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A group of receptor kinases are essential for CLAVATA signalling to maintain stem cell homeostasis

Abstract

Continuous organ initiation and outgrowth in plants relies on the proliferation and differentiation of stem cells maintained by the CLAVATA (CLV)–WUSCHEL (WUS) negative-feedback loop1,2,3. Leucine-rich repeat receptor-like protein kinases (LRR-RLKs), including CLV1, BARELY ANY MERISTEMS and RECEPTOR-LIKE PROTEIN KINASE 2 (RPK2), a receptor-like protein CLV2 and a pseudokinase CORYNE (CRN) are involved in the perception of the CLV3 signal to repress WUS expression4,5,6,7,8,9,10. WUS, a homeodomain transcription factor, in turn directly activates CLV3 expression and promotes stem cell activity in the shoot apical meristem11,12. However, the signalling mechanism immediately following the perception of CLV3 by its receptors is poorly understood. Here, we show that a group of LRR-RLKs, designated as CLAVATA3 INSENSITIVE RECEPTOR KINASES (CIKs), have essential roles in regulating CLV3-mediated stem cell homeostasis. The cik1234 quadruple mutant exhibits a significantly enlarged SAM, resembling clv mutants. Genetic analyses and biochemical assays demonstrated that CIKs function as co-receptors of CLV1, CLV2/CRN and RPK2 to mediate CLV3 signalling through phosphorylation. Our findings not only widen the understanding of the underlying mechanism of CLV3 signal transduction in regulating stem cell fate but also reveal a novel group of RLKs that function as co-receptors to possibly mediate multiple extrinsic and intrinsic signals during plant growth and development.

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Fig. 1: CIKs are essential for maintaining the shoot stem cell homeostasis.
Fig. 2: CIKs are involved in the CLV3-mediated signalling pathway.
Fig. 3: CIKs integrate all three parallel receptor kinase-mediated pathways to transduce the CLV3 signal.
Fig. 4: CIKs function as co-receptors of CLV1, CRN and RPK2.

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Acknowledgements

We are grateful to the Arabidopsis Biological Resource Center (ABRC) and the Nottingham Arabidopsis Stock Centre (NASC) for providing the T-DNA insertion lines used in this study. We thank H. Li (Core Facility for Life Science Research, Lanzhou University) for SEM technique assistance, and D. Braun (University of Missouri) for his critical reading of the manuscript. This work was supported by the National Natural Science Foundation of China (31770312, 31471402, 31270229 and 31070283), the Ministry of Education (113058A and NCET-12-0249), the 111 Project (B16022), the Fundamental Research Funds for the Central Universities (lzujbky-2017-it01, lzujbky-2017-kb05 and 2022013zrk014) and the Gansu Provincial Science & Technology Department (17ZD2NA015-06 and 17ZD2NA016-5).

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C.H. and X.G. designed all experiments, analysed the data and wrote the manuscript. C.H. performed most of the experiments and prepared the data. Y.Z. conducted the pull-down, in vitro phosphorylation assays and physiological treatment of CLEs on roots. Y.C. performed the RNA in situ hybridization analyses. K.C. contributed to the high-order mutants. W.L. contributed to the maize experiments. M.Z., H.Y., Z.W., L.Z. and Y.X. contributed to the generation and analysis of myriad transgenic plants. Y.Z., Z.W., M.L., J.Y., S.H., K.H. and J.L. helped prepare the manuscript.

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Correspondence to Xiaoping Gou.

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Hu, C., Zhu, Y., Cui, Y. et al. A group of receptor kinases are essential for CLAVATA signalling to maintain stem cell homeostasis. Nature Plants 4, 205–211 (2018). https://doi.org/10.1038/s41477-018-0123-z

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