Divergence among rice cultivars reveals roles for transposition and epimutation in ongoing evolution of genomic imprinting

Rodrigues JA, Hsieh P-H, Ruan D, Nishimura T, Sharma MK, Sharma R, Ye X, Nguyen ND, Nijjar S, Ronald PC, Fischer RL, ZILBERMAN D. 2021. Divergence among rice cultivars reveals roles for transposition and epimutation in ongoing evolution of genomic imprinting. Proceedings of the National Academy of Sciences. 118(29), e2104445118.

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Author
Rodrigues, Jessica A.; Hsieh, Ping-Hung; Ruan, Deling; Nishimura, Toshiro; Sharma, Manoj K.; Sharma, Rita; Ye, XinYi; Nguyen, Nicholas D.; Nijjar, Sukhranjan; Ronald, Pamela C.; Fischer, Robert L.; ZILBERMAN, DanielIST Austria
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Abstract
Parent-of-origin–dependent gene expression in mammals and flowering plants results from differing chromatin imprints (genomic imprinting) between maternally and paternally inherited alleles. Imprinted gene expression in the endosperm of seeds is associated with localized hypomethylation of maternally but not paternally inherited DNA, with certain small RNAs also displaying parent-of-origin–specific expression. To understand the evolution of imprinting mechanisms in Oryza sativa (rice), we analyzed imprinting divergence among four cultivars that span both japonica and indica subspecies: Nipponbare, Kitaake, 93-11, and IR64. Most imprinted genes are imprinted across cultivars and enriched for functions in chromatin and transcriptional regulation, development, and signaling. However, 4 to 11% of imprinted genes display divergent imprinting. Analyses of DNA methylation and small RNAs revealed that endosperm-specific 24-nt small RNA–producing loci show weak RNA-directed DNA methylation, frequently overlap genes, and are imprinted four times more often than genes. However, imprinting divergence most often correlated with local DNA methylation epimutations (9 of 17 assessable loci), which were largely stable within subspecies. Small insertion/deletion events and transposable element insertions accompanied 4 of the 9 locally epimutated loci and associated with imprinting divergence at another 4 of the remaining 8 loci. Correlating epigenetic and genetic variation occurred at key regulatory regions—the promoter and transcription start site of maternally biased genes, and the promoter and gene body of paternally biased genes. Our results reinforce models for the role of maternal-specific DNA hypomethylation in imprinting of both maternally and paternally biased genes, and highlight the role of transposition and epimutation in rice imprinting evolution.
Publishing Year
Date Published
2021-07-16
Journal Title
Proceedings of the National Academy of Sciences
Acknowledgement
We thank W. Schackwitz, M. Joel, and the Joint Genome Institute sequencing team for generating the IR64 genome sequence and initial analysis; L. Bartley and E. Marvinney for genomic DNA preparation for IR64 resequencing; and the University of California (UC), Berkeley Sanger sequencing team for technical advice and service. This work was partially funded by NSF Grant IOS-1025890 (to R.L.F. and D.Z.), NIH Grant GM69415 (to R.L.F. and D.Z.), NIH Grant GM122968 (to P.C.R.), a Young Investigator Grant from the Arnold and Mabel Beckman Foundation (to D.Z.), an International Fulbright Science and Technology Award (to J.A.R.), and a Taiwan Ministry of Education Studying Abroad Scholarship (to P.-H.H.). This work used the Vincent J. Coates Genomics Sequencing Laboratory at UC Berkeley, supported by NIH Instrumentation Grant S10 OD018174.
Volume
118
Issue
29
Article Number
e2104445118
ISSN
eISSN
IST-REx-ID

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Rodrigues JA, Hsieh P-H, Ruan D, et al. Divergence among rice cultivars reveals roles for transposition and epimutation in ongoing evolution of genomic imprinting. Proceedings of the National Academy of Sciences. 2021;118(29). doi:10.1073/pnas.2104445118
Rodrigues, J. A., Hsieh, P.-H., Ruan, D., Nishimura, T., Sharma, M. K., Sharma, R., … ZILBERMAN, D. (2021). Divergence among rice cultivars reveals roles for transposition and epimutation in ongoing evolution of genomic imprinting. Proceedings of the National Academy of Sciences. National Academy of Sciences. https://doi.org/10.1073/pnas.2104445118
Rodrigues, Jessica A., Ping-Hung Hsieh, Deling Ruan, Toshiro Nishimura, Manoj K. Sharma, Rita Sharma, XinYi Ye, et al. “Divergence among Rice Cultivars Reveals Roles for Transposition and Epimutation in Ongoing Evolution of Genomic Imprinting.” Proceedings of the National Academy of Sciences. National Academy of Sciences, 2021. https://doi.org/10.1073/pnas.2104445118.
J. A. Rodrigues et al., “Divergence among rice cultivars reveals roles for transposition and epimutation in ongoing evolution of genomic imprinting,” Proceedings of the National Academy of Sciences, vol. 118, no. 29. National Academy of Sciences, 2021.
Rodrigues JA, Hsieh P-H, Ruan D, Nishimura T, Sharma MK, Sharma R, Ye X, Nguyen ND, Nijjar S, Ronald PC, Fischer RL, ZILBERMAN D. 2021. Divergence among rice cultivars reveals roles for transposition and epimutation in ongoing evolution of genomic imprinting. Proceedings of the National Academy of Sciences. 118(29), e2104445118.
Rodrigues, Jessica A., et al. “Divergence among Rice Cultivars Reveals Roles for Transposition and Epimutation in Ongoing Evolution of Genomic Imprinting.” Proceedings of the National Academy of Sciences, vol. 118, no. 29, e2104445118, National Academy of Sciences, 2021, doi:10.1073/pnas.2104445118.
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