Imprinted expression of genes and small RNA is associated with localized hypomethylation of the maternal genome in rice endosperm

Rodrigues JA, Ruan R, Nishimura T, Sharma MK, Sharma R, Ronald PC, Fischer RL, ZILBERMAN D. 2013. Imprinted expression of genes and small RNA is associated with localized hypomethylation of the maternal genome in rice endosperm. Proceedings of the National Academy of Sciences. 110(19), 7934–7939.


Journal Article | Published | English

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Author
Rodrigues, Jessica A.; Ruan, Randy; Nishimura, Toshiro; Sharma, Manoj K.; Sharma, Rita; Ronald, Pamela C; Fischer, Robert L.; ZILBERMAN, DanielIST Austria
Department
Abstract
Arabidopsis thaliana endosperm, a transient tissue that nourishes the embryo, exhibits extensive localized DNA demethylation on maternally inherited chromosomes. Demethylation mediates parent-of-origin–specific (imprinted) gene expression but is apparently unnecessary for the extensive accumulation of maternally biased small RNA (sRNA) molecules detected in seeds. Endosperm DNA in the distantly related monocots rice and maize is likewise locally hypomethylated, but whether this hypomethylation is generally parent-of-origin specific is unknown. Imprinted expression of sRNA also remains uninvestigated in monocot seeds. Here, we report high-coverage sequencing of the Kitaake rice cultivar that enabled us to show that localized hypomethylation in rice endosperm occurs solely on the maternal genome, preferring regions of high DNA accessibility. Maternally expressed imprinted genes are enriched for hypomethylation at putative promoter regions and transcriptional termini and paternally expressed genes at promoters and gene bodies, mirroring our recent results in A. thaliana. However, unlike in A. thaliana, rice endosperm sRNA populations are dominated by specific strong sRNA-producing loci, and imprinted 24-nt sRNAs are expressed from both parental genomes and correlate with hypomethylation. Overlaps between imprinted sRNA loci and imprinted genes expressed from opposite alleles suggest that sRNAs may regulate genomic imprinting. Whereas sRNAs in seedling tissues primarily originate from small class II (cut-and-paste) transposable elements, those in endosperm are more uniformly derived, including sequences from other transposon classes, as well as genic and intergenic regions. Our data indicate that the endosperm exhibits a unique pattern of sRNA expression and suggest that localized hypomethylation of maternal endosperm DNA is conserved in flowering plants.
Publishing Year
Date Published
2013-05-07
Journal Title
Proceedings of the National Academy of Sciences
Volume
110
Issue
19
Page
7934-7939
ISSN
eISSN
IST-REx-ID

Cite this

Rodrigues JA, Ruan R, Nishimura T, et al. Imprinted expression of genes and small RNA is associated with localized hypomethylation of the maternal genome in rice endosperm. Proceedings of the National Academy of Sciences. 2013;110(19):7934-7939. doi:10.1073/pnas.1306164110
Rodrigues, J. A., Ruan, R., Nishimura, T., Sharma, M. K., Sharma, R., Ronald, P. C., … ZILBERMAN, D. (2013). Imprinted expression of genes and small RNA is associated with localized hypomethylation of the maternal genome in rice endosperm. Proceedings of the National Academy of Sciences. National Academy of Sciences. https://doi.org/10.1073/pnas.1306164110
Rodrigues, Jessica A., Randy Ruan, Toshiro Nishimura, Manoj K. Sharma, Rita Sharma, Pamela C Ronald, Robert L. Fischer, and Daniel ZILBERMAN. “Imprinted Expression of Genes and Small RNA Is Associated with Localized Hypomethylation of the Maternal Genome in Rice Endosperm.” Proceedings of the National Academy of Sciences. National Academy of Sciences, 2013. https://doi.org/10.1073/pnas.1306164110.
J. A. Rodrigues et al., “Imprinted expression of genes and small RNA is associated with localized hypomethylation of the maternal genome in rice endosperm,” Proceedings of the National Academy of Sciences, vol. 110, no. 19. National Academy of Sciences, pp. 7934–7939, 2013.
Rodrigues JA, Ruan R, Nishimura T, Sharma MK, Sharma R, Ronald PC, Fischer RL, ZILBERMAN D. 2013. Imprinted expression of genes and small RNA is associated with localized hypomethylation of the maternal genome in rice endosperm. Proceedings of the National Academy of Sciences. 110(19), 7934–7939.
Rodrigues, Jessica A., et al. “Imprinted Expression of Genes and Small RNA Is Associated with Localized Hypomethylation of the Maternal Genome in Rice Endosperm.” Proceedings of the National Academy of Sciences, vol. 110, no. 19, National Academy of Sciences, 2013, pp. 7934–39, doi:10.1073/pnas.1306164110.
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