Two bifunctional inositol pyrophosphate kinases/phosphatases control plant phosphate homeostasis

Publikation: Beitrag in FachzeitschriftArtikelForschungPeer-Review

Autoren

  • 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

Organisationseinheiten

Externe Organisationen

  • Universität Genf
  • Leibniz-Institut für Molekulare Pharmakologie (FMP)
  • Humboldt-Universität zu Berlin (HU Berlin)
  • Max-Planck-Institut für molekulare Pflanzenphysiologie
  • Rheinische Friedrich-Wilhelms-Universität Bonn
  • Center of Plant Systems Biology and Biotechnology CPSBB
  • Albert-Ludwigs-Universität Freiburg
Forschungs-netzwerk anzeigen

Details

OriginalspracheEnglisch
Aufsatznummere43582
FachzeitschriftELIFE
Jahrgang8
Frühes Online-Datum22 Aug. 2019
PublikationsstatusElektronisch veröffentlicht (E-Pub) - 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.

Zitieren

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

Publikation: Beitrag in FachzeitschriftArtikelForschungPeer-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, Jg. 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, Artikel e43582. Vorabveröffentlichung online. 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 ; Jahrgang 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. ",
year = "2019",
month = aug,
day = "22",
doi = "10.1101/467076",
language = "English",
volume = "8",
journal = "ELIFE",
issn = "2050-084X",
publisher = "eLife Sciences Publications",

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Download

TY - JOUR

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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U2 - 10.1101/467076

DO - 10.1101/467076

M3 - Article

C2 - 31436531

AN - SCOPUS:85071788543

VL - 8

JO - ELIFE

JF - ELIFE

SN - 2050-084X

M1 - e43582

ER -