DNA demethylases remodel DNA methylation in rice gametes and zygote and are required for reproduction

Zhou, Shaoli; Xue, Lijun; Liu, Qian; Zhao, Yu; Jiang, Wei; Wu, Anqi; Zhou, Dao‐Xiu

doi:10.1016/j.molp.2021.06.006

Cited by 38 publications

(53 citation statements)

References 72 publications

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“…Newly detected zygote siRNAs mark future CHH hypermethylation sites in mature embryos Hypermethylation of embryo has been reported in a number of angiosperm species, including Arabidopsis, soybean, chickpea, Brassica rapa, and rice (Bouyer et al, 2017;Chakraborty et al, 2020;Kawakatsu et al, 2017;Li et al, 2020b;Lin et al, 2017;Rajkumar et al, 2020;Zhou et al, 2021). We found that newly detected siRNA loci have abundant CHH methylation in embryos that is dependent on the RdDM methyltransferase DRM2 (Fig 5C).…”

Section: A Special Class Of Highly Abundant Maternal Sirnas Persists In the Zygotesupporting

confidence: 54%

Resetting of the 24-nt siRNA landscape in rice zygotes

Li¹,

Gent

et al. 2020

Preprint

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The zygote, a totipotent stem cell, constitutes a critical stage of the life cycle for all sexually reproducing organisms. It is produced by fusion of two differentiated cells, egg and sperm, that in plants have radically different siRNA transcriptomes from each other and from multicellular embryos. Here we examined the small RNA transcriptome of unicellular rice zygotes. We find that the overall 24-nt siRNA landscape in the zygote resembles that of the unfertilized egg cell, consistent with maternal carry-over. A large fraction (∼75%) of the siRNAs in the zygote arise from a small proportion (∼2%) of siRNA loci, which corresponded to similar loci in the egg cell and ovary. However, these highly expressing loci were distinct from endosperm siren loci that were detected in later stage endosperm. miRNA abundances changed rapidly after fertilization, resulting in a miRNA profile distinct from the egg cell. Notably, the de novo 24-nt siRNAs expressed by the zygote had characteristics of canonical siRNAs, such as proximity to genes and tendency to overlap TIR DNA transposable elements, and resembled seedling siRNA loci, indicating a return to the canonical siRNA profile typical of vegetative tissues. Taken together, our results suggest that resetting of the gametic epigenome towards the canonical vegetative profile is initiated before the first embryonic division.

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Section: A Special Class Of Highly Abundant Maternal Sirnas Persists In the Zygotesupporting

confidence: 54%

Resetting of the 24-nt siRNA landscape in rice zygotes

Li¹,

Gent

et al. 2020

Preprint

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“…In Arabidopsis and rice, loss of DME function leads to seed abortion [5,14,39]. Here we found that the kernels of the zmros1ab double mutants are viable, and the double mutant gamete was transmitted at the expected ratio in the self-pollinated ear of the zmros1a/+;zmros1b/+ plants.…”

Section: The Hypomethylation In Maize Endosperm Requires Zmros1abmentioning

confidence: 75%

DNA demethylation affects imprinted gene expression in maize endosperm

Luo

et al. 2022

Genome Biol

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Background DNA demethylation occurs in many species and is involved in diverse biological processes. However, the occurrence and role of DNA demethylation in maize remain unknown. Results We analyze loss-of-function mutants of two major genes encoding DNA demethylases. No significant change in DNA methylation has been detected in these mutants. However, we detect increased DNA methylation levels in the mutants around genes and some transposons. The increase in DNA methylation is accompanied by alteration in gene expression, with a tendency to show downregulation, especially for the genes that are preferentially expressed in endosperm. Imprinted expression of both maternally and paternally expressed genes changes in F1 hybrid with the mutant as female and the wild-type as male parental line, but not in the reciprocal hybrid. This alteration in gene expression is accompanied by allele-specific DNA methylation differences, suggesting that removal of DNA methylation of the maternal allele is required for the proper expression of these imprinted genes. Finally, we demonstrate that hypermethylation in the double mutant is associated with reduced binding of transcription factor to its target, and altered gene expression. Conclusions Our results suggest that active removal of DNA methylation is important for transcription factor binding and proper gene expression in maize endosperm.

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“…Interestingly, the expression of ROS1C / DNG701 and ROS1D / DNG704 was suppressed, whereas that of ROS1A / DNG702 was increased. These three genes were recently reported to demethylate DNA in the gamete and zygote, which is crucial for zygote gene expression and development ( Zhou et al, 2021b ). In addition, a mutation in ROS1A / DNG702 can generally lead to the increase of CG and CHG but not of CHH hypermethylation on genomes of rice endosperms ( Liu J. et al, 2018 ).…”

Section: Resultsmentioning

confidence: 99%

CG and CHG Methylation Contribute to the Transcriptional Control of OsPRR37-Output Genes in Rice

Liu

et al. 2022

Front. Plant Sci.

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Plant circadian clock coordinates endogenous transcriptional rhythms with diurnal changes of environmental cues. OsPRR37, a negative component in the rice circadian clock, reportedly regulates transcriptome rhythms, and agronomically important traits. However, the underlying regulatory mechanisms of OsPRR37-output genes remain largely unknown. In this study, whole genome bisulfite sequencing and high-throughput RNA sequencing were applied to verify the role of DNA methylation in the transcriptional control of OsPRR37-output genes. We found that the overexpression of OsPRR37 suppressed rice growth and altered cytosine methylations in CG and CHG sequence contexts in but not the CHH context (H represents A, T, or C). In total, 35 overlapping genes were identified, and 25 of them showed negative correlation between the methylation level and gene expression. The promoter of the hexokinase gene OsHXK1 was hypomethylated at both CG and CHG sites, and the expression of OsHXK1 was significantly increased. Meanwhile, the leaf starch content was consistently lower in OsPRR37 overexpression lines than in the recipient parent Guangluai 4. Further analysis with published data of time-course transcriptomes revealed that most overlapping genes showed peak expression phases from dusk to dawn. The genes involved in DNA methylation, methylation maintenance, and DNA demethylation were found to be actively expressed around dusk. A DNA glycosylase, namely ROS1A/DNG702, was probably the upstream candidate that demethylated the promoter of OsHXK1. Taken together, our results revealed that CG and CHG methylation contribute to the transcriptional regulation of OsPRR37-output genes, and hypomethylation of OsHXK1 leads to decreased starch content and reduced plant growth in rice.

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DNA demethylases remodel DNA methylation in rice gametes and zygote and are required for reproduction

Cited by 38 publications

References 72 publications

Resetting of the 24-nt siRNA landscape in rice zygotes

Resetting of the 24-nt siRNA landscape in rice zygotes

DNA demethylation affects imprinted gene expression in maize endosperm

CG and CHG Methylation Contribute to the Transcriptional Control of OsPRR37-Output Genes in Rice

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