Chromatin Regulates Bipartite-Classified Small RNA Expression to Maintain Epigenome Homeostasis in Arabidopsis

Papareddy, Ranjith; Páldi, Katalin; Paulraj, Subramanian; Kao, Ping; Nodine, Michael D.

doi:10.1101/2020.05.04.076885

Cited by 4 publications

(4 citation statements)

References 112 publications

(157 reference statements)

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“…2 b), suggesting that euchromatic embryo hypermethylation might be common among plants. Recent work demonstrates that Arabidopsis heterochromatin is decondensed and produces abundant 24-nt siRNAs during embryogenesis [ 43 ], providing an opportunity for the RdDM machinery to access this chromatin for hypermethylation.…”

Section: Discussionmentioning

confidence: 99%

Embryo CHH hypermethylation is mediated by RdDM and is autonomously directed in Brassica rapa

et al. 2021

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Background RNA-directed DNA methylation (RdDM) initiates cytosine methylation in all contexts and maintains asymmetric CHH methylation. Mature plant embryos show one of the highest levels of CHH methylation, and it has been suggested that RdDM is responsible for this hypermethylation. Because loss of RdDM in Brassica rapa causes seed abortion, embryo methylation might play a role in seed development. RdDM is required in the maternal sporophyte, suggesting that small RNAs from the maternal sporophyte might translocate to the developing embryo, triggering DNA methylation that prevents seed abortion. This raises the question of whether embryo hypermethylation is autonomously regulated by the embryo itself or influenced by the maternal sporophyte. Results Here, we demonstrate that B. rapa embryos are hypermethylated in both euchromatin and heterochromatin and that this process requires RdDM. Contrary to the current models, B. rapa embryo hypermethylation is not correlated with demethylation of the endosperm. We also show that maternal somatic RdDM is not sufficient for global embryo hypermethylation, and we find no compelling evidence for maternal somatic influence over embryo methylation at any locus. Decoupling of maternal and zygotic RdDM leads to successful seed development despite the loss of embryo CHH hypermethylation. Conclusions We conclude that embryo CHH hypermethylation is conserved, autonomously controlled, and not required for embryo development. Furthermore, maternal somatic RdDM, while required for seed development, does not directly influence embryo methylation patterns.

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Section: Discussionmentioning

confidence: 99%

Embryo CHH hypermethylation is mediated by RdDM and is autonomously directed in Brassica rapa

et al. 2021

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“…In B. rapa, we detect hypermethylation in both heterochromatin and euchromatin ( Figure 2B), suggesting that euchromatic embryo hypermethylation might be common among plants. Recent work demonstrates that Arabidopsis heterochromatin is decondensed and produces abundant 24-nt siRNAs during embryogenesis [42], providing an opportunity for the RdDM machinery to access this chromatin for hypermethylation.…”

Section: Discussionmentioning

confidence: 99%

Embryo CHH hypermethylation is mediated by RdDM and is autonomously directed inBrassica rapa

Chakraborty

Kendall

Grover

et al. 2020

Preprint

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Background: RNA directed DNA methylation (RdDM) initiates cytosine methylation in all contexts, and maintains asymmetric CHH methylation (where H is any base other than G). Mature plant embryos show one of the highest levels of CHH methylation, and it has been suggested that RdDM is responsible for this hypermethylation. Because loss of RdDM in Brassica rapa causes seed abortion, embryo methylation might play a role in seed development. RdDM is required in the maternal sporophyte, suggesting that small RNAs from the maternal sporophyte might translocate to the developing embryo, triggering DNA methylation that prevents seed abortion. This raises the question whether embryo hypermethylation is autonomously regulated by the embryo itself or influenced by the maternal sporophyte. Results: Here, we demonstrate that B. rapa embryos are hypermethylated in both euchromatin and heterochromatin and that this process requires RdDM. Contrary to current models, B. rapa embryo hypermethylation is not correlated with demethylation of the endosperm. We also show that maternal somatic RdDM is not sufficient for global embryo hypermethylation, and we find no compelling evidence for maternal somatic influence over embryo methylation at any locus. Decoupling of maternal and zygotic RdDM leads to successful seed development despite loss of embryo CHH hypermethylation. Conclusions: We conclude that embryo CHH hypermethylation is conserved, autonomously controlled, and not required for embryo development. Furthermore, maternal somatic RdDM, while required for seed development, does not directly influence embryo methylation patterns.

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“…It has been proposed that such abundance is associated with epigenetic safeguard mechanisms for controlling the expression of transposons and heterochromatic repeats during embryo development [16,20]. A recent study [21] showed that siRNAs generated from transposable elements (TEs), highly numerous in Arabidopsis embryos and typically 24-nt long, originate both from euchromatic TEs, being required not only during embryogenesis as a way of silencing TEs, but also from heterochromatic TEs specifically required during embryogenesis to help establish TE methylation de novo, which is then maintained during post-embryogenesis independently of siRNAs.…”

Section: Small Rna Expression Profiles In Embryonic Tissuesmentioning

confidence: 99%

“…Such as for the Arabidopsis model system, most frequently used for better understanding the regulation of SE, many differentially expressed miRNAs have also been identified in other embryogenic cultures of different gymnosperms [18], mono-and dicotyledonous plants [15,21,26,27]. From these studies, a large number of miRNAs has been associated with SE target genes related to auxin perception, signaling and biosynthesis, as presented in Figure 1.…”

Section: Auxins and Mirna-arf Interactionsmentioning

confidence: 99%

Small Non-Coding RNAs at the Crossroads of Regulatory Pathways Controlling Somatic Embryogenesis in Seed Plants

Alves

Cordeiro

Correia

et al. 2021

Plants

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Small non-coding RNAs (sncRNAs) are molecules with important regulatory functions during development and environmental responses across all groups of terrestrial plants. In seed plants, the development of a mature embryo from the zygote follows a synchronized cell division sequence, and growth and differentiation events regulated by highly regulated gene expression. However, given the distinct features of the initial stages of embryogenesis in gymnosperms and angiosperms, it is relevant to investigate to what extent such differences emerge from differential regulation mediated by sncRNAs. Within these, the microRNAs (miRNAs) are the best characterized class, and while many miRNAs are conserved and significantly represented across angiosperms and other seed plants during embryogenesis, some miRNA families are specific to some plant lineages. Being a model to study zygotic embryogenesis and a relevant biotechnological tool, we systematized the current knowledge on the presence and characterization of miRNAs in somatic embryogenesis (SE) of seed plants, pinpointing the miRNAs that have been reported to be associated with SE in angiosperm and gymnosperm species. We start by conducting an overview of sncRNA expression profiles in the embryonic tissues of seed plants. We then highlight the miRNAs described as being involved in the different stages of the SE process, from its induction to the full maturation of the somatic embryos, adding references to zygotic embryogenesis when relevant, as a contribution towards a better understanding of miRNA-mediated regulation of SE.

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Chromatin Regulates Bipartite-Classified Small RNA Expression to Maintain Epigenome Homeostasis in Arabidopsis

Cited by 4 publications

References 112 publications

Embryo CHH hypermethylation is mediated by RdDM and is autonomously directed in Brassica rapa

Embryo CHH hypermethylation is mediated by RdDM and is autonomously directed in Brassica rapa

Embryo CHH hypermethylation is mediated by RdDM and is autonomously directed inBrassica rapa

Small Non-Coding RNAs at the Crossroads of Regulatory Pathways Controlling Somatic Embryogenesis in Seed Plants

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