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Title: The C-Terminal Domains SnRK2 Box and ABA Box Have a Role in Sugarcane SnRK2s Auto-Activation and Activity

Abstract

Resistance to drought stress is fundamental to plant survival and development. Abscisic acid (ABA) is one of the major hormones involved in different types of abiotic and biotic stress responses. ABA intracellular signaling has been extensively explored in Arabidopsis thaliana and occurs via a phosphorylation cascade mediated by three related protein kinases, denominated SnRK2s (SNF1-related protein kinases). However, the role of ABA signaling and the biochemistry of SnRK2 in crop plants remains underexplored. Considering the importance of the ABA hormone in abiotic stress tolerance, here we investigated the regulatory mechanism of sugarcane SnRK2s—known as stress/ABAactivated protein kinases (SAPKs). The crystal structure of ScSAPK10 revealed the characteristic SnRK2 family architecture, in which the regulatory SnRK2 box interacts with the kinase domain αC helix. To study sugarcane SnRK2 regulation, we produced a series of mutants for the protein regulatory domains SnRK2 box and ABA box. Mutations in ScSAPK8 SnRK2 box aimed at perturbing its interaction with the protein kinase domain reduced protein kinase activity in vitro. On the other hand, mutations to ScSAPK ABA box did not impact protein kinase activity but did alter the protein autophosphorylation pattern. Taken together, our results demonstrate that both SnRK2 and ABA boxes might play amore » role in sugarcane SnRK2 function.« less

Authors:
 [1];  [2];  [3];  [2];  [4];  [2];  [5];  [1];  [2]
  1. State Univ. of Campinas (Brazil)
  2. Univ. Estadual de Campinas (UNICAMP) (Brazil)
  3. MaRS Center, Toronto, ON (Canada)
  4. Univ. Estadual de Campinas (UNICAMP) (Brazil); Univ. of Oxford (United Kingdom)
  5. Univ. of Oxford (United Kingdom)
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1600826
Grant/Contract Number:  
AC02-06CH11357
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Plant Science
Additional Journal Information:
Journal Volume: 10; Journal Issue: 09, 2019; Journal ID: ISSN 1664-462X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
ENGLISH
Subject:
59 BASIC BIOLOGICAL SCIENCES; abscisic acid; abiotic stress; SnRK2; crop plant; kinase regulation; sugarcane

Citation Formats

Righetto, Germanna Lima, Sriranganadane, Dev, Halabelian, Levon, Chiodi, Carla G., Elkins, Jonathan M., Massirer, Katlin B., Gileadi, Opher, Menossi, Marcelo, and Couñago, Rafael M. The C-Terminal Domains SnRK2 Box and ABA Box Have a Role in Sugarcane SnRK2s Auto-Activation and Activity. United States: N. p., 2019. Web. doi:10.3389/fpls.2019.01105.
Righetto, Germanna Lima, Sriranganadane, Dev, Halabelian, Levon, Chiodi, Carla G., Elkins, Jonathan M., Massirer, Katlin B., Gileadi, Opher, Menossi, Marcelo, & Couñago, Rafael M. The C-Terminal Domains SnRK2 Box and ABA Box Have a Role in Sugarcane SnRK2s Auto-Activation and Activity. United States. https://doi.org/10.3389/fpls.2019.01105
Righetto, Germanna Lima, Sriranganadane, Dev, Halabelian, Levon, Chiodi, Carla G., Elkins, Jonathan M., Massirer, Katlin B., Gileadi, Opher, Menossi, Marcelo, and Couñago, Rafael M. Tue . "The C-Terminal Domains SnRK2 Box and ABA Box Have a Role in Sugarcane SnRK2s Auto-Activation and Activity". United States. https://doi.org/10.3389/fpls.2019.01105. https://www.osti.gov/servlets/purl/1600826.
@article{osti_1600826,
title = {The C-Terminal Domains SnRK2 Box and ABA Box Have a Role in Sugarcane SnRK2s Auto-Activation and Activity},
author = {Righetto, Germanna Lima and Sriranganadane, Dev and Halabelian, Levon and Chiodi, Carla G. and Elkins, Jonathan M. and Massirer, Katlin B. and Gileadi, Opher and Menossi, Marcelo and Couñago, Rafael M.},
abstractNote = {Resistance to drought stress is fundamental to plant survival and development. Abscisic acid (ABA) is one of the major hormones involved in different types of abiotic and biotic stress responses. ABA intracellular signaling has been extensively explored in Arabidopsis thaliana and occurs via a phosphorylation cascade mediated by three related protein kinases, denominated SnRK2s (SNF1-related protein kinases). However, the role of ABA signaling and the biochemistry of SnRK2 in crop plants remains underexplored. Considering the importance of the ABA hormone in abiotic stress tolerance, here we investigated the regulatory mechanism of sugarcane SnRK2s—known as stress/ABAactivated protein kinases (SAPKs). The crystal structure of ScSAPK10 revealed the characteristic SnRK2 family architecture, in which the regulatory SnRK2 box interacts with the kinase domain αC helix. To study sugarcane SnRK2 regulation, we produced a series of mutants for the protein regulatory domains SnRK2 box and ABA box. Mutations in ScSAPK8 SnRK2 box aimed at perturbing its interaction with the protein kinase domain reduced protein kinase activity in vitro. On the other hand, mutations to ScSAPK ABA box did not impact protein kinase activity but did alter the protein autophosphorylation pattern. Taken together, our results demonstrate that both SnRK2 and ABA boxes might play a role in sugarcane SnRK2 function.},
doi = {10.3389/fpls.2019.01105},
journal = {Frontiers in Plant Science},
number = 09, 2019,
volume = 10,
place = {United States},
year = {2019},
month = {9}
}

Works referenced in this record:

High-throughput production of human proteins for crystallization: The SGC experience
journal, October 2010

  • Savitsky, Pavel; Bray, James; Cooper, Christopher D. O.
  • Journal of Structural Biology, Vol. 172, Issue 1
  • DOI: 10.1016/j.jsb.2010.06.008

A gate–latch–lock mechanism for hormone signalling by abscisic acid receptors
journal, November 2009

  • Melcher, Karsten; Ng, Ley-Moy; Zhou, X. Edward
  • Nature, Vol. 462, Issue 7273
  • DOI: 10.1038/nature08613

Overview of the CCP 4 suite and current developments
journal, March 2011

  • Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D.
  • Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4
  • DOI: 10.1107/S0907444910045749

ZmOST1 mediates abscisic acid regulation of guard cell ion channels and drought stress responses
journal, November 2018

  • Wu, Qiqi; Wang, Mei; Shen, Jianlin
  • Journal of Integrative Plant Biology, Vol. 61, Issue 4
  • DOI: 10.1111/jipb.12714

The EMBL-EBI search and sequence analysis tools APIs in 2019
journal, April 2019

  • Madeira, Fábio; Park, Young mi; Lee, Joon
  • Nucleic Acids Research, Vol. 47, Issue W1
  • DOI: 10.1093/nar/gkz268

Arabidopsis OST1 Protein Kinase Mediates the Regulation of Stomatal Aperture by Abscisic Acid and Acts Upstream of Reactive Oxygen Species Production
journal, November 2002

  • Mustilli, Anna-Chiara; Merlot, Sylvain; Vavasseur, Alain
  • The Plant Cell, Vol. 14, Issue 12
  • DOI: 10.1105/tpc.007906

Identification and Bioinformatics Analysis of SnRK2 and CIPK Family Genes in Sorghum
journal, January 2010


The PRIDE database and related tools and resources in 2019: improving support for quantification data
journal, November 2018

  • Perez-Riverol, Yasset; Csordas, Attila; Bai, Jingwen
  • Nucleic Acids Research, Vol. 47, Issue D1
  • DOI: 10.1093/nar/gky1106

ABA-Activated SnRK2 Protein Kinase is Required for Dehydration Stress Signaling in Arabidopsis
journal, December 2002

  • Yoshida, Riichiro; Hobo, Tokunori; Ichimura, Kazuya
  • Plant and Cell Physiology, Vol. 43, Issue 12
  • DOI: 10.1093/pcp/pcf188

Structural basis of abscisic acid signalling
journal, October 2009

  • Miyazono, Ken-ichi; Miyakawa, Takuya; Sawano, Yoriko
  • Nature, Vol. 462, Issue 7273
  • DOI: 10.1038/nature08583

Structure of Ligand-Bound Intermediates of Crop ABA Receptors Highlights PP2C as Necessary ABA Co-receptor
journal, September 2017

  • Moreno-Alvero, María; Yunta, Cristina; Gonzalez-Guzman, Miguel
  • Molecular Plant, Vol. 10, Issue 9
  • DOI: 10.1016/j.molp.2017.07.004

Protein Phosphatases 2C Regulate the Activation of the Snf1-Related Kinase OST1 by Abscisic Acid in Arabidopsis
journal, October 2009

  • Vlad, Florina; Rubio, Silvia; Rodrigues, Americo
  • The Plant Cell, Vol. 21, Issue 10
  • DOI: 10.1105/tpc.109.069179

Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis
journal, September 2009

  • Umezawa, T.; Sugiyama, N.; Mizoguchi, M.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 41
  • DOI: 10.1073/pnas.0907095106

PHENIX : building new software for automated crystallographic structure determination
journal, October 2002

  • Adams, Paul D.; Grosse-Kunstleve, Ralf W.; Hung, Li-Wei
  • Acta Crystallographica Section D Biological Crystallography, Vol. 58, Issue 11
  • DOI: 10.1107/S0907444902016657

The Regulatory Domain of SRK2E/OST1/SnRK2.6 Interacts with ABI1 and Integrates Abscisic Acid (ABA) and Osmotic Stress Signals Controlling Stomatal Closure in Arabidopsis
journal, December 2005

  • Yoshida, Riichiro; Umezawa, Taishi; Mizoguchi, Tsuyoshi
  • Journal of Biological Chemistry, Vol. 281, Issue 8
  • DOI: 10.1074/jbc.M509820200

Structural basis for basal activity and autoactivation of abscisic acid (ABA) signaling SnRK2 kinases
journal, December 2011

  • Ng, L. -M.; Soon, F. -F.; Zhou, X. E.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 52
  • DOI: 10.1073/pnas.1118651109

XDS
journal, January 2010

  • Kabsch, Wolfgang
  • Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2
  • DOI: 10.1107/S0907444909047337

Differential Activation of the Rice Sucrose Nonfermenting1–Related Protein Kinase2 Family by Hyperosmotic Stress and Abscisic Acid
journal, April 2004

  • Kobayashi, Yuhko; Yamamoto, Shuhei; Minami, Hideyuki
  • The Plant Cell, Vol. 16, Issue 5
  • DOI: 10.1105/tpc.019943

In vitro reconstitution of an abscisic acid signalling pathway
journal, November 2009

  • Fujii, Hiroaki; Chinnusamy, Viswanathan; Rodrigues, Americo
  • Nature, Vol. 462, Issue 7273
  • DOI: 10.1038/nature08599

SMART, a simple modular architecture research tool: Identification of signaling domains
journal, May 1998

  • Schultz, J.; Milpetz, F.; Bork, P.
  • Proceedings of the National Academy of Sciences, Vol. 95, Issue 11
  • DOI: 10.1073/pnas.95.11.5857

Identification of Two Protein Kinases Required for Abscisic Acid Regulation of Seed Germination, Root Growth, and Gene Expression in Arabidopsis
journal, February 2007

  • Fujii, Hiroaki; Verslues, Paul E.; Zhu, Jian-Kang
  • The Plant Cell, Vol. 19, Issue 2
  • DOI: 10.1105/tpc.106.048538

Molecular Mimicry Regulates ABA Signaling by SnRK2 Kinases and PP2C Phosphatases
journal, November 2011


The Structure of Arabidopsis thaliana OST1 Provides Insights into the Kinase Regulation Mechanism in Response to Osmotic Stress
journal, November 2011

  • Yunta, Cristina; Martínez-Ripoll, Martín; Zhu, Jian-Kang
  • Journal of Molecular Biology, Vol. 414, Issue 1
  • DOI: 10.1016/j.jmb.2011.09.041

The Pfam protein families database: towards a more sustainable future
journal, December 2015

  • Finn, Robert D.; Coggill, Penelope; Eberhardt, Ruth Y.
  • Nucleic Acids Research, Vol. 44, Issue D1
  • DOI: 10.1093/nar/gkv1344

Structural insights into the mechanism of abscisic acid signaling by PYL proteins
journal, November 2009

  • Yin, Ping; Fan, He; Hao, Qi
  • Nature Structural & Molecular Biology, Vol. 16, Issue 12
  • DOI: 10.1038/nsmb.1730

MolProbity : all-atom structure validation for macromolecular crystallography
journal, December 2009

  • Chen, Vincent B.; Arendall, W. Bryan; Headd, Jeffrey J.
  • Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1
  • DOI: 10.1107/S0907444909042073

Arabidopsis mutant deficient in 3 abscisic acid-activated protein kinases reveals critical roles in growth, reproduction, and stress
journal, May 2009

  • Fujii, H.; Zhu, J. -K.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 20
  • DOI: 10.1073/pnas.0903144106

The rapid generation of mutation data matrices from protein sequences
journal, January 1992


Different phosphorylation mechanisms are involved in the activation of sucrose non-fermenting 1 related protein kinases 2 by osmotic stresses and abscisic acid
journal, November 2006

  • Boudsocq, Marie; Droillard, Marie-Jo; Barbier-Brygoo, Hélène
  • Plant Molecular Biology, Vol. 63, Issue 4
  • DOI: 10.1007/s11103-006-9103-1

Features and development of Coot
journal, March 2010

  • Emsley, P.; Lohkamp, B.; Scott, W. G.
  • Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4
  • DOI: 10.1107/S0907444910007493

Overexpression of a Common Wheat Gene TaSnRK2.8 Enhances Tolerance to Drought, Salt and Low Temperature in Arabidopsis
journal, December 2010


REFMAC 5 for the refinement of macromolecular crystal structures
journal, March 2011

  • Murshudov, Garib N.; Skubák, Pavol; Lebedev, Andrey A.
  • Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4
  • DOI: 10.1107/S0907444911001314

Mechanism of CDK activation revealed by the structure of a cyclinA-CDK2 complex
journal, July 1995

  • Jeffrey, Philip D.; Russo, Alicia A.; Polyak, Kornelia
  • Nature, Vol. 376, Issue 6538
  • DOI: 10.1038/376313a0

Identification of Nine Sucrose Nonfermenting 1-related Protein Kinases 2 Activated by Hyperosmotic and Saline Stresses in Arabidopsis thaliana
journal, July 2004

  • Boudsocq, M.; Barbier-Brygoo, H.; Lauriere, C.
  • Journal of Biological Chemistry, Vol. 279, Issue 40
  • DOI: 10.1074/jbc.M405259200

Regulators of PP2C Phosphatase Activity Function as Abscisic Acid Sensors
journal, April 2009


MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets
journal, March 2016

  • Kumar, Sudhir; Stecher, Glen; Tamura, Koichiro
  • Molecular Biology and Evolution, Vol. 33, Issue 7
  • DOI: 10.1093/molbev/msw054

Identification of Features Regulating OST1 Kinase Activity and OST1 Function in Guard Cells
journal, June 2006

  • Belin, Christophe; de Franco, Pierre-Olivier; Bourbousse, Clara
  • Plant Physiology, Vol. 141, Issue 4
  • DOI: 10.1104/pp.106.079327

Regulation of Protein Kinases
journal, September 2004


Three SnRK2 Protein Kinases are the Main Positive Regulators of Abscisic Acid Signaling in Response to Water Stress in Arabidopsis
journal, September 2009

  • Fujita, Yasunari; Nakashima, Kazuo; Yoshida, Takuya
  • Plant and Cell Physiology, Vol. 50, Issue 12
  • DOI: 10.1093/pcp/pcp147

GSK3-like kinases positively modulate abscisic acid signaling through phosphorylating subgroup III SnRK2s in Arabidopsis
journal, June 2014

  • Cai, Zhenying; Liu, Jingjing; Wang, Haijiao
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 26
  • DOI: 10.1073/pnas.1316717111

Molecular Basis of the Core Regulatory Network in ABA Responses: Sensing, Signaling and Transport
journal, October 2010

  • Umezawa, T.; Nakashima, K.; Miyakawa, T.
  • Plant and Cell Physiology, Vol. 51, Issue 11
  • DOI: 10.1093/pcp/pcq156

Genome-wide identification and characterization of SnRK2 gene family in cotton (Gossypium hirsutum L.)
journal, June 2017


SnRK2 Protein Kinases—Key Regulators of Plant Response to Abiotic Stresses
journal, December 2011

  • Kulik, Anna; Wawer, Izabela; Krzywińska, Ewa
  • OMICS: A Journal of Integrative Biology, Vol. 15, Issue 12
  • DOI: 10.1089/omi.2011.0091

The Maize OST1 Kinase Homolog Phosphorylates and Regulates the Maize SNAC1-Type Transcription Factor
journal, February 2013


The nuts and bolts of AGC protein kinases
journal, January 2010

  • Pearce, Laura R.; Komander, David; Alessi, Dario R.
  • Nature Reviews Molecular Cell Biology, Vol. 11, Issue 1
  • DOI: 10.1038/nrm2822

Cloning and characterization of the SnRK2 gene family from Zea mays
journal, September 2008


Analysis and Functional Annotation of an Expressed Sequence Tag Collection for Tropical Crop Sugarcane
journal, December 2003