Small RNA-mediated DNA methylation during plant reproduction

Chow, Hiu Tung; Mosher, Rebecca A.

doi:10.1093/plcell/koad010

Cited by 18 publications

(20 citation statements)

References 142 publications

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“…Along with DNA methylation, DNA demethylation pathway players, such as demethylase DME in Arabidopsis and ROS1a in rice central cells, were also implicated in imprinting across plants (Xiao et al, 2003; Gehring et al, 2006; Kim et al, 2019). One of the crucial players in plant epigenetics are sRNAs and their expression drastically increases in reproductive tissues (Chow and Mosher, 2023; Hari Sundar G et al, 2023). Unlike Arabidopsis , other dicots like B. rapa and Capsella RdDM mutants showed pollen and seed abnormalities (Mosher et al, 2009; Grover et al, 2018; Wang et al, 2020).…”

Section: Discussionmentioning

confidence: 99%

Upstream regulator of genomic imprinting in rice endosperm is a small RNA-associated chromatin remodeler

Pal,

Sundar G,

et al. 2023

Preprint

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Genomic imprinting is observed in endosperm, a placenta-like seed tissue, where transposable elements (TEs) and repeat-derived small(s)RNAs mediate epigenetic changes in plants. In imprinting, uniparental gene expression arises due to parent-specific epigenetic marks on one allele but not on the other. The importance of sRNAs and their regulation in endosperm development or in imprinting is poorly understood in crops. Here we show that a previously uncharacterized CLASSY (CLSY)-family chromatin remodeler named OsCLSY3 is essential for rice endosperm development and imprinting, acting as an upstream player in sRNA pathway. Comparative transcriptome and genetic analysis indicated its endosperm-preferred expression and its paternally imprinted nature. These important features were modulated by RNA-directed DNA methylation (RdDM) of tandemly arranged TEs in its promoter. Upon perturbation of OsCLSY3 in transgenic lines we observed defects in endosperm development and loss of around 70% of all sRNAs. Interestingly, well-conserved endosperm-specific sRNAs (siren) that are vital for reproductive fitness in angiosperms were dependent on OsCLSY3. We also observed many imprinted genes and seed development-associated genes under the control of CLSY3-dependent RdDM. These results support an essential role of OsCLSY3 in rice endosperm development and imprinting, and propose similar regulatory strategies involving CLSY3 homologs among other cereals.

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Section: Discussionmentioning

confidence: 99%

Upstream regulator of genomic imprinting in rice endosperm is a small RNA-associated chromatin remodeler

Pal,

Sundar G,

et al. 2023

Preprint

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“…While the rules governing such competition remain to be elucidated, presuming some CLSYs are preferred over others, it would add another dimension to their regulation of DNA methylation. Past studies already demonstrated that the CLSYs are differentially expressed during development and that they target Pol IV to distinct genomic targets 10,20 , resulting in tissue-specific methylation patterns and links between specific CLSYs and several epigenetically regulated traits 16,62 . Within this context, our discovery of a CLSY docking motif in Pol IV suggests a new layer of regulation that could control DNA methylation patterns: competition for binding to the Pol IV complex.…”

Section: Discussionmentioning

confidence: 99%

CLSY docking to Pol IV requires a conserved domain critical for small RNA biogenesis and transposon silencing

Felgines,

Rymen,

Martins

et al. 2023

Preprint

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Eukaryotes must balance the need for gene transcription by RNA polymerase II (Pol II) against the danger of mutations caused by transposable element (TE) proliferation. In plants, these gene expression and TE silencing activities are divided between different RNA polymerases. Specifically, RNA polymerase IV (Pol IV), which evolved from Pol II, transcribes TEs to generate small interfering RNAs (siRNAs) that guide DNA methylation and block TE transcription by Pol II. While the Pol IV complex is recruited to TEs via SNF2-like CLASSY (CLSY) proteins, how Pol IV partners with the CLSYs remains unknown. Here we identified a conserved CYC-YPMF motif that is specific to Pol IV and is positioned on the complex exterior. Furthermore, we found that this motif is essential for the co-purification of all four CLSYs with Pol IV, but that only one CLSY is present in any given Pol IV complex. These findings support a “one CLSY per Pol IV” model where the CYC-YPMF motif acts as a CLSY-docking site. Indeed, mutations in and around this motif phenocopypol ivnull mutants. Together, these findings provide structural and functional insights into a critical protein feature that distinguishes Pol IV from other RNA polymerases, allowing it to promote genome stability by targeting TEs for silencing.

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“…The abundance of 24-nt siRNA was related to the level of TE methylation in B. napus Plants achieve TE silencing and maintain genome stability through DNA methylation. The RdDM pathway acts primarily on TEs and is vital for methylation maintenance (Chow & Mosher, 2023), while siRNA is an essential component of the RdDM pathway. In order to further explore the influence of epigenetic modifications on TE methylation during allopolyploidization, we analyzed the regulatory role of the RdDM pathway in TE methylation in combination with small RNA data.…”

Section: Allopolyploidization Affected the Dna Methylation Level Of Tesmentioning

confidence: 99%

“…DNA methylation is conserved in the genome, and abnormal changes can cause developmental failure in plants and animals, as well as embryo lethality (Zhang et al., 2018). In plants, the RNA‐directed DNA methylation (RdDM) pathway mediates de novo DNA methylation, mainly acting on short TEs and DNA near TEs, and is involved in many biological functions such as pathogen defense, stress response, reproduction, and genome interaction (Burgess et al., 2022; Chow & Mosher, 2023; Matzke & Mosher, 2014; Zemach et al., 2013; Zhang et al., 2018). As a critical component of the RdDM pathway, 24‐nt siRNAs are the most abundant small RNA in plant genomes (Chow & Mosher, 2023), direct TE methylation to regulate gene expression, and control rice tillering and stress resistance (Sun et al., 2021; Xu et al., 2020).…”

Section: Introductionmentioning

confidence: 99%

“…In plants, the RNA‐directed DNA methylation (RdDM) pathway mediates de novo DNA methylation, mainly acting on short TEs and DNA near TEs, and is involved in many biological functions such as pathogen defense, stress response, reproduction, and genome interaction (Burgess et al., 2022; Chow & Mosher, 2023; Matzke & Mosher, 2014; Zemach et al., 2013; Zhang et al., 2018). As a critical component of the RdDM pathway, 24‐nt siRNAs are the most abundant small RNA in plant genomes (Chow & Mosher, 2023), direct TE methylation to regulate gene expression, and control rice tillering and stress resistance (Sun et al., 2021; Xu et al., 2020). The number of siRNAs originating from TEs increases during seed development in B. napus , promoting selective subgenome silencing (Ziegler et al., 2023).…”

Section: Introductionmentioning

confidence: 99%

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Genomic asymmetric epigenetic modification of transposable elements is involved in gene expression regulation of allopolyploid Brassica napus

Xiao,

Xi,

Wang

et al. 2023

The Plant Journal

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SUMMARYPolyploids are common and have a wide geographical distribution and environmental adaptability. Allopolyploidy may lead to the activation of transposable elements (TE). However, the mechanism of epigenetic modification of TEs in the establishment and evolution of allopolyploids remains to be explored. We focused on the TEs of model allopolyploid Brassica napus (AnAnCnCn), exploring the TE characteristics of the genome, epigenetic modifications of TEs during allopolyploidization, and regulation of gene expression by TE methylation. In B. napus, approximately 50% of the genome was composed of TEs. TEs increased with proximity to genes, especially DNA transposons. TE methylation levels were negatively correlated with gene expression, and changes in TE methylation levels were able to regulate the expression of neighboring genes related to responses to light intensity and stress, which promoted powerful adaptation of allopolyploids to new environments. TEs can be synergistically regulated by RNA‐directed DNA methylation pathways and histone modifications. The epigenetic modification levels of TEs tended to be similar to those of the diploid parents during the genome evolution of B. napus. The TEs of the An subgenome were more likely to be modified, and the imbalance in TE number and epigenetic modification level in the An and Cn subgenomes may lead to the establishment of subgenome dominance. Our study analyzed the characteristics of TE location, DNA methylation, siRNA, and histone modification in B. napus and highlighted the importance of TE epigenetic modifications during the allopolyploidy process, providing support for revealing the mechanism of allopolyploid formation and evolution.

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Small RNA-mediated DNA methylation during plant reproduction

Cited by 18 publications

References 142 publications

Upstream regulator of genomic imprinting in rice endosperm is a small RNA-associated chromatin remodeler

Upstream regulator of genomic imprinting in rice endosperm is a small RNA-associated chromatin remodeler

CLSY docking to Pol IV requires a conserved domain critical for small RNA biogenesis and transposon silencing

Genomic asymmetric epigenetic modification of transposable elements is involved in gene expression regulation of allopolyploid Brassica napus

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