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BIL1-mediated MP phosphorylation integrates PXY and cytokinin signalling in secondary growth

Nature Plants volume 4, pages 605–614 (2018)Cite this article

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Abstract

Vascular cambium proliferation in plants is crucial for the generation of vascular tissues and for mechanical strength. Phytohormones and mobile peptides are key regulators of vascular cambial activity during secondary growth; however, the signalling cross-talk underlying their coordinated action is largely unknown. Here, we reveal that BIN2-LIKE 1 (BIL1), a glycogen synthase kinase 3, integrates the PHLOEM INTERCALATED WITH XYLEM/tracheary element differentiation inhibitory factor (TDIF) RECEPTOR (PXY/TDR) module into MONOPTEROS/AUXIN RESPONSE FACTOR 5 (MP/ARF5) transcription factor action during secondary growth. BIL1-mediated phosphorylation of MP/ARF5 enhances its negative effect on vascular cambial activity, which upregulates the negative regulators of cytokinin signalling ARABIDOPSIS RESPONSE REGULATOR 7 (ARR7) and ARR15. PXY/TDR inhibits BIL1 activity, which attenuates the effect of MP/ARF5 on ARR7 and ARR15 expression, thus increasing vascular cambial activity. Together, these results suggest that BIL1 is a key mediator that links peptide signalling with auxin–cytokinin signalling for the maintenance of cambial activity.

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Fig. 1: BIL1 is a negative regulator of cambial activity.
Fig. 2: BIL1-mediated MP phosphorylation negatively regulates cambial activity.
Fig. 3: BIL1 and MP attenuate the cytokinin response to regulate cambial activity.
Fig. 4: TDIF–PXY functions upstream of the BIL1–MP module and suppresses their negative effect on cambial activity.

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Acknowledgements

We thank K. Choi and F. Rolland for critical reading of the manuscript and useful suggestions. This work was carried out with the support of the Cooperative Research Program for Agriculture Science and Technology Development (Project No. PJ010953022018) Rural Development Administration, Republic of Korea, and with the support of Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Science, ICT and Future Planning (2017R1A2A1A17069734).

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  1. These authors contributed equally: Soeun Han, Hyunwoo Cho.

Authors and Affiliations

  1. Department of Life Sciences, Pohang University of Science and Technology, Pohang, Korea

    Soeun Han, Hyunwoo Cho, Jaegyun Noh, Heejae Nam, Seungchul Lee & Ildoo Hwang

  2. Centre for Organismal Studies (COS), Heidelberg University, Heidelberg, Germany

    Jiyan Qi & Thomas Greb

  3. Department of New Biology, Daegu Gyeongbuk Institute of Science and Technology, Daegu, Korea

    Hee-Jung Jung & Daehee Hwang

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Contributions

S.H., H.C., J.N., J.Q. and H.N. performed the experiments. H.-J.J. and D.H. performed the LC–MS/MS analysis. S.L. analysed the RNA-seq data. S.H., H.C., T.G. and I.H. designed the experiments and analysed the data. S.H., H.C. and I.H. wrote the manuscript.

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Correspondence to Ildoo Hwang.

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Han, S., Cho, H., Noh, J. et al. BIL1-mediated MP phosphorylation integrates PXY and cytokinin signalling in secondary growth. Nature Plants 4, 605–614 (2018). https://doi.org/10.1038/s41477-018-0180-3

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