Abstract
DNA methylation, also known as 5-methylcytosine, is an epigenetic modification that has crucial functions in plant growth, development and adaptation. The cellular DNA methylation level is tightly regulated by the combined action of DNA methyltransferases and demethylases. Protein complexes involved in the targeting and interpretation of DNA methylation have been identified, revealing intriguing roles of methyl-DNA binding proteins and molecular chaperones. Structural studies and in vitro reconstituted enzymatic systems have provided mechanistic insights into RNA-directed DNA methylation, the main pathway catalysing de novo methylation in plants. A better understanding of the regulatory mechanisms will enable locus-specific manipulation of the DNA methylation status. CRISPR–dCas9-based epigenome editing tools are being developed for this goal. Given that DNA methylation patterns can be stably transmitted through meiosis, and that large phenotypic variations can be contributed by epimutations, epigenome editing holds great promise in crop breeding by creating additional phenotypic variability on the same genetic material.
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Acknowledgements
The authors apologize to all colleagues whose work could not be cited because of space limitations. They thank Y. Zhang from the CAS Center for Excellence in Molecular Plant Sciences for the careful reading and helpful discussion of the manuscript. This work was partly supported by the National Key Research and Development Program of China (2021YFA1300401 to H.Z. and 2021YFA1300400 to J.-K.Z.).
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J.-K.Z. made a substantial contribution to discussion of content, wrote and reviewed/edited the manuscript before submission. H.Z. researched data for the article, made a substantial contribution to discussion of content, wrote and reviewed/edited the manuscript before submission.
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Glossary
- De novo DNA methylation
-
A process of adding a methyl group to the cytosine base of unmethylated DNA. Among CG, CHG and CHH methylation, only CHH methylation is asymmetrical, that is, its complementary strand is not methylated. Thus, maintaining CHH methylation during DNA replication requires de novo methyltransferase activity.
- EasiRNAs
-
Secondary small interfering RNAs produced from AGO1-microRNA-cleaved transposable element transcripts. Production of easiRNAs in the pollen relies on DCL2, DCL4 and RNA polymerase IV.
- Epigenetic modification
-
Covalent modification of the DNA or histones that confers mitotically or meiotically heritable alterations of gene expression status but does not involve DNA sequence changes.
- Epigenetic recombination inbred lines
-
Epigenetic recombinant inbred lines are created by crosses between wild-type and hypomethylated (such as met1 or ddm1 mutant) plants followed by multiple generations of inbreeding.
- Gene body methylation
-
DNA methylation pattern associated with a subset of genes. It is characterized by medium to high levels of CG methylation and depletion of non-CG methylation in the gene body and low methylation around transcription start and termination sites.
- Interploidy hybridization barriers
-
Intraspecific hybridization barriers between individual plants with different ploidy levels, also known as the triploid block.
- Intragenic heterochromatin
-
A heterochromatin region located within an expressed protein-coding gene.
- Mutation accumulation lines
-
Plant lines that are propagated from a single founder through inbreeding and single-seed descent for several generations in the laboratory with the aim of minimizing the effect of natural selection and allowing the accumulation of spontaneous mutations (and epimutations).
- Paramutation
-
An epigenetic phenomenon whereby one allele induces heritable changes in the expression status of the other allele of the same locus. Paramutation has been discovered in both plants and animals.
- PhasiRNA
-
Secondary small interfering RNAs generated from the AGO-microRNA-cleaved mRNAs or long non-coding RNAs. The production of phasiRNAs involves RDR6, SGS3 and DCLs.
- Polymerase backtracking
-
Reversible sliding of a polymerase along the DNA or RNA template.
- Selective sweeps
-
Genomic regions with reduced genetic variation because a linked beneficial mutation increases in frequency and becomes fixed in the population.
- Siren siRNAs
-
A small number of highly expressed RNA polymerase IV-dependent small interfering RNAs (siRNAs) that were first reported in the rice endosperm. Siren siRNAs are also identified in female gametophytes and the surrounding sporophytic tissue.
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Zhang, H., Zhu, JK. Epigenetic gene regulation in plants and its potential applications in crop improvement. Nat Rev Mol Cell Biol (2024). https://doi.org/10.1038/s41580-024-00769-1
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DOI: https://doi.org/10.1038/s41580-024-00769-1
