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SHORT-ROOT stabilizes PHOSPHATE1 to regulate phosphate allocation in Arabidopsis

Nature Plants volume 8, pages 1074–1081 (2022)Cite this article

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Abstract

The coordinated distribution of inorganic phosphate (Pi) between roots and shoots is an important process that plants use to maintain Pi homeostasis. SHORT-ROOT (SHR) is well characterized for its function in root radial patterning. Here we demonstrate a role of SHR in controlling Pi allocation from root to shoot by regulating PHOSPHATE1 in the root differentiation zone. We recovered a weak mutant allele of SHR in Arabidopsis that accumulates much less Pi in the shoot and shows a constitutive Pi starvation response under Pi-sufficient conditions. In addition, Pi starvation suppresses SHR protein accumulation and releases its inhibition on the HD–ZIP III transcription factor PHB. PHB accumulates and directly binds the promoter of PHOSPHATE2 to upregulate its transcription, resulting in PHOSPHATE1 degradation in the xylem-pole pericycle cells. Our findings reveal a previously unrecognized mechanism of how plants regulate Pi translocation from roots to shoots.

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Fig. 1: SHR is required for Pi translocation from roots to shoots.
Fig. 2: PHO1 localization pattern and protein levels are altered in phod1.
Fig. 3: PHB directly regulates PHO2 expression.
Fig. 4: A decrease in SHR levels in roots restricts Pi allocation to shoots under long-term Pi starvation.

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Data availability

The RNA-seq data in this study have been deposited in the NCBI Gene Expression Omnibus with the accession code GSE199834. Source data are provided with this paper.

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Acknowledgements

This work was supported by grants from the Shanghai Sailing Program (no. 20YF1456100) to X.X. and from the Chinese Academy of Sciences to M.L.

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Author notes

  1. These authors contributed equally: Xinlong Xiao, Jieqiong Zhang.

Authors and Affiliations

  1. Shanghai Center for Plant Stress Biology, CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Shanghai, China

    Xinlong Xiao, Jieqiong Zhang, Viswanathan Satheesh, Fanxiao Meng, Wenlan Gao, Jinsong Dong & Mingguang Lei

  2. School of Life Sciences and Technology, Tongji University, Shanghai, China

    Jieqiong Zhang

  3. University of Chinese Academy of Sciences, Beijing, China

    Jieqiong Zhang, Fanxiao Meng & Wenlan Gao

  4. School of Life Sciences, Tsinghua University, Beijing, China

    Zai Zheng & Dong Liu

  5. State Key Laboratory of Crop Stress Adaptation and Improvement, School of Life Sciences, Henan University, Kaifeng, China

    Guo-Yong An & Mingguang Lei

  6. Aix Marseille University, CEA, CNRS, BIAM, UMR7265, EBM (Bioénergies et microalgues), Saint-Paul lez Durance, France

    Laurent Nussaume

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Contributions

M.L. and X.X. conceived and designed the study. X.X. and J.Z. performed most of the experiments and analysed the data with M.L. The other authors assisted in the experiments and discussed the results. X.X., V.S. and M.L. wrote the manuscript.

Corresponding author

Correspondence to Mingguang Lei.

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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 Figs. 1–10, Table 1 and unprocessed gels for Supplementary Figs. 3, 8 and 9.

Reporting Summary

Supplementary Data 1

DEGs in the shoot of phod1.

Supplementary Data 2

Source data for Supplementary Figs. 1–10.

Supplementary Video 1

SHR–GFP in the root differentiation zone under P+ conditions.

Supplementary Video 2

SHR–GFP in the root differentiation zone under P− conditions.

Supplementary Video 3

PHB–GFP in the root differentiation zone under P+ conditions.

Supplementary Video 4

PHB–GFP in the root differentiation zone under P− conditions.

Source data

Source Data Fig. 1

Source data.

Source Data Fig. 2

Source data.

Source Data Fig. 3

Source data.

Source Data Fig. 4

Source data.

Source Data Fig. 2

Unprocessed western blot gels.

Source Data Fig. 3

Unprocessed western blot gels.

Source Data Fig. 4

Unprocessed western blot gels.

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Xiao, X., Zhang, J., Satheesh, V. et al. SHORT-ROOT stabilizes PHOSPHATE1 to regulate phosphate allocation in Arabidopsis. Nat. Plants 8, 1074–1081 (2022). https://doi.org/10.1038/s41477-022-01231-w

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