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.
Data availability
Pi measurements: raw data included in actual figurePhenotypes: representative lines shown in main figures, at least three independent lines shown in figure supplementsWestern blots: full western blots shown in figure supplementsProtein gels: Full gels shown in figure 5 supplement 1 and figure 6 supplement 1DNA sequences of the truncated VIH2 transcript is in figure 2 supplement 1NMR data: full 1D and 2D spectra shown in figure 5 and figure 5 supplement 2, figure 6 supplement 2
Article and author information
Author details
Funding
H2020 European Research Council (310856)
- Michael Hothorn
Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (CRSII5_170925)
- Dorothea Fiedler
- Michael Hothorn
Howard Hughes Medical Institute (55008733)
- Michael Hothorn
European Molecular Biology Organization (ALTF 493-2015)
- Kelvin Lau
Leibniz-Gemeinschaft (SAW-2017-FMP-1)
- Dorothea Fiedler
Deutsche Forschungsgemeinschaft (SCHA 1274/4-1)
- Gabriel Schaaf
Max-Planck-Gesellschaft
- Youjun Zhang
- Alisdair R Fernie
Horizon 2020 Framework Programme (PlantaSYST)
- Youjun Zhang
- Alisdair R Fernie
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Jürgen Kleine-Vehn, University of Natural Resources and Life Sciences, Austria
Version history
- Received: November 12, 2018
- Accepted: August 21, 2019
- Accepted Manuscript published: August 22, 2019 (version 1)
- Version of Record published: September 6, 2019 (version 2)
Copyright
© 2019, Zhu et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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