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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.

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.

References

  1. Rouached, H. et al. Regulation of phosphate starvation responses in plants: signaling players and cross-talks. Mol. Plant 3, 288–299 (2010).

    Article  CAS  Google Scholar 

  2. Hamburger, D. et al. Identification and characterization of the Arabidopsis PHO1 gene involved in phosphate loading to the xylem. Plant Cell 14, 889–902 (2002).

    Article  CAS  Google Scholar 

  3. Liu, T.-Y. et al. PHO2-dependent degradation of PHO1 modulates phosphate homeostasis in Arabidopsis. Plant Cell 24, 2168–2183 (2012).

    Article  CAS  Google Scholar 

  4. Chen, Y.-F. et al. The WRKY6 transcription factor modulates PHOSPHATE1 expression in response to low Pi stress in Arabidopsis. Plant Cell 21, 3554–3566 (2009).

    Article  CAS  Google Scholar 

  5. Ye, Q. et al. The ubiquitin E3 ligase PRU1 regulates WRKY6 degradation to modulate phosphate homeostasis in response to low-Pi stress in Arabidopsis. Plant Cell 30, 1062–1076 (2018).

    Article  CAS  Google Scholar 

  6. Silva-Navas, A. et al. Role of cis-zeatin in root responses to phosphate starvation. N. Phytol. 224, 242–257 (2019).

    Article  CAS  Google Scholar 

  7. Hermans, C. et al. How do plants respond to nutrient shortage by biomass allocation? Trends Plant Sci. 11, 610–617 (2006).

    Article  CAS  Google Scholar 

  8. Lei, M. et al. Genetic and genomic evidence that sucrose is a global regulator of plant responses to phosphate starvation in Arabidopsis. Plant Physiol. 156, 1116–1130 (2011).

    Article  CAS  Google Scholar 

  9. Schneeberger, K. et al. SHOREmap: simultaneous mapping and mutation identification by deep sequencing. Nat. Methods 6, 550–551 (2009).

    Article  CAS  Google Scholar 

  10. Benfey, P. N. et al. Root development in Arabidopsis: four mutants with dramatically altered root morphogenesis. Development 119, 57–70 (1993).

    Article  CAS  Google Scholar 

  11. Hirano, Y. et al. Structure of the SHR–SCR heterodimer bound to the BIRD/IDD transcriptional factor JKD. Nat. Plants https://doi.org/10.1038/nplants.2017.10 (2017).

  12. Ittisoponpisan, S. et al. Can predicted protein 3D-structures provide reliable insights into whether missense variants are disease-associated? J. Mol. Biol. 431, 2197–2212 (2019).

    Article  CAS  Google Scholar 

  13. Rubio, V. et al. A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Genes Dev. 15, 2122–2133 (2001).

    Article  CAS  Google Scholar 

  14. Bustos, R. et al. A central regulatory system largely controls transcriptional activation and repression responses to phosphate starvation in Arabidopsis. PLoS Genet. 6, e1001102 (2010).

    Article  Google Scholar 

  15. Cui, H. et al. An evolutionarily conserved mechanism delimiting SHR movement defines a single layer of endodermis in plants. Science 316, 421–425 (2007).

    Article  CAS  Google Scholar 

  16. Arpat, A. B. et al. Functional expression of PHO1 to the Golgi and trans-Golgi network and its role in export of inorganic phosphate. Plant J. 71, 479–491 (2012).

    CAS  PubMed  Google Scholar 

  17. Sebastian, J. et al. PHABULOSA controls the quiescent center-independent root meristem activities in Arabidopsis thaliana. PLoS Genet. 11, e1004973 (2015).

    Article  Google Scholar 

  18. Carlsbecker, A. et al. Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate. Nature 465, 316–321 (2010).

    Article  CAS  Google Scholar 

  19. Miyashima, S. et al. Non-cell-autonomous microRNA165 acts in a dose-dependent manner to regulate multiple differentiation status in the Arabidopsis root. Development 138, 2303–2313 (2011).

    Article  CAS  Google Scholar 

  20. Zheng, Z. et al. Blue light-triggered chemical reactions underlie phosphate deficiency-induced inhibition of root elongation of Arabidopsis seedlings grown in petri dishes. Mol. Plant 12, 1515–1523 (2019).

    Article  CAS  Google Scholar 

  21. Chiou, T. J. & Lin, S. I. Signaling network in sensing phosphate availability in plants. Annu. Rev. Plant Biol. 62, 185–206 (2011).

    Article  CAS  Google Scholar 

  22. Laurenzio, L. D. et al. The SCARECROW gene regulates an asymmetric cell division that is essential for generating the radial organization of the Arabidopsis root. Cell 86, 423–433 (1996).

    Article  Google Scholar 

  23. Lei, M. et al. Ethylene signalling is involved in regulation of phosphate starvation-induced gene expression and production of acid phosphatases and anthocyanin in Arabidopsis. N. Phytol. 189, 1084–1095 (2011).

    Article  CAS  Google Scholar 

  24. Schneeberger, K. et al. Simultaneous alignment of short reads against multiple genomes. Genome Biol. 10, R98 (2009).

    Article  Google Scholar 

  25. Clough, S. J. & Bent, A. F. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735–743 (1998).

    Article  CAS  Google Scholar 

  26. Jain, A. et al. Differential effects of sucrose and auxin on localized phosphate deficiency-induced modulation of different traits of root system architecture in Arabidopsis. Plant Physiol. 144, 232–247 (2007).

    Article  CAS  Google Scholar 

  27. Danku, J. et al. Large-scale plant ionomics. Methods Mol. Biol. 953, 255–276 (2013).

    CAS  PubMed  Google Scholar 

  28. Lahner, B. et al. Genomic scale profiling of nutrient and trace elements in Arabidopsis thaliana. Nat. Biotechnol. 21, 1215–1221 (2003).

    Article  CAS  Google Scholar 

  29. Bieza, K. & Lois, R. An Arabidopsis mutant tolerant to lethal ultraviolet-B levels shows constitutively elevated accumulation of flavonoids and other phenolics. Plant Physiol. 126, 1105–1115 (2001).

    Article  CAS  Google Scholar 

  30. Bainbridge, K. et al. Grafting in Arabidopsis. Methods Mol. Biol. 1062, 155–163 (2014).

    Article  Google Scholar 

  31. Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013).

    Article  CAS  Google Scholar 

  32. Pertea, M. et al. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat. Biotechnol. 33, 290–295 (2015).

    Article  CAS  Google Scholar 

  33. Love, M. I. et al. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).

    Article  Google Scholar 

  34. Yu, G. et al. clusterProfiler: an R package for comparing biological themes among gene clusters. Omics 16, 284–287 (2012).

    Article  CAS  Google Scholar 

  35. Yoo, S.-D. et al. Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat. Protoc. 2, 1565–1572 (2007).

    Article  CAS  Google Scholar 

  36. Saleh, A. et al. An efficient chromatin immunoprecipitation (ChIP) protocol for studying histone modifications in Arabidopsis plants. Nat. Protoc. 3, 1018–1025 (2008).

    Article  CAS  Google Scholar 

  37. Xiao, X. et al. A group of SUVH methyl-DNA binding proteins regulate expression of the DNA demethylase ROS1 in Arabidopsis. J. Integr. Plant Biol. 61, 110–119 (2019).

    Article  CAS  Google Scholar 

  38. Steffens, N. O. et al. AthaMap: an online resource for in silico transcription factor binding sites in the Arabidopsis thaliana genome. Nucleic Acids Res. 32, D368–D372 (2004).

    Article  CAS  Google Scholar 

Download references

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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