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Quantitative RNA pseudouridine maps reveal multilayered translation control through plant rRNA, tRNA and mRNA pseudouridylation

Nature Plants volume 11, pages 234–247 (2025)Cite this article

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Abstract

Pseudouridine (Ψ) is the most abundant RNA modification, yet studies of Ψ have been hindered by a lack of robust methods to profile comprehensive Ψ maps. Here we utilize bisulfite-induced deletion sequencing to generate transcriptome-wide Ψ maps at single-base resolution across various plant species. Integrating ribosomal RNA, transfer RNA and messenger RNA Ψ stoichiometry with mRNA abundance and polysome profiling data, we uncover a multilayered regulation of translation efficiency through Ψ modifications. rRNA pseudouridylation could globally control translation, although the effects vary at different rRNA Ψ sites. Ψ in the tRNA T-arm loop shows strong positive correlations between Ψ stoichiometry and the translation efficiency of their respective codons. We observed a general inverse correlation between Ψ level and mRNA stability, but a positive correlation with translation efficiency in Arabidopsis seedlings. In conclusion, our study provides critical resources for Ψ research in plants and proposes prevalent translation regulation through rRNA, tRNA and mRNA pseudouridylation.

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Fig. 1: BID-seq reveals evolutionarily conserved pseudouridylation in rRNA across monocots and dicots.
Fig. 2: Ψ stoichiometries on rRNA modification sites affect translation across different tissues.
Fig. 3: Ψ stoichiometries on tRNA affect translation across different plant tissues.
Fig. 4: BID-seq identifies abundant mRNA Ψ sites across different plant species.
Fig. 5: Comprehensive base-resolution maps of mRNA Ψ sites in rice and Arabidopsis.
Fig. 6: Ψ modifications affect mRNA stability and translation in Arabidopsis seedlings.

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Data availability

All data supporting the findings of this study are available in the main text or the Supplementary tables. The BID-seq and RNA-seq data reported in this study have been deposited in the Gene Expression Omnibus database (https://www.ncbi.nlm.nih.gov/geo) under accession numbers GSE262373, GSE262374, GSE262375, GSE262376, GSE277198 and GSE277201. Source data are provided with this paper.

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Acknowledgements

We thank the Margot and Tomas Pritzker Family Foundation for the Pritzker Plant Biology Center at the University of Chicago, and the Bill & Melinda Gates Agricultural Innovations (Gates Ag One). C.H. is an investigator of the Howard Hughes Medical Institute.

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Author notes

  1. These authors contributed equally: Haoxuan Li, Guanqun Wang, Chang Ye.

Authors and Affiliations

  1. Department of Chemistry, Department of Biochemistry and Molecular Biology, and Institute for Biophysical Dynamics, The University of Chicago, Chicago, IL, USA

    Haoxuan Li, Guanqun Wang, Chang Ye, Zhongyu Zou, Bochen Jiang, Fan Yang, Kayla He, Chengwei Ju, Lisheng Zhang, Boyang Gao, Shun Liu, Yanming Chen & Chuan He

  2. Howard Hughes Medical Institute, Chicago, IL, USA

    Haoxuan Li, Guanqun Wang, Chang Ye, Zhongyu Zou & Chuan He

  3. Department of Biology, Hong Kong Baptist University and School of Life Sciences and State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong, Hong Kong, China

    Guanqun Wang & Jianhua Zhang

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Contributions

C.H., H.L., G.W. and C.Y. conceived the original idea and project. H.L. and G.W. performed the experiments. H.L. and C.Y. analysed the data. C.H. oversaw the study. G.W., H.L., C.Y. and C.H. wrote the paper. Z.Z., B.J., F.Y., K.H., C.J., L.Z., B.G., S.L., Y.C. and J.Z. participated in experiment design and discussions. All authors approved the paper.

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Correspondence to Chuan He.

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Competing interests

The authors have filed a provision patent application of the method reported in this paper through the University of Chicago. C.H. is a scientific founder, a member of the scientific advisory board and equity holder of Aferna Bio and Ellis Bio, a scientific cofounder and equity holder of Accent Therapeutics, and a member of the scientific advisory board of Rona Therapeutics and Element Biosciences. The other authors declare no competing interests.

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Extended data

Extended Data Fig. 1 The rRNA Ψ sites in the rRNAs of nuclear 18S, nuclear 5.8S and nuclear 25S identified in Arabidopsis using BID-seq.

The Ψ sites were accurately marked and compared with previously published sites. Yellow color marks the Ψ sites identified by BID-seq only; Grey color marks the Ψ sites only previously published, but not identified in this study; Blue color marks the Ψ sites that not only identified in this study but reported previously.

Extended Data Fig. 2 The conserved Ψ sites in the rRNAs of nuclear 18S, nuclear 5.8S and nuclear 25S in rice and Arabidopsis.

The Ψ sites were accurately marked and compared with previously published sites. Yellow color marks the Ψ sites only in rice. Blue color marks the Ψ sites conserved in both rice and Arabidopsis.

Extended Data Fig. 3 The conserved Ψ sites in the rRNA of nuclear 18S, nuclear 5.8S and nuclear 25S in maize and Arabidopsis.

The Ψ sites were accurately marked and compared with previously published sites. Yellow color marks the Ψ sites only in maize. Blue color marks the Ψ sites conserved in both maize and Arabidopsis.

Extended Data Fig. 4 The conserved Ψ sites in the rRNAs of nuclear 18S, nuclear 5.8S and nuclear 25S in soybean and Arabidopsis.

The Ψ sites were accurately marked and compared with previously published sites. Yellow color marks the Ψ sites only in soybean. Blue color marks the Ψ sites conserved in both soybean and Arabidopsis.

Extended Data Fig. 5 rRNA sequence conservation and rRNA Ψ sites among plant species and mammals.

a, The number of total- and conserved Ψ sites in rRNAs of nuclear 18S, nuclear 5.8S, nuclear 25S, chloroplast 23S, and mitochondria 26S identified in the four plants. b, c, The mutation types of the ossvr1 and osrlua3 mutant lines, in the background of ZH11 using CRISPR-Cas9. d, Diagram comparing the rRNA sequence conservation and Ψ sites for nuclear encoded 18S, 5.8S and 25S/28S rRNAs in four plant species as well as mouse and human. The yellow to purple colors represent the rRNA sequence conservation scores ranging from low to high. Each spot represents a rRNA Ψ site in different species. The Ψ site numbers are labeled along with the species names. Number in red color stands for the number of Ψ sites aligned to human rRNA among the total number of nuclear encoded rRNA Ψ sites identified in corresponding species. A total of 105 Ψ sites are identified in nuclear encoded rRNA in human. The BID-seq datasets of mouse and human were downloaded from the Gene Expression Omnibus database under the accession number of GSE238245 and GSE179798 respectively.

Source data

Extended Data Fig. 6 Correlation analysis of Ψ level with translation efficiency of genes across multiple tissues in Arabidopsis.

a, Correlation analysis between Ψ level on each rRNA site and 977 transcripts’ translation efficiency at transcript level (Etranscript). The median correlation value was shown by the yellow or the blue dot. The error bars represent the interquartile range (IQR). Etranscript were calculated by normaling ribosome-bound RNA (with polysome footprinting data) to the whole-cell mRNA level. b, Examples of Ψ sites on Nu-18S: 913 and Nu-18S: 1195 that calculated with the correlations between Ψ levels and translation efficiency (Etranscript) among nine Arabidopsis tissues are shown. Etranscript were calculated by normaling ribosome-bound RNA (with polysome footprinting data) to the whole-cell mRNA level. Examples of correlations regarding to specific genes were also showed in b. Nu-18S: 913 belongs to the initiation region, and Nu-18S: 1195 belongs to the decoding region. c, Heatmap showing all the correlation value between the Ψ level of each rRNA site and the translation efficiency (Etranscript) of each transcript. The correlation matrix was clustered by the similarities score among Ψ sites and 977 transcripts.

Extended Data Fig. 7 Ψ modification motifs in Arabidopsis and rice.

a, b, All potential TΨG motif sequences with a sliding window of 1nt in Arabidopsis (a) and rice (b). Motifs with fractions over 20% were selected to plot the figure and the number of each motif (N) is shown. c, d, All potential TΨC motif sequences with a sliding window of 1nt in Arabidopsis (c) and rice (d). All the detected Ψ sites within tissues were combined to calculate the motifs. Motifs with fractions over 20% were selected to plot the figure and the number of each motif (N) is showed. The sliding window of 1 nt means 1 nucleotide upstream and 1 nucleotide downstream of the given motif. Combining with the motif length of 3 nt, the window size is 5 nt. e, f, Heatmap showing motif types and numbers of Ψ modifications in each tissue of Arabidopsis (e) and rice (f). All the detected Ψ sites within tissues were combined to calculate the motifs. 8DAY represents 8 days and 2 W represents 2 weeks. 10DAA represents 10 days after anthesis.

Source data

Extended Data Fig. 8 Overview of the quality of BID-seq data.

a–c, mRNA Ψ levels in the harvested samples were quantified using LC-MS/MS for rice (a), Arabidopsis (b), maize and soybean (c). Three biological replicates were used. Data are means ± SD, n = 3. d, e, Principal component analysis (PCA) of Ψ fractions in Arabidopsis (d) and in rice (e) across different tissues. 8DAY represents 8 days and 2 W represents 2 weeks. 10DAA represents 10 days after anthesis.

Source data

Extended Data Fig. 9 mRNA Ψ modification in various tissues of Arabidopsis and rice.

a, BID-seq revealed a large number of mRNA Ψ sites in ten rice tissues. b, Diverse average Ψ fractions on mRNA across different tissues in rice, including plumule (n = 1,468), radicle (n = 1,851), seedling 8DAY (n = 1,153), seedling 2 W (n = 1,781), straw heading (n = 1,710), flag leaf heading (n = 1,631), panicle (n = 1,604), flag leaf 10DAA (n = 1,699), embryo (n = 1,844), and endosperm (n = 1,128) shown in boxplot. The red dots mark the mean, the lines show the median, the boxes represent the interquartile range (IQR), and the whiskers extend to 1.5× of the IQR. c, Boxplot showing fractions of tissue common (n = 123) and unique mRNA Ψ sites in Arabidopsis, including seedling (n = 478), shoot (n = 400), root (n = 1,160), rossta leaf (n = 385), cauline leaf (n = 315), stem (n = 416), flower (n = 706), silique (n = 370), and seed (n = 712). d, Boxplot showing fractions of tissue common (n = 55) and unique mRNA Ψ sites in rice, including plumule (n = 399), radicle (n = 1,042), seedling 8DAY (n = 200), seedling 2 W (n = 552), straw heading (n = 408), flag leaf heading (n = 509), panicle (n = 440), flag leaf 10DAA (n = 482), embryo (n = 728), and endosperm (n = 401). The lines show the median, the boxes represent the interquartile range (IQR), and the whiskers extend to 1.5× of the IQR. 8DAY represents 8 days and 2 W represents 2 weeks. 10DAA represents 10 days after anthesis.

Source data

Supplementary information

Reporting Summary

Supplementary Tables 1–3

Supplementary Table 1. Number of tRNA Ψ sites among nine Arabidopsis tissues. Supplementary Table 2. Number of mRNA Ψ sites among nine Arabidopsis tissues. Supplementary Table 3. Number of mRNA Ψ sites among ten different rice tissues.

Source data

Source Data Fig. 1

Source data for Figs. 1, 2 and 5 and Extended Data Figs. 5, 7, 8 and 9.

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Li, H., Wang, G., Ye, C. et al. Quantitative RNA pseudouridine maps reveal multilayered translation control through plant rRNA, tRNA and mRNA pseudouridylation. Nat. Plants 11, 234–247 (2025). https://doi.org/10.1038/s41477-024-01894-7

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