SnRK2 protein kinases and mRNA decapping machinery control root development and response to salt

Dorota Kawa, A.J. Meyer, Henk L. Dekker, Ahmed Abd-El-Haliem, Kris Gevaert, Eveline Van De Slijke, Justyna Maszkowska, Maria Bucholc, Grazyna Dobrowolska, Geert de Jaeger, Robert C. Schuurink, Michel A. Haring, Christa Testerink

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

SNF1-RELATED PROTEIN KINASES 2 (SnRK2) are important components of early osmotic and salt stress signaling pathways in plants. The Arabidopsis (Arabidopsis thaliana) SnRK2 family comprises the abscisic acid (ABA)-activated protein kinases SnRK2.2, SnRK2.3, SnRK2.6, SnRK2.7, and SnRK2.8, and the ABA-independent subclass 1 protein kinases SnRK2.1, SnRK2.4, SnRK2.5, SnRK2.9, and SnRK2.10. ABA-independent SnRK2s act at the post-transcriptional level via phosphorylation of VARICOSE (VCS), a member of the mRNA decapping complex, that catalyzes the first step of 5'mRNA decay. Here, we identified VCS and VARICOSE RELATED (VCR) as interactors and phosphorylation targets of SnRK2.5, SnRK2.6, and SnRK2.10. All three protein kinases phosphorylated Ser645 and Ser1156 of VCS, while SnRK2.6 and SnRK2.10 also phosphorylated VCS Ser692 and Ser680 of VCR. We showed that subclass 1 SnRK2s, VCS, and 5' EXORIBONUCLEASE 4 (XRN4) are involved in regulating root growth under control conditions as well as modulating root system architecture in response to salt stress. Our results suggest interesting patterns of redundancy within subclass 1 SnRK2 protein kinases, with SnRK2.1, SnRK2.5 and SnRK2.9 controlling root growth under non-stress conditions and SnRK2.4 and SnRK2.10 acting mostly in response to salinity. We propose that subclass 1 SnRK2s function in root development under salt stress by affecting the transcript levels of aquaporins, as well as CYP79B2, an enzyme involved in auxin biosynthesis.
Original languageEnglish
JournalPlant Physiology
Volume182
Issue number1
DOIs
Publication statusPublished - 1 Jan 2020

Fingerprint

protein kinases
Abscisic Acid
Protein Kinases
Salts
salts
Messenger RNA
Arabidopsis
salt stress
abscisic acid
Phosphorylation
Aquaporins
Indoleacetic Acids
Osmotic Pressure
Salinity
RNA Stability
Growth
root growth
phosphorylation
aquaporins
osmotic stress

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Kawa, Dorota ; Meyer, A.J. ; Dekker, Henk L. ; Abd-El-Haliem, Ahmed ; Gevaert, Kris ; Van De Slijke, Eveline ; Maszkowska, Justyna ; Bucholc, Maria ; Dobrowolska, Grazyna ; de Jaeger, Geert ; Schuurink, Robert C. ; Haring, Michel A. ; Testerink, Christa. / SnRK2 protein kinases and mRNA decapping machinery control root development and response to salt. In: Plant Physiology. 2020 ; Vol. 182, No. 1.
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abstract = "SNF1-RELATED PROTEIN KINASES 2 (SnRK2) are important components of early osmotic and salt stress signaling pathways in plants. The Arabidopsis (Arabidopsis thaliana) SnRK2 family comprises the abscisic acid (ABA)-activated protein kinases SnRK2.2, SnRK2.3, SnRK2.6, SnRK2.7, and SnRK2.8, and the ABA-independent subclass 1 protein kinases SnRK2.1, SnRK2.4, SnRK2.5, SnRK2.9, and SnRK2.10. ABA-independent SnRK2s act at the post-transcriptional level via phosphorylation of VARICOSE (VCS), a member of the mRNA decapping complex, that catalyzes the first step of 5'mRNA decay. Here, we identified VCS and VARICOSE RELATED (VCR) as interactors and phosphorylation targets of SnRK2.5, SnRK2.6, and SnRK2.10. All three protein kinases phosphorylated Ser645 and Ser1156 of VCS, while SnRK2.6 and SnRK2.10 also phosphorylated VCS Ser692 and Ser680 of VCR. We showed that subclass 1 SnRK2s, VCS, and 5' EXORIBONUCLEASE 4 (XRN4) are involved in regulating root growth under control conditions as well as modulating root system architecture in response to salt stress. Our results suggest interesting patterns of redundancy within subclass 1 SnRK2 protein kinases, with SnRK2.1, SnRK2.5 and SnRK2.9 controlling root growth under non-stress conditions and SnRK2.4 and SnRK2.10 acting mostly in response to salinity. We propose that subclass 1 SnRK2s function in root development under salt stress by affecting the transcript levels of aquaporins, as well as CYP79B2, an enzyme involved in auxin biosynthesis.",
author = "Dorota Kawa and A.J. Meyer and Dekker, {Henk L.} and Ahmed Abd-El-Haliem and Kris Gevaert and {Van De Slijke}, Eveline and Justyna Maszkowska and Maria Bucholc and Grazyna Dobrowolska and {de Jaeger}, Geert and Schuurink, {Robert C.} and Haring, {Michel A.} and Christa Testerink",
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Kawa, D, Meyer, AJ, Dekker, HL, Abd-El-Haliem, A, Gevaert, K, Van De Slijke, E, Maszkowska, J, Bucholc, M, Dobrowolska, G, de Jaeger, G, Schuurink, RC, Haring, MA & Testerink, C 2020, 'SnRK2 protein kinases and mRNA decapping machinery control root development and response to salt', Plant Physiology, vol. 182, no. 1. https://doi.org/10.1104/pp.19.00818

SnRK2 protein kinases and mRNA decapping machinery control root development and response to salt. / Kawa, Dorota; Meyer, A.J.; Dekker, Henk L.; Abd-El-Haliem, Ahmed; Gevaert, Kris; Van De Slijke, Eveline; Maszkowska, Justyna; Bucholc, Maria; Dobrowolska, Grazyna; de Jaeger, Geert; Schuurink, Robert C.; Haring, Michel A.; Testerink, Christa.

In: Plant Physiology, Vol. 182, No. 1, 01.01.2020.

Research output: Contribution to journalArticleAcademicpeer-review

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T1 - SnRK2 protein kinases and mRNA decapping machinery control root development and response to salt

AU - Kawa, Dorota

AU - Meyer, A.J.

AU - Dekker, Henk L.

AU - Abd-El-Haliem, Ahmed

AU - Gevaert, Kris

AU - Van De Slijke, Eveline

AU - Maszkowska, Justyna

AU - Bucholc, Maria

AU - Dobrowolska, Grazyna

AU - de Jaeger, Geert

AU - Schuurink, Robert C.

AU - Haring, Michel A.

AU - Testerink, Christa

N1 - Postprint staat op de W-schijf

PY - 2020/1/1

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N2 - SNF1-RELATED PROTEIN KINASES 2 (SnRK2) are important components of early osmotic and salt stress signaling pathways in plants. The Arabidopsis (Arabidopsis thaliana) SnRK2 family comprises the abscisic acid (ABA)-activated protein kinases SnRK2.2, SnRK2.3, SnRK2.6, SnRK2.7, and SnRK2.8, and the ABA-independent subclass 1 protein kinases SnRK2.1, SnRK2.4, SnRK2.5, SnRK2.9, and SnRK2.10. ABA-independent SnRK2s act at the post-transcriptional level via phosphorylation of VARICOSE (VCS), a member of the mRNA decapping complex, that catalyzes the first step of 5'mRNA decay. Here, we identified VCS and VARICOSE RELATED (VCR) as interactors and phosphorylation targets of SnRK2.5, SnRK2.6, and SnRK2.10. All three protein kinases phosphorylated Ser645 and Ser1156 of VCS, while SnRK2.6 and SnRK2.10 also phosphorylated VCS Ser692 and Ser680 of VCR. We showed that subclass 1 SnRK2s, VCS, and 5' EXORIBONUCLEASE 4 (XRN4) are involved in regulating root growth under control conditions as well as modulating root system architecture in response to salt stress. Our results suggest interesting patterns of redundancy within subclass 1 SnRK2 protein kinases, with SnRK2.1, SnRK2.5 and SnRK2.9 controlling root growth under non-stress conditions and SnRK2.4 and SnRK2.10 acting mostly in response to salinity. We propose that subclass 1 SnRK2s function in root development under salt stress by affecting the transcript levels of aquaporins, as well as CYP79B2, an enzyme involved in auxin biosynthesis.

AB - SNF1-RELATED PROTEIN KINASES 2 (SnRK2) are important components of early osmotic and salt stress signaling pathways in plants. The Arabidopsis (Arabidopsis thaliana) SnRK2 family comprises the abscisic acid (ABA)-activated protein kinases SnRK2.2, SnRK2.3, SnRK2.6, SnRK2.7, and SnRK2.8, and the ABA-independent subclass 1 protein kinases SnRK2.1, SnRK2.4, SnRK2.5, SnRK2.9, and SnRK2.10. ABA-independent SnRK2s act at the post-transcriptional level via phosphorylation of VARICOSE (VCS), a member of the mRNA decapping complex, that catalyzes the first step of 5'mRNA decay. Here, we identified VCS and VARICOSE RELATED (VCR) as interactors and phosphorylation targets of SnRK2.5, SnRK2.6, and SnRK2.10. All three protein kinases phosphorylated Ser645 and Ser1156 of VCS, while SnRK2.6 and SnRK2.10 also phosphorylated VCS Ser692 and Ser680 of VCR. We showed that subclass 1 SnRK2s, VCS, and 5' EXORIBONUCLEASE 4 (XRN4) are involved in regulating root growth under control conditions as well as modulating root system architecture in response to salt stress. Our results suggest interesting patterns of redundancy within subclass 1 SnRK2 protein kinases, with SnRK2.1, SnRK2.5 and SnRK2.9 controlling root growth under non-stress conditions and SnRK2.4 and SnRK2.10 acting mostly in response to salinity. We propose that subclass 1 SnRK2s function in root development under salt stress by affecting the transcript levels of aquaporins, as well as CYP79B2, an enzyme involved in auxin biosynthesis.

U2 - 10.1104/pp.19.00818

DO - 10.1104/pp.19.00818

M3 - Article

VL - 182

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JF - Plant Physiology

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