Two bifunctional inositol pyrophosphate kinases/phosphatases control plant phosphate homeostasis

Research output: Contribution to journalArticleResearchpeer review

Authors

  • Jinsheng Zhu
  • Kelvin Lau
  • Robert Puschmann
  • Robert K. Harmel
  • Youjun Zhang
  • Verena Pries
  • Philipp Gaugler
  • Larissa Broger
  • Amit K. Dutta
  • Henning J. Jessen
  • Gabriel Schaaf
  • Alisdair R. Fernie
  • Ludwig A. Hothorn
  • Dorothea Fiedler
  • Michael Hothorn

Research Organisations

External Research Organisations

  • University of Geneva
  • Leibniz-Forschungsinstitut für Molekulare Pharmakologie (FMP)
  • Humboldt-Universität zu Berlin (HU Berlin)
  • Max Planck Institute of Molecular Plant Physiology (MPI-MP)
  • University of Bonn
  • Center of Plant Systems Biology and Biotechnology CPSBB
  • University of Freiburg
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Details

Original languageEnglish
Article numbere43582
JournalELIFE
Volume8
Early online date22 Aug 2019
Publication statusE-pub ahead of print - 22 Aug 2019

Abstract

Many eukaryotic proteins regulating phosphate (Pi) homeostasis contain SPX domains that are receptors for inositol pyrophosphates (PP-InsP), suggesting that PP-InsPs may regulate Pi homeostasis. Here we report that deletion of two diphosphoinositol pentakisphosphate kinases VIH1/2 impairs plant growth and leads to constitutive Pi starvation responses. Deletion of phosphate starvation response transcription factors partially rescues vih1 vih2 mutant phenotypes, placing diphosphoinositol pentakisphosphate kinases in plant Pi signal transduction cascades. VIH1/ 2 are bifunctional enzymes able to generate and break-down PP-InsPs. Mutations in the kinase active site lead to increased Pi levels and constitutive Pi starvation responses. ATP levels change significantly in different Pi growth conditions. ATP-Mg2+ concentrations shift the relative kinase and phosphatase activities of diphosphoinositol pentakisphosphate kinases in vitro. Pi inhibits the phosphatase activity of the enzyme. Thus, VIH1 and VIH2 relay changes in cellular ATP and Pi concentrations to changes in PP-InsP levels, allowing plants to maintain sufficient Pi levels.

ASJC Scopus subject areas

Cite this

Two bifunctional inositol pyrophosphate kinases/phosphatases control plant phosphate homeostasis. / Zhu, Jinsheng; Lau, Kelvin; Puschmann, Robert et al.
In: ELIFE, Vol. 8, e43582, 22.08.2019.

Research output: Contribution to journalArticleResearchpeer review

Zhu, J, Lau, K, Puschmann, R, Harmel, RK, Zhang, Y, Pries, V, Gaugler, P, Broger, L, Dutta, AK, Jessen, HJ, Schaaf, G, Fernie, AR, Hothorn, LA, Fiedler, D & Hothorn, M 2019, 'Two bifunctional inositol pyrophosphate kinases/phosphatases control plant phosphate homeostasis', ELIFE, vol. 8, e43582. https://doi.org/10.1101/467076, https://doi.org/10.7554/eLife.43582, https://doi.org/10.15488/9307
Zhu, J., Lau, K., Puschmann, R., Harmel, R. K., Zhang, Y., Pries, V., Gaugler, P., Broger, L., Dutta, A. K., Jessen, H. J., Schaaf, G., Fernie, A. R., Hothorn, L. A., Fiedler, D., & Hothorn, M. (2019). Two bifunctional inositol pyrophosphate kinases/phosphatases control plant phosphate homeostasis. ELIFE, 8, Article e43582. Advance online publication. https://doi.org/10.1101/467076, https://doi.org/10.7554/eLife.43582, https://doi.org/10.15488/9307
Zhu J, Lau K, Puschmann R, Harmel RK, Zhang Y, Pries V et al. Two bifunctional inositol pyrophosphate kinases/phosphatases control plant phosphate homeostasis. ELIFE. 2019 Aug 22;8:e43582. Epub 2019 Aug 22. doi: 10.1101/467076, 10.7554/eLife.43582, 10.15488/9307
Zhu, Jinsheng ; Lau, Kelvin ; Puschmann, Robert et al. / Two bifunctional inositol pyrophosphate kinases/phosphatases control plant phosphate homeostasis. In: ELIFE. 2019 ; Vol. 8.
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@article{39629784cee94b87a5c9985e193bc14e,
title = "Two bifunctional inositol pyrophosphate kinases/phosphatases control plant phosphate homeostasis",
abstract = "Many eukaryotic proteins regulating phosphate (Pi) homeostasis contain SPX domains that are receptors for inositol pyrophosphates (PP-InsP), suggesting that PP-InsPs may regulate Pi homeostasis. Here we report that deletion of two diphosphoinositol pentakisphosphate kinases VIH1/2 impairs plant growth and leads to constitutive Pi starvation responses. Deletion of phosphate starvation response transcription factors partially rescues vih1 vih2 mutant phenotypes, placing diphosphoinositol pentakisphosphate kinases in plant Pi signal transduction cascades. VIH1/ 2 are bifunctional enzymes able to generate and break-down PP-InsPs. Mutations in the kinase active site lead to increased Pi levels and constitutive Pi starvation responses. ATP levels change significantly in different Pi growth conditions. ATP-Mg2+ concentrations shift the relative kinase and phosphatase activities of diphosphoinositol pentakisphosphate kinases in vitro. Pi inhibits the phosphatase activity of the enzyme. Thus, VIH1 and VIH2 relay changes in cellular ATP and Pi concentrations to changes in PP-InsP levels, allowing plants to maintain sufficient Pi levels.",
author = "Jinsheng Zhu and Kelvin Lau and Robert Puschmann and Harmel, {Robert K.} and Youjun Zhang and Verena Pries and Philipp Gaugler and Larissa Broger and Dutta, {Amit K.} and Jessen, {Henning J.} and Gabriel Schaaf and Fernie, {Alisdair R.} and Hothorn, {Ludwig A.} and Dorothea Fiedler and Michael Hothorn",
note = "Funding Information: This work was supported by European Research Council under the European Union{\textquoteright}s Seventh Framework Programme (FP/2007–2013)/ERC Grant Agreement 310856 (to MH), by Swiss National Foundation Sinergia Grant CRSII5_170925 (to DF and MH), by grant SCHA 1274/4–1 from the Deutsche Forschungsgemeinschaft (to GS) and by an HHMI International Research Scholar Award (to MH). KL was supported by an EMBO long-term fellowship (ALTF-493–2015). RKH and RP were supported by the Leibniz Gemeinschaft (SAW-2017-FMP-1). YZ and ARF were supported by the Max-Planck Society and the European Union{\textquoteright}s Horizon 2020 research and innovation program, project PlantaSYST. We thank D Couto, L Lorenzo-Orts, M Ried, J Savarin and Y Poirier for critically reading the manuscript. ",
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Download

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T1 - Two bifunctional inositol pyrophosphate kinases/phosphatases control plant phosphate homeostasis

AU - Zhu, Jinsheng

AU - Lau, Kelvin

AU - Puschmann, Robert

AU - Harmel, Robert K.

AU - Zhang, Youjun

AU - Pries, Verena

AU - Gaugler, Philipp

AU - Broger, Larissa

AU - Dutta, Amit K.

AU - Jessen, Henning J.

AU - Schaaf, Gabriel

AU - Fernie, Alisdair R.

AU - Hothorn, Ludwig A.

AU - Fiedler, Dorothea

AU - Hothorn, Michael

N1 - Funding Information: This work was supported by European Research Council under the European Union’s Seventh Framework Programme (FP/2007–2013)/ERC Grant Agreement 310856 (to MH), by Swiss National Foundation Sinergia Grant CRSII5_170925 (to DF and MH), by grant SCHA 1274/4–1 from the Deutsche Forschungsgemeinschaft (to GS) and by an HHMI International Research Scholar Award (to MH). KL was supported by an EMBO long-term fellowship (ALTF-493–2015). RKH and RP were supported by the Leibniz Gemeinschaft (SAW-2017-FMP-1). YZ and ARF were supported by the Max-Planck Society and the European Union’s Horizon 2020 research and innovation program, project PlantaSYST. We thank D Couto, L Lorenzo-Orts, M Ried, J Savarin and Y Poirier for critically reading the manuscript.

PY - 2019/8/22

Y1 - 2019/8/22

N2 - Many eukaryotic proteins regulating phosphate (Pi) homeostasis contain SPX domains that are receptors for inositol pyrophosphates (PP-InsP), suggesting that PP-InsPs may regulate Pi homeostasis. Here we report that deletion of two diphosphoinositol pentakisphosphate kinases VIH1/2 impairs plant growth and leads to constitutive Pi starvation responses. Deletion of phosphate starvation response transcription factors partially rescues vih1 vih2 mutant phenotypes, placing diphosphoinositol pentakisphosphate kinases in plant Pi signal transduction cascades. VIH1/ 2 are bifunctional enzymes able to generate and break-down PP-InsPs. Mutations in the kinase active site lead to increased Pi levels and constitutive Pi starvation responses. ATP levels change significantly in different Pi growth conditions. ATP-Mg2+ concentrations shift the relative kinase and phosphatase activities of diphosphoinositol pentakisphosphate kinases in vitro. Pi inhibits the phosphatase activity of the enzyme. Thus, VIH1 and VIH2 relay changes in cellular ATP and Pi concentrations to changes in PP-InsP levels, allowing plants to maintain sufficient Pi levels.

AB - Many eukaryotic proteins regulating phosphate (Pi) homeostasis contain SPX domains that are receptors for inositol pyrophosphates (PP-InsP), suggesting that PP-InsPs may regulate Pi homeostasis. Here we report that deletion of two diphosphoinositol pentakisphosphate kinases VIH1/2 impairs plant growth and leads to constitutive Pi starvation responses. Deletion of phosphate starvation response transcription factors partially rescues vih1 vih2 mutant phenotypes, placing diphosphoinositol pentakisphosphate kinases in plant Pi signal transduction cascades. VIH1/ 2 are bifunctional enzymes able to generate and break-down PP-InsPs. Mutations in the kinase active site lead to increased Pi levels and constitutive Pi starvation responses. ATP levels change significantly in different Pi growth conditions. ATP-Mg2+ concentrations shift the relative kinase and phosphatase activities of diphosphoinositol pentakisphosphate kinases in vitro. Pi inhibits the phosphatase activity of the enzyme. Thus, VIH1 and VIH2 relay changes in cellular ATP and Pi concentrations to changes in PP-InsP levels, allowing plants to maintain sufficient Pi levels.

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JO - ELIFE

JF - ELIFE

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