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Translational control of phloem development by RNA G-quadruplex–JULGI determines plant sink strength

Abstract

The emergence of a plant vascular system was a prerequisite for the colonization of land; however, it is unclear how the photosynthate transporting system was established during plant evolution. Here, we identify a novel translational regulatory module for phloem development involving the zinc-finger protein JULGI (JUL) and its targets, the 5′ untranslated regions (UTRs) of the SUPPRESSOR OF MAX2 1-LIKE4/5 (SMXL4/5) mRNAs, which is exclusively conserved in vascular plants. JUL directly binds and induces an RNA G-quadruplex in the 5′ UTR of SMXL4/5, which are key promoters of phloem differentiation. We show that RNA G-quadruplex formation suppresses SMXL4/5 translation and restricts phloem differentiation. In turn, JUL deficiency promotes phloem formation and strikingly increases sink strength per seed. We propose that the translational regulation by the JUL/5′ UTR G-quadruplex module is a major determinant of phloem establishment, thereby determining carbon allocation to sink tissues, and that this mechanism was a key invention during the emergence of vascular plants.

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Fig. 1: Identification of a negative regulator, JULGI, in phloem differentiation.
Fig. 2: JUL1 targets the G-quadruplex-forming sequence in the SMXL5 5′ UTR that is exclusively conserved in vascular plants.
Fig. 3: Phenotypes of smxl4/5 loss-of-function mutants.
Fig. 4: JUL1 directly binds to the G-quadruplex-forming motif and induces G-quadruplex formation of the SMXL5 5′ UTR.
Fig. 5: Cytosolic JUL and SMXL5 in the phloem and cambium controls phloem development.
Fig. 6: JUL1 interaction with the G-quadruplex in the SMXL5 5′ UTR is necessary and sufficient for JUL1-mediated translation inhibition of SMXL5.
Fig. 7: JUL-directed SMXL4/5 translational repression inhibits phloem differentiation.
Fig. 8: JUL deficiency enhances sink strengths of seed in tobacco and Arabidopsis.

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Acknowledgements

We thank V.N. Kim for critical reading and useful suggestions, H.S. Yoon for advice on phylogenetic analysis. This work was supported by grants to I.H. from the Basic Science Research Programme (2017R1A2A1A17069734) through the National Research Foundation (NRF) funded by the Ministry of Science, ICT and Future Planning, and from the Cooperative Research Programme for Agriculture Science & Technology Development (PJ010953022018) funded by Rural Development Administration, Korea. T.V.T.D is supported by the Korean Research Fellowship programme (2017H1D3A1A03055171).

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Contributions

H.C. and H.S.C. performed all experiments. H.C. and I.H. designed the experiments and analysed data. J.Y. performed genetic screening for charactering JUL. H.J. performed the RNA SELEX analysis and analysed data with H.C. and C.B. C.P. performed phylogenetic analysis. T.V.T.D. conducted reporter assay using protoplast. H.N. contributed to VISUAL analysis. H.Y. performed CD analysis. J.Jeon conducted dissociation constant measurement. E.K. performed sucrose density gradient analysis with S.K.J. J.P. conducted reporter assay with HEK293T cell with Y.L. H.C. and I.H. wrote the manuscript.

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Correspondence to Ildoo Hwang.

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Supplementary information

Supplementary Information

Supplementary Figures 1–9

Reporting Summary

Supplementary Table 1

JULGI homologues in plant kingdom

Supplementary Table 2

Phloem-specific genes containing RNA G-quadruplex

Supplementary Table 3

SMXLs and its 5'UTR in plant kingdom

Supplementary Table 4

Primers used in this study

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Cho, H., Cho, H.S., Nam, H. et al. Translational control of phloem development by RNA G-quadruplex–JULGI determines plant sink strength. Nature Plants 4, 376–390 (2018). https://doi.org/10.1038/s41477-018-0157-2

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