle or a context-dependent phenomenon is still under debate, pressing for studying the relationship between TEs, DNA methylation, and nearby gene expression in additional plant species. Here, we used the grass Brachypodium distachyon as a model and produced DNA methylation and transcriptome profiles for 11 natural accessions. In contrast to what is observed in Arabidopsis thaliana, we found that TEs have a limited impact on methylation spreading and that only few TE families are associated with a low expression of their adjacent genes. Interestingly, we found that a subset of TE insertion polymorphisms is associated with differential gene expression across accessions. Thus, although not having a global impact on gene expression, distinct TE insertions may contribute to specific gene expression patterns in B. distachyon.


Author(s):  
Michele Wyler ◽  
Christoph Stritt ◽  
Jean-Claude Walser ◽  
Célia Baroux ◽  
Anne C. Roulin

AbstractTransposable elements (TEs) constitute a large fraction of plant genomes and are mostly present in a transcriptionally silent state through repressive epigenetic modifications such as DNA methylation. TE silencing is believed to influence the regulation of adjacent genes, possibly as DNA methylation spreads away from the TE. Whether this is a general principle or a context-dependent phenomenon is still under debate, pressing for studying the relationship between TEs, DNA methylation and nearby gene expression in additional plant species. Here we used the grass Brachypodium distachyon as a model and produced DNA methylation and transcriptome profiles for eleven natural accessions. In contrast to what is observed in Arabidopsis thaliana, we found that TEs have a limited impact on methylation spreading and that only few TE families are associated to a low expression of their adjacent genes. Interestingly, we found that a subset of TE insertion polymorphisms is associated with differential gene expression across accessions. Thus, although not having a global impact on gene expression, distinct TE insertions may contribute to specific gene expression patterns in B. distachyon.Significance statementTransposable elements (TEs) are a major component of plant genomes and a source of genetic and epigenetic innovations underlying adaptation to changing environmental conditions. Yet molecular evidence linking TE silencing and nearby gene expression are lacking for many plant species. We show that in the model grass Brachypodium DNA methylation spreads over very short distances around TEs, with an influence on gene expression for a small subset of TE families.


2021 ◽  
Vol 12 ◽  
Author(s):  
Suresh Kumar ◽  
Trilochan Mohapatra

Epigenetic modifications in DNA bases and histone proteins play important roles in the regulation of gene expression and genome stability. Chemical modification of DNA base (e.g., addition of a methyl group at the fifth carbon of cytosine residue) switches on/off the gene expression during developmental process and environmental stresses. The dynamics of DNA base methylation depends mainly on the activities of the writer/eraser guided by non-coding RNA (ncRNA) and regulated by the developmental/environmental cues. De novo DNA methylation and active demethylation activities control the methylation level and regulate the gene expression. Identification of ncRNA involved in de novo DNA methylation, increased DNA methylation proteins guiding DNA demethylase, and methylation monitoring sequence that helps maintaining a balance between DNA methylation and demethylation is the recent developments that may resolve some of the enigmas. Such discoveries provide a better understanding of the dynamics/functions of DNA base methylation and epigenetic regulation of growth, development, and stress tolerance in crop plants. Identification of epigenetic pathways in animals, their existence/orthologs in plants, and functional validation might improve future strategies for epigenome editing toward climate-resilient, sustainable agriculture in this era of global climate change. The present review discusses the dynamics of DNA methylation (cytosine/adenine) in plants, its functions in regulating gene expression under abiotic/biotic stresses, developmental processes, and genome stability.


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