CIPK11-Dependent Phosphorylation Modulates FIT Activity to Promote Arabidopsis Iron Acquisition in Response to Calcium Signaling

Regina Gratz; Prabha Manishankar; Rumen Ivanov; Philipp Köster; Inga Mohr; Ksenia Trofimov; Leonie Steinhorst; Johannes Meiser; Hans Jörg Mai; Maria Drerup; Sibylle Arendt; Michael Holtkamp; Uwe Karst; Jörg Kudla; Petra Bauer; Tzvetina Brumbarova

doi:10.1016/j.devcel.2019.01.006

CIPK11-Dependent Phosphorylation Modulates FIT Activity to Promote Arabidopsis Iron Acquisition in Response to Calcium Signaling

Regina Gratz, Prabha Manishankar, Rumen Ivanov, Philipp Köster, Inga Mohr, Ksenia Trofimov, Leonie Steinhorst, Johannes Meiser, Hans Jörg Mai, Maria Drerup, Sibylle Arendt, Michael Holtkamp, Uwe Karst, Jörg Kudla, Petra Bauer^*, Tzvetina Brumbarova

^*Corresponding author for this work

Research output: Contribution to journal › Article › Research › peer-review

90 Citations (Scopus)

Abstract

Nutrient acquisition is entangled with growth and stress in sessile organisms. The bHLH transcription factor FIT is a key regulator of Arabidopsis iron (Fe) acquisition and post-translationally activated upon low Fe. We identified CBL-INTERACTING PROTEIN KINASE CIPK11 as a FIT interactor. Cytosolic Ca ²⁺ concentration and CIPK11 expression are induced by Fe deficiency. cipk11 mutant plants display compromised root Fe mobilization and seed Fe content. Fe uptake is dependent on CBL1/CBL9. CIPK11 phosphorylates FIT at Ser272, and mutation of this target site modulates FIT nuclear accumulation, homo-dimerization, interaction with bHLH039, and transcriptional activity and affects the plant's Fe-uptake ability. We propose that Ca ²⁺ -triggered CBL1/9-mediated activation of CIPK11 and subsequent phosphorylation of FIT shifts inactive into active FIT, allowing regulatory protein interactions in the nucleus. This biochemical link between Fe deficiency and the cellular Ca ²⁺ decoding machinery represents an environment-sensing mechanism to adjust nutrient uptake.

Original language	English
Pages (from-to)	726-740.e10
Journal	Developmental Cell
Volume	48
Issue number	5
DOIs	https://doi.org/10.1016/j.devcel.2019.01.006
Publication status	Published - 11 Mar 2019
Externally published	Yes

Keywords

CBL
CIPK11
FIT
bHLH039
iron deficiency
nucleocytoplasmic partitioning
protein interaction
protein mobility
protein phosphorylation
stress

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10.1016/j.devcel.2019.01.006

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Gratz, R., Manishankar, P., Ivanov, R., Köster, P., Mohr, I., Trofimov, K., Steinhorst, L., Meiser, J., Mai, H. J., Drerup, M., Arendt, S., Holtkamp, M., Karst, U., Kudla, J., Bauer, P., & Brumbarova, T. (2019). CIPK11-Dependent Phosphorylation Modulates FIT Activity to Promote Arabidopsis Iron Acquisition in Response to Calcium Signaling. Developmental Cell, 48(5), 726-740.e10. https://doi.org/10.1016/j.devcel.2019.01.006

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title = "CIPK11-Dependent Phosphorylation Modulates FIT Activity to Promote Arabidopsis Iron Acquisition in Response to Calcium Signaling",

abstract = " Nutrient acquisition is entangled with growth and stress in sessile organisms. The bHLH transcription factor FIT is a key regulator of Arabidopsis iron (Fe) acquisition and post-translationally activated upon low Fe. We identified CBL-INTERACTING PROTEIN KINASE CIPK11 as a FIT interactor. Cytosolic Ca 2+ concentration and CIPK11 expression are induced by Fe deficiency. cipk11 mutant plants display compromised root Fe mobilization and seed Fe content. Fe uptake is dependent on CBL1/CBL9. CIPK11 phosphorylates FIT at Ser272, and mutation of this target site modulates FIT nuclear accumulation, homo-dimerization, interaction with bHLH039, and transcriptional activity and affects the plant's Fe-uptake ability. We propose that Ca 2+ -triggered CBL1/9-mediated activation of CIPK11 and subsequent phosphorylation of FIT shifts inactive into active FIT, allowing regulatory protein interactions in the nucleus. This biochemical link between Fe deficiency and the cellular Ca 2+ decoding machinery represents an environment-sensing mechanism to adjust nutrient uptake.",

keywords = "CBL, CIPK11, FIT, bHLH039, iron deficiency, nucleocytoplasmic partitioning, protein interaction, protein mobility, protein phosphorylation, stress",

author = "Regina Gratz and Prabha Manishankar and Rumen Ivanov and Philipp K{\"o}ster and Inga Mohr and Ksenia Trofimov and Leonie Steinhorst and Johannes Meiser and Mai, {Hans J{\"o}rg} and Maria Drerup and Sibylle Arendt and Michael Holtkamp and Uwe Karst and J{\"o}rg Kudla and Petra Bauer and Tzvetina Brumbarova",

note = "Publisher Copyright: {\textcopyright} 2019 Elsevier Inc.",

year = "2019",

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day = "11",

doi = "10.1016/j.devcel.2019.01.006",

language = "English",

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Gratz, R, Manishankar, P, Ivanov, R, Köster, P, Mohr, I, Trofimov, K, Steinhorst, L, Meiser, J, Mai, HJ, Drerup, M, Arendt, S, Holtkamp, M, Karst, U, Kudla, J, Bauer, P & Brumbarova, T 2019, 'CIPK11-Dependent Phosphorylation Modulates FIT Activity to Promote Arabidopsis Iron Acquisition in Response to Calcium Signaling', Developmental Cell, vol. 48, no. 5, pp. 726-740.e10. https://doi.org/10.1016/j.devcel.2019.01.006

TY - JOUR

T1 - CIPK11-Dependent Phosphorylation Modulates FIT Activity to Promote Arabidopsis Iron Acquisition in Response to Calcium Signaling

AU - Gratz, Regina

AU - Manishankar, Prabha

AU - Ivanov, Rumen

AU - Köster, Philipp

AU - Mohr, Inga

AU - Trofimov, Ksenia

AU - Steinhorst, Leonie

AU - Meiser, Johannes

AU - Mai, Hans Jörg

AU - Drerup, Maria

AU - Arendt, Sibylle

AU - Holtkamp, Michael

AU - Karst, Uwe

AU - Kudla, Jörg

AU - Bauer, Petra

AU - Brumbarova, Tzvetina

PY - 2019/3/11

Y1 - 2019/3/11

N2 - Nutrient acquisition is entangled with growth and stress in sessile organisms. The bHLH transcription factor FIT is a key regulator of Arabidopsis iron (Fe) acquisition and post-translationally activated upon low Fe. We identified CBL-INTERACTING PROTEIN KINASE CIPK11 as a FIT interactor. Cytosolic Ca 2+ concentration and CIPK11 expression are induced by Fe deficiency. cipk11 mutant plants display compromised root Fe mobilization and seed Fe content. Fe uptake is dependent on CBL1/CBL9. CIPK11 phosphorylates FIT at Ser272, and mutation of this target site modulates FIT nuclear accumulation, homo-dimerization, interaction with bHLH039, and transcriptional activity and affects the plant's Fe-uptake ability. We propose that Ca 2+ -triggered CBL1/9-mediated activation of CIPK11 and subsequent phosphorylation of FIT shifts inactive into active FIT, allowing regulatory protein interactions in the nucleus. This biochemical link between Fe deficiency and the cellular Ca 2+ decoding machinery represents an environment-sensing mechanism to adjust nutrient uptake.

AB - Nutrient acquisition is entangled with growth and stress in sessile organisms. The bHLH transcription factor FIT is a key regulator of Arabidopsis iron (Fe) acquisition and post-translationally activated upon low Fe. We identified CBL-INTERACTING PROTEIN KINASE CIPK11 as a FIT interactor. Cytosolic Ca 2+ concentration and CIPK11 expression are induced by Fe deficiency. cipk11 mutant plants display compromised root Fe mobilization and seed Fe content. Fe uptake is dependent on CBL1/CBL9. CIPK11 phosphorylates FIT at Ser272, and mutation of this target site modulates FIT nuclear accumulation, homo-dimerization, interaction with bHLH039, and transcriptional activity and affects the plant's Fe-uptake ability. We propose that Ca 2+ -triggered CBL1/9-mediated activation of CIPK11 and subsequent phosphorylation of FIT shifts inactive into active FIT, allowing regulatory protein interactions in the nucleus. This biochemical link between Fe deficiency and the cellular Ca 2+ decoding machinery represents an environment-sensing mechanism to adjust nutrient uptake.

KW - CBL

KW - CIPK11

KW - FIT

KW - bHLH039

KW - iron deficiency

KW - nucleocytoplasmic partitioning

KW - protein interaction

KW - protein mobility

KW - protein phosphorylation

KW - stress

UR - http://www.scopus.com/inward/record.url?scp=85062297113&partnerID=8YFLogxK

U2 - 10.1016/j.devcel.2019.01.006

DO - 10.1016/j.devcel.2019.01.006

M3 - Article

C2 - 30713077

AN - SCOPUS:85062297113

SN - 1534-5807

VL - 48

SP - 726-740.e10

JO - Developmental Cell

JF - Developmental Cell

IS - 5

ER -

CIPK11-Dependent Phosphorylation Modulates FIT Activity to Promote Arabidopsis Iron Acquisition in Response to Calcium Signaling

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Keywords

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