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RNA demethylation increases the yield and biomass of rice and potato plants in field trials

Abstract

RNA N6-methyladenosine (m6A) modifications are essential in plants. Here, we show that transgenic expression of the human RNA demethylase FTO in rice caused a more than threefold increase in grain yield under greenhouse conditions. In field trials, transgenic expression of FTO in rice and potato caused ~50% increases in yield and biomass. We demonstrate that the presence of FTO stimulates root meristem cell proliferation and tiller bud formation and promotes photosynthetic efficiency and drought tolerance but has no effect on mature cell size, shoot meristem cell proliferation, root diameter, plant height or ploidy. FTO mediates substantial m6A demethylation (around 7% of demethylation in poly(A) RNA and around 35% decrease of m6A in non-ribosomal nuclear RNA) in plant RNA, inducing chromatin openness and transcriptional activation. Therefore, modulation of plant RNA m6A methylation is a promising strategy to dramatically improve plant growth and crop yield.

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Fig. 1: Transgenic expression of FTO increases yield and biomass of rice and potato plants in the field.
Fig. 2: FTO increases root meristem cell proliferation, root growth, tiller formation and photosynthesis efficiency.
Fig. 3: Transcriptome-wide identification and analysis of FTO-mediated m6A-demethylation sites in rice.
Fig. 4: FTO increases plant chromatin accessibility and affects various metabolic pathways.

Data availability

m6A-seq and quantitative RNA-seq data generated by this study were deposited in the GEO database under the accession number GSE135549. Source data are provided with this paper.

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Acknowledgements

We thank Y. Wang for paraffin embedding station support, C. Xu for microtome support and X. Meng and J. Wang for assistance during field work. This work was supported by the National Basic Research Program of China (2019YFA0802201 and 2017YFA0505201 to G.J.), the National Natural Science Foundation of China (21822702, 21820102008, 92053109 and 21432002 to G.J.), the Beijing Natural Science Foundation (Z200010 to G.J.), EpiPlanta Biotech Ltd. (to G.J.), the Beijing Advanced Innovation Center for Genomics at Peking University (to G.J.) and the Zhong Ziyi Education Foundation (to C.H.). C.H. is a Howard Hughes Medical Institute Investigator.

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Contributions

G.J. and C.H. conceived the original idea and designed original studies. Q.Y. performed most experiments with help from Y.L., Y. Xiao., S.Z., X.W., Y. Xu, Y.L., J.Y., J.T., H.-C.D., L.-H.W., Q.T., C.W., Wutong Zhang, Y.W., P.S., Q.L., Wei Zhang, S.D., H.Y., H.Z. and B.S. S.L. performed most computational analysis with help from J.W. G.J. and C.H. wrote the manuscript with input from Q.Y. and S.L.

Corresponding authors

Correspondence to Baoan Song or Chuan He or Guifang Jia.

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Competing interests

A patent application has been filed by EpiPlanta Biotech Ltd. for the technology disclosed in this publication. C.H. is a scientific founder and a member of the scientific advisory board of Accent Therapeutics.

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Peer review information Nature Biotechnology thanks Brian Gregory and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Supplementary information

Supplementary Information

Supplementary Figs. 1–24, Tables 1–6, Results and Methods.

Reporting Summary

Supplementary Data 1

Hypo-m6A-containing genes in transgenic rice shoots and roots.

Supplementary Data 2

GO analyses of hypo-m6A-containing genes in transgenic rice shoots and roots.

Supplementary Data 3

Analysis of quantitative RNA sequencing data, focusing on differential expression of mRNA and repeat RNA.

Supplementary Data 4

Upregulated pathways revealed by GSEA between WT and FTO-transgenic rice shoots and roots.

Supplementary Data 5

Unprocessed gel for Supplementary Fig. 1c.

Supplementary Data 6

Unprocessed western blot for Supplementary Fig. 1d.

Supplementary Data 7

Unprocessed western blot for Supplementary Fig. 24.

Supplementary Data 8

Flow cytometry sequential gating strategy for Supplementary Fig. 21.

Source data

Source Data Fig. 4

Unprocessed western blot for Fig. 4b.

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Yu, Q., Liu, S., Yu, L. et al. RNA demethylation increases the yield and biomass of rice and potato plants in field trials. Nat Biotechnol (2021). https://doi.org/10.1038/s41587-021-00982-9

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