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Endogenous stress-related signal directs shoot stem cell fate in Arabidopsis thaliana

Nature Plants volume 7, pages 1276–1287 (2021)Cite this article

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Abstract

Stem cell populations in all multicellular organisms are situated in a niche, which is a special microenvironment that defines stem cell fate. The interplay between stem cells and their niches is crucial for stem cell maintenance. Here, we show that an endogenous stress-related signal (ESS) is overrepresented in the shoot stem cell niche under natural growth conditions, and the vast majority of known stem-cell-specific and niche-specific genes responded to stress signals. Interference with the ESS in the stem cell niche by blocking ethylene signalling impaired stem cell maintenance. Ethylene-insensitive 3 (EIN3), the key transcription factor in ethylene signalling, directly actives the expression of the stress hub transcription factor AGAMOUS-LIKE 22 (AGL22) in the stem cell niche and relays ESS signals to the WUSCHEL/CLAVATA network. Our results provide a mechanistic framework for ESS signalling control of the stem cell niche and demonstrate that plant stem cells are maintained by a native stress microenvironment in vivo.

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Fig. 1: Plant stem cells are accumulated in the mp clv3 double mutant.
Fig. 2: SNC-specific genes respond to ethylene.
Fig. 3: EIN3 and EILs are involved in stem cell maintenance.
Fig. 4: EIN3 directly activates AGL22 expression.
Fig. 5: AGL22 maintains stem cell fate by positively regulating WUS expression.
Fig. 6: AGL22 mediates ESS signalling transduction in the stem cell niche.
Fig. 7: AGL22 integrates endogenous and exogenous stress signals to regulate plant development.

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Data availability

The RNA-seq data have been deposited in the NCBI GEO and are accessible through GEO series accession number GSE77169. Source data are provided with this paper.

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Acknowledgements

This work was supported by grants to Z.Z. from the Strategic Priority Research Program of the Chinese Academy of Sciences (grant no. XDB27030105) and the National Natural Science Foundation of China (grant nos. 31870264 and 31570273). We thank Y. Hou for help with identifying the mp clv3 double mutant. We thank J. Lohmann, Z. Ding, D. Yu, C. Li, C. Xiang, C.-K. Wen and G. Coupland for sharing plant materials.

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  1. These authors contributed equally: Jian Zeng, Xiang Li, Qiang Ge.

Authors and Affiliations

  1. Hefei National Laboratory for Physical Sciences at the Microscale, CAS Center for Excellence in Molecular Plant Sciences, School of Life Sciences, Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei, China

    Jian Zeng, Xiang Li, Qiang Ge, Linjie Luo, Zhaoxia Tian & Zhong Zhao

  2. School of Life Sciences, Guangzhou University, Guangzhou Higher Education Mega Center, Guangzhou, China

    Zhicheng Dong

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Contributions

Z.Z., J.Z. and Z.T. designed the experiments, analysed the data and wrote the manuscript. Z.D. and Z.T. conducted RNA-seq. L.L. performed the in situ hybridization of WUS, CSD3 and AP1 on WT, clv3 and mp clv3. X.L. and Q.G. analysed the ein3-1 eil2 eil3 triple mutant and UBQ10::SVP/ein3 eil2 eil3 plants and performed the PEG treatment and EMSAs. J.Z. conducted all the other experiments.

Corresponding authors

Correspondence to Zhaoxia Tian or Zhong Zhao.

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The authors declare no competing interests.

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Peer review information Nature Plants thanks the anonymous reviewers for their contribution to the peer review of this work.

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Supplementary information

Supplementary Information

Supplementary Methods, Figs. 1–16, unprocessed gels or blots for supplementary figures and legends for Tables 1–6.

Reporting Summary

Supplementary Tables

Table 1: List of SNC-, PZ- and F-specific genes. Table 2: List of the top 500 candidate genes in the SNC. Table 3: Distribution of hormone response genes in profiles according to annotation. Table 4: Distribution of stress response genes in profiles by annotation. Table 5: Gene Ontology term enrichment analysis of profiles for the SNC, PZ and F. Table 6: Oligonucleotides used in this study (5′→3′).

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Unprocessed EMSA gels.

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Zeng, J., Li, X., Ge, Q. et al. Endogenous stress-related signal directs shoot stem cell fate in Arabidopsis thaliana. Nat. Plants 7, 1276–1287 (2021). https://doi.org/10.1038/s41477-021-00985-z

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