DNA methylation as a system of plant genomic immunity

Kim, M. Yvonne; Zilberman, Daniel

doi:10.1016/j.tplants.2014.01.014

Cited by 167 publications

(170 citation statements)

References 92 publications

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“…However, a recent study suggests that both 21-and 24-nt sRNAs are involved in deposition of DNA methylation (6). It is proposed that the 21-nt sRNAs may establish DNA methylation, whereas the 24-nt species are involved in its amplification and maintenance (7,8).…”

mentioning

confidence: 99%

Mobile small RNAs regulate genome-wide DNA methylation

Lewsey

Hardcastle

Melnyk

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

206

162

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RNA silencing at the transcriptional and posttranscriptional levels regulates endogenous gene expression, controls invading transposable elements (TEs), and protects the cell against viruses. Key components of the mechanism are small RNAs (sRNAs) of 21–24 nt that guide the silencing machinery to their nucleic acid targets in a nucleotide sequence-specific manner. Transcriptional gene silencing is associated with 24-nt sRNAs and RNA-directed DNA methylation (RdDM) at cytosine residues in three DNA sequence contexts (CG, CHG, and CHH). We previously demonstrated that 24-nt sRNAs are mobile from shoot to root in Arabidopsis thaliana and confirmed that they mediate DNA methylation at three sites in recipient cells. In this study, we extend this finding by demonstrating that RdDM of thousands of loci in root tissues is dependent upon mobile sRNAs from the shoot and that mobile sRNA-dependent DNA methylation occurs predominantly in non-CG contexts. Mobile sRNA-dependent non-CG methylation is largely dependent on the DOMAINS REARRANGED METHYLTRANSFERASES 1/2 (DRM1/DRM2) RdDM pathway but is independent of the CHROMOMETHYLASE (CMT)2/3 DNA methyltransferases. Specific superfamilies of TEs, including those typically found in gene-rich euchromatic regions, lose DNA methylation in a mutant lacking 22- to 24-nt sRNAs (dicer-like 2, 3, 4 triple mutant). Transcriptome analyses identified a small number of genes whose expression in roots is associated with mobile sRNAs and connected to DNA methylation directly or indirectly. Finally, we demonstrate that sRNAs from shoots of one accession move across a graft union and target DNA methylation de novo at normally unmethylated sites in the genomes of root cells from a different accession.

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mentioning

confidence: 99%

Mobile small RNAs regulate genome-wide DNA methylation

Lewsey

Hardcastle

Melnyk

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

206

162

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“…Dramatic increases in genome size, notably in the grasses, are driven by bursts of retroelement or DNA-repeat expansion that tend to preserve an underlying conserved order and composition of genes 9 . DNA repeats have an important role in generating phenotypic diversity and plants have evolved epigenetic mechanisms to limit the parasitic expansion of repeats 10,11 . The other dominant feature of plant-genome evolution is whole-genome duplication (see Box 1 for a definition of this and other terms that are used in crop improvement), which is pervasive in most plant lineages 12 .…”

Section: Crop Plant Genomesmentioning

confidence: 99%

Genomic innovation for crop improvement

Bevan

Uauy

Wulff

et al. 2017

Nature

331

240

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Crop production needs to increase to secure future food supplies, while reducing its impact on ecosystems. Detailed characterization of plant genome structure and genetic diversity is crucial for meeting these challenges. Advances in genome sequencing and assembly are being used to access to the large and complex genomes of crops and their wild relatives. Sequencing of wild crop relatives is identifying a wide spectrum of genetic variation, permitting the association of genetic diversity with diverse agronomic phenotypes. In combination with improved and automated phenotyping assays and functional genomic studies, genomics is providing new foundations for crop-breeding systems. In the twentieth century, famines caused by political crises, mismanagement of food production or genocide killed an estimated 70 million people and were second only to war as the greatest manmade cause of death 1 . The father of the Green Revolution, Norman Borlaug, summarized the importance of crops: "Without food, people perish, social and political organizations disintegrate, and civilizations collapse. " For thousands of years, people have dedicated considerable resources to securing food supplies; for example, grain supplies to ancient Rome were secured through an extensive network of long-distance transport, and the distribution of grain was coordinated and subsidized by the cura annonae ('care for the grain supply'), an important figure who contributed to the maintenance of political unity and power.During the past 10,000 years, a period known as the Holocene, Earth's environment has been unusually stable. This probably facilitated the domestication of crops from wild species, resulting in steadily improved yields and adaptation to new agricultural areas. The production of food is now carried out on a vast scale, with 38% of Earth's surface dedicated to agriculture 2 . This increased production is having a pervasive influence on ecosystems worldwide: nitrogen production for agriculture accounts for 1.2% of global energy consumption 3 ; photosynthesis can no longer maintain stable levels of atmospheric carbon dioxide; and food production consumes around 70% of freshwater supplies. The modelling of crop responses to increases in temperature predicts that there will be a considerable reduction in the yield of rice, an important crop around the world 4 . Climate change could also alter the dynamics of crop pathogenic agents by altering the range of vectors and by compromising the immune response of crops 5 .Crop production must therefore adapt to more variable environments and the substantial impact it has on the environment needs to be reduced. Productivity must also increase at a much greater rate than in the past to meet the needs of Earth's growing population 6 . Genetic improvements in crop performance continue to be crucial for increasing crop productivity, but current rates of improvement are unable to meet the demands of sustainability and food security 7 . Plant genomics has a central role in the improvement of crops, includi...

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“…3 Gene silencing is involved in several biological processes of plants, including defending the genome from transposable elements (TEs), development, imprinting, environmental responses and stress memory. [3][4][5][6][7][8][9][10][11] Cytosine residues of DNA can be modified by the addition of a methyl group. This is associated with transcriptional gene silencing and formation of repressive chromatin, influencing potentially both structure and function of target loci.…”

Section: Introductionmentioning

confidence: 99%

“…[12][13][14][15] Methylation may be directed to specific cytosine residues by the RNA-directed DNA methylation (RdDM) gene silencing pathway. 4,[16][17][18][19] We take a 4 stage framework as a basic model for RdDM, following Bond & Baulcombe. 19 Initiation occurs first, during which 21/22 nt sRNAs sharing sequence homology with target loci are generated by DICER-LIKE (DCL) family enzymes DCL2 and DCL4.…”

Section: Introductionmentioning

confidence: 99%

“…2,3,21 DRM1 and DRM2 then methylate cytosines of target loci in non-CG contexts (CHG and CHH, where H is A, T or C). 4,22 Twenty-4 nt sRNAs then act through the RNA polymerase IV (PolIV)-dependent pathway in a self-reinforcing RNA-dependent maintenance phase that includes methylation of CG and non-CG context cytosines. DCL3 is responsible primarily for generation of this size of sRNAs.…”

Section: Introductionmentioning

confidence: 99%

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Mobile small RNAs and their role in regulating cytosine methylation of DNA

Hardcastle

Lewsey

2016

RNA Biology

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Small (s)RNAs of 21 to 24 nucleotides are associated with RNA silencing and methylation of DNA cytosine residues. All sizes can move from cell-to-cell and long distance in plants, directing RNA silencing in destination cells. Twenty-four nucleotide sRNAs are the predominant long-distance mobile species. Thousands move from shoot to root, where they target methylation of transposable elements both directly and indirectly. We derive several classes of interaction between small RNAs and methylation and use these to explore the mechanisms of methylation and gene expression that associate with mobile sRNA signaling.

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DNA methylation as a system of plant genomic immunity

Cited by 167 publications

References 92 publications

Mobile small RNAs regulate genome-wide DNA methylation

Mobile small RNAs regulate genome-wide DNA methylation

Genomic innovation for crop improvement

Mobile small RNAs and their role in regulating cytosine methylation of DNA

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