Characterization of Imprinted Genes in Rice Reveals Conservation of Regulation and Imprinting with Other Plant Species

Overview

Journal Plant Physiol

Specialty Physiology

Date 2018 Jun 20

PMID 29914891

Citations 27

Authors

Chen Chen

Tingting Li

Shan Zhu

Zehou Liu

Zhenyuan Shi

Xiaoming Zheng

Rui Chen

Jianfeng Huang

Yi Shen

Shiyou Luo

Lei Wang

Qiao-Quan Liu

Zhiguo E

Affiliations

Soon will be listed here.

Abstract

Genomic imprinting is an epigenetic phenomenon by which certain genes display differential expression in a parent-of-origin-dependent manner. Hundreds of imprinted genes have been identified from several plant species. Here, we identified, with a high level of confidence, 208 imprinted gene candidates from rice (). Imprinted genes of rice showed limited association with the transposable elements, which contrasts with findings from Arabidopsis (). Generally, imprinting in rice is conserved within a species, but intraspecific variation also was detected. The imprinted rice genes do not show signatures of selection, which suggests that domestication has had a limited evolutionary consequence on genomic imprinting. Although conservation of imprinting in plants is limited, we show that some loci are imprinted in several different species. Moreover, our results suggest that different types of epigenetic regulation can be established either before or after fertilization. Imprinted 24-nucleotide small RNAs and their neighboring genes tend to express alleles from different parents. This association was not observed between 21-nucleotide small RNAs and their neighboring genes. Together, our findings suggest that the regulation of imprinting can be diverse, and genomic imprinting has evolutionary and biological significance.

Citing Articles

Maternally expressed FERTILIZATION-INDEPENDENT ENDOSPERM1 regulates seed dormancy and aleurone development in rice.

Cheng X, Zhang S, E Z, Yang Z, Cao S, Zhang R Plant Cell. 2024; 37(1).

PMID: 39549266 PMC: 11663568. DOI: 10.1093/plcell/koae304.

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

Pal A, Gandhivel V, Nambiar A, Shivaprasad P Nat Commun. 2024; 15(1):7807.

PMID: 39242590 PMC: 11379814. DOI: 10.1038/s41467-024-52239-z.

Multilayered epigenetic control of persistent and stage-specific imprinted genes in rice endosperm.

Tonosaki K, Susaki D, Morinaka H, Ono A, Nagata H, Furuumi H Nat Plants. 2024; 10(8):1231-1245.

PMID: 39080502 DOI: 10.1038/s41477-024-01754-4.

Parental dialectic: Epigenetic conversations in endosperm.

Khouider S, Gehring M Curr Opin Plant Biol. 2024; 81:102591.

PMID: 38944896 PMC: 11392645. DOI: 10.1016/j.pbi.2024.102591.

The transcriptome landscape of developing barley seeds.

Kovacik M, Nowicka A, Zwyrtkova J, Strejckova B, Vardanega I, Esteban E Plant Cell. 2024; 36(7):2512-2530.

PMID: 38635902 PMC: 11218782. DOI: 10.1093/plcell/koae095.

References

Huang X, Kurata N, Wei X, Wang Z, Wang A, Zhao Q . A map of rice genome variation reveals the origin of cultivated rice. Nature. 2012; 490(7421):497-501. PMC: 7518720. DOI: 10.1038/nature11532. View

Schoft V, Chumak N, Choi Y, Hannon M, Garcia-Aguilar M, Machlicova A . Function of the DEMETER DNA glycosylase in the Arabidopsis thaliana male gametophyte. Proc Natl Acad Sci U S A. 2011; 108(19):8042-7. PMC: 3093457. DOI: 10.1073/pnas.1105117108. View

Xu X, Liu X, Ge S, Jensen J, Hu F, Li X . Resequencing 50 accessions of cultivated and wild rice yields markers for identifying agronomically important genes. Nat Biotechnol. 2011; 30(1):105-11. DOI: 10.1038/nbt.2050. View

Vu T, Nakamura M, Calarco J, Susaki D, Lim P, Kinoshita T . RNA-directed DNA methylation regulates parental genomic imprinting at several loci in Arabidopsis. Development. 2013; 140(14):2953-60. PMC: 3879202. DOI: 10.1242/dev.092981. View

Zhang H, Liang W, Yang X, Luo X, Jiang N, Ma H . Carbon starved anther encodes a MYB domain protein that regulates sugar partitioning required for rice pollen development. Plant Cell. 2010; 22(3):672-89. PMC: 2861464. DOI: 10.1105/tpc.109.073668. View

Zemach A, Kim M, Silva P, Rodrigues J, Dotson B, Brooks M . Local DNA hypomethylation activates genes in rice endosperm. Proc Natl Acad Sci U S A. 2010; 107(43):18729-34. PMC: 2972920. DOI: 10.1073/pnas.1009695107. View

Hatorangan M, Laenen B, Steige K, Slotte T, Kohler C . Rapid Evolution of Genomic Imprinting in Two Species of the Brassicaceae. Plant Cell. 2016; 28(8):1815-27. PMC: 5006707. DOI: 10.1105/tpc.16.00304. View

Shirzadi R, Andersen E, Bjerkan K, Gloeckle B, Heese M, Ungru A . Genome-wide transcript profiling of endosperm without paternal contribution identifies parent-of-origin-dependent regulation of AGAMOUS-LIKE36. PLoS Genet. 2011; 7(2):e1001303. PMC: 3040660. DOI: 10.1371/journal.pgen.1001303. View

Raissig M, Bemer M, Baroux C, Grossniklaus U . Genomic imprinting in the Arabidopsis embryo is partly regulated by PRC2. PLoS Genet. 2013; 9(12):e1003862. PMC: 3854695. DOI: 10.1371/journal.pgen.1003862. View

10.

Coppe A, Danieli G, Bortoluzzi S . REEF: searching REgionally Enriched Features in genomes. BMC Bioinformatics. 2006; 7:453. PMC: 1624853. DOI: 10.1186/1471-2105-7-453. View

11.

Song X, Huang W, Shi M, Zhu M, Lin H . A QTL for rice grain width and weight encodes a previously unknown RING-type E3 ubiquitin ligase. Nat Genet. 2007; 39(5):623-30. DOI: 10.1038/ng2014. View

12.

Yang B, Sugio A, White F . Os8N3 is a host disease-susceptibility gene for bacterial blight of rice. Proc Natl Acad Sci U S A. 2006; 103(27):10503-10508. PMC: 1502487. DOI: 10.1073/pnas.0604088103. View

13.

Huh J, Bauer M, Hsieh T, Fischer R . Cellular programming of plant gene imprinting. Cell. 2008; 132(5):735-44. DOI: 10.1016/j.cell.2008.02.018. View

14.

Zhang M, Xie S, Dong X, Zhao X, Zeng B, Chen J . Genome-wide high resolution parental-specific DNA and histone methylation maps uncover patterns of imprinting regulation in maize. Genome Res. 2013; 24(1):167-76. PMC: 3875858. DOI: 10.1101/gr.155879.113. View

15.

Bernardi J, Lanubile A, Li Q, Kumar D, Kladnik A, Cook S . Impaired auxin biosynthesis in the defective endosperm18 mutant is due to mutational loss of expression in the ZmYuc1 gene encoding endosperm-specific YUCCA1 protein in maize. Plant Physiol. 2012; 160(3):1318-28. PMC: 3490580. DOI: 10.1104/pp.112.204743. View

16.

Waters A, Makarevitch I, Eichten S, Swanson-Wagner R, Yeh C, Xu W . Parent-of-origin effects on gene expression and DNA methylation in the maize endosperm. Plant Cell. 2011; 23(12):4221-33. PMC: 3269861. DOI: 10.1105/tpc.111.092668. View

17.

Luo M, Taylor J, Spriggs A, Zhang H, Wu X, Russell S . A genome-wide survey of imprinted genes in rice seeds reveals imprinting primarily occurs in the endosperm. PLoS Genet. 2011; 7(6):e1002125. PMC: 3121744. DOI: 10.1371/journal.pgen.1002125. View

18.

Yuan J, Chen S, Jiao W, Wang L, Wang L, Ye W . Both maternally and paternally imprinted genes regulate seed development in rice. New Phytol. 2017; 216(2):373-387. DOI: 10.1111/nph.14510. View

19.

Xin M, Yang R, Li G, Chen H, Laurie J, Ma C . Dynamic expression of imprinted genes associates with maternally controlled nutrient allocation during maize endosperm development. Plant Cell. 2013; 25(9):3212-27. PMC: 3809528. DOI: 10.1105/tpc.113.115592. View

20.

Gehring M, Huh J, Hsieh T, Penterman J, Choi Y, Harada J . DEMETER DNA glycosylase establishes MEDEA polycomb gene self-imprinting by allele-specific demethylation. Cell. 2006; 124(3):495-506. PMC: 4106368. DOI: 10.1016/j.cell.2005.12.034. View