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

Righetto, Germanna Lima; Sriranganadane, Dev; Halabelian, Levon; Chiodi, Carla G.; Elkins, Jonathan M.; Massirer, Katlin B.; Gileadi, Opher; Menossi, Marcelo; Couñago, Rafael M.

doi:10.3389/fpls.2019.01105

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

Journal Article · 17 September 2019 · Frontiers in Plant Science

DOI: https://doi.org/10.3389/fpls.2019.01105 · OSTI ID:1600826

Righetto, Germanna Lima ^[1]; Sriranganadane, Dev ^[2]; Halabelian, Levon ^[3]; Chiodi, Carla G. ^[2]; Elkins, Jonathan M. ^[4]; Massirer, Katlin B. ^[2]; Gileadi, Opher ^[5]; Menossi, Marcelo ^[1]; Couñago, Rafael M. ^[2]

State Univ. of Campinas (Brazil)
Univ. Estadual de Campinas (UNICAMP) (Brazil)
MaRS Center, Toronto, ON (Canada)
Univ. Estadual de Campinas (UNICAMP) (Brazil); Univ. of Oxford (United Kingdom)
Univ. of Oxford (United Kingdom)

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.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1600826

Journal Information:: Frontiers in Plant Science, Journal Name: Frontiers in Plant Science Journal Issue: 09, 2019 Vol. 10; ISSN 1664-462X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

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Structure of Ligand-Bound Intermediates of Crop ABA Receptors Highlights PP2C as Necessary ABA Co-receptor Moreno-Alvero, María; Yunta, Cristina; Gonzalez-Guzman, Miguel Molecular Plant, Vol. 10, Issue 9 https://doi.org/10.1016/j.molp.2017.07.004	journal	September 2017
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Structural insights into the mechanism of abscisic acid signaling by PYL proteins Yin, Ping; Fan, He; Hao, Qi Nature Structural & Molecular Biology, Vol. 16, Issue 12 https://doi.org/10.1038/nsmb.1730	journal	November 2009
Arabidopsis mutant deficient in 3 abscisic acid-activated protein kinases reveals critical roles in growth, reproduction, and stress Fujii, H.; Zhu, J. -K. Proceedings of the National Academy of Sciences, Vol. 106, Issue 20 https://doi.org/10.1073/pnas.0903144106	journal	May 2009
Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis Umezawa, T.; Sugiyama, N.; Mizoguchi, M. Proceedings of the National Academy of Sciences, Vol. 106, Issue 41 https://doi.org/10.1073/pnas.0907095106	journal	September 2009
Structural basis for basal activity and autoactivation of abscisic acid (ABA) signaling SnRK2 kinases Ng, L. -M.; Soon, F. -F.; Zhou, X. E. Proceedings of the National Academy of Sciences, Vol. 108, Issue 52 https://doi.org/10.1073/pnas.1118651109	journal	December 2011
GSK3-like kinases positively modulate abscisic acid signaling through phosphorylating subgroup III SnRK2s in Arabidopsis Cai, Zhenying; Liu, Jingjing; Wang, Haijiao Proceedings of the National Academy of Sciences, Vol. 111, Issue 26 https://doi.org/10.1073/pnas.1316717111	journal	June 2014
SMART, a simple modular architecture research tool: Identification of signaling domains Schultz, J.; Milpetz, F.; Bork, P. Proceedings of the National Academy of Sciences, Vol. 95, Issue 11 https://doi.org/10.1073/pnas.95.11.5857	journal	May 1998
Identification of Nine Sucrose Nonfermenting 1-related Protein Kinases 2 Activated by Hyperosmotic and Saline Stresses in Arabidopsis thaliana Boudsocq, M.; Barbier-Brygoo, H.; Lauriere, C. Journal of Biological Chemistry, Vol. 279, Issue 40 https://doi.org/10.1074/jbc.M405259200	journal	July 2004
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 Yoshida, Riichiro; Umezawa, Taishi; Mizoguchi, Tsuyoshi Journal of Biological Chemistry, Vol. 281, Issue 8 https://doi.org/10.1074/jbc.M509820200	journal	December 2005
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Three SnRK2 Protein Kinases are the Main Positive Regulators of Abscisic Acid Signaling in Response to Water Stress in Arabidopsis Fujita, Yasunari; Nakashima, Kazuo; Yoshida, Takuya Plant and Cell Physiology, Vol. 50, Issue 12 https://doi.org/10.1093/pcp/pcp147	journal	September 2009
Molecular Basis of the Core Regulatory Network in ABA Responses: Sensing, Signaling and Transport Umezawa, T.; Nakashima, K.; Miyakawa, T. Plant and Cell Physiology, Vol. 51, Issue 11 https://doi.org/10.1093/pcp/pcq156	journal	October 2010
Analysis and Functional Annotation of an Expressed Sequence Tag Collection for Tropical Crop Sugarcane Vettore, A. L. Genome Research, Vol. 13, Issue 12 https://doi.org/10.1101/gr.1532103	journal	December 2003
Identification of Features Regulating OST1 Kinase Activity and OST1 Function in Guard Cells Belin, Christophe; de Franco, Pierre-Olivier; Bourbousse, Clara Plant Physiology, Vol. 141, Issue 4 https://doi.org/10.1104/pp.106.079327	journal	June 2006
Arabidopsis OST1 Protein Kinase Mediates the Regulation of Stomatal Aperture by Abscisic Acid and Acts Upstream of Reactive Oxygen Species Production Mustilli, Anna-Chiara; Merlot, Sylvain; Vavasseur, Alain The Plant Cell, Vol. 14, Issue 12 https://doi.org/10.1105/tpc.007906	journal	November 2002
Differential Activation of the Rice Sucrose Nonfermenting1–Related Protein Kinase2 Family by Hyperosmotic Stress and Abscisic Acid Kobayashi, Yuhko; Yamamoto, Shuhei; Minami, Hideyuki The Plant Cell, Vol. 16, Issue 5 https://doi.org/10.1105/tpc.019943	journal	April 2004
Identification of Two Protein Kinases Required for Abscisic Acid Regulation of Seed Germination, Root Growth, and Gene Expression in Arabidopsis Fujii, Hiroaki; Verslues, Paul E.; Zhu, Jian-Kang The Plant Cell, Vol. 19, Issue 2 https://doi.org/10.1105/tpc.106.048538	journal	February 2007
Protein Phosphatases 2C Regulate the Activation of the Snf1-Related Kinase OST1 by Abscisic Acid in Arabidopsis Vlad, Florina; Rubio, Silvia; Rodrigues, Americo The Plant Cell, Vol. 21, Issue 10 https://doi.org/10.1105/tpc.109.069179	journal	October 2009
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MolProbity : all-atom structure validation for macromolecular crystallography Chen, Vincent B.; Arendall, W. Bryan; Headd, Jeffrey J. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1 https://doi.org/10.1107/S0907444909042073	journal	December 2009
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Overview of the CCP 4 suite and current developments Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444910045749	journal	March 2011
REFMAC 5 for the refinement of macromolecular crystal structures Murshudov, Garib N.; Skubák, Pavol; Lebedev, Andrey A. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444911001314	journal	March 2011
ZmOST1 mediates abscisic acid regulation of guard cell ion channels and drought stress responses Wu, Qiqi; Wang, Mei; Shen, Jianlin Journal of Integrative Plant Biology, Vol. 61, Issue 4 https://doi.org/10.1111/jipb.12714	journal	November 2018
Regulators of PP2C Phosphatase Activity Function as Abscisic Acid Sensors Ma, Y.; Szostkiewicz, I.; Korte, A. Science https://doi.org/10.1126/science.1172408	journal	April 2009
Abscisic Acid Inhibits Type 2C Protein Phosphatases via the PYR/PYL Family of START Proteins Park, S. -Y.; Fung, P.; Nishimura, N. Science https://doi.org/10.1126/science.1173041	journal	April 2009
Molecular Mimicry Regulates ABA Signaling by SnRK2 Kinases and PP2C Phosphatases Soon, Fen-Fen; Ng, Ley-Moy; Zhou, X. Edward Science, Vol. 335, Issue 6064 https://doi.org/10.1126/science.1215106	journal	November 2011
Genome-wide identification and characterization of SnRK2 gene family in cotton (Gossypium hirsutum L.) Liu, Zhao; Ge, Xiaoyang; Yang, Zuoren BMC Genetics, Vol. 18, Issue 1 https://doi.org/10.1186/s12863-017-0517-3	journal	June 2017
Overexpression of a Common Wheat Gene TaSnRK2.8 Enhances Tolerance to Drought, Salt and Low Temperature in Arabidopsis Zhang, Hongying; Mao, Xinguo; Wang, Chengshe PLoS ONE, Vol. 5, Issue 12 https://doi.org/10.1371/journal.pone.0016041	journal	December 2010
The Maize OST1 Kinase Homolog Phosphorylates and Regulates the Maize SNAC1-Type Transcription Factor Vilela, Belmiro; Moreno-Cortés, Alicia; Rabissi, Agnese PLoS ONE, Vol. 8, Issue 2 https://doi.org/10.1371/journal.pone.0058105	journal	February 2013
Genome-wide identification and characterization of SnRK2 gene family in cotton (Gossypium hirsutum L.) Liu, Zhao; Ge, Xiaoyang; Yang, Zuoren figshare https://doi.org/10.6084/m9.figshare.c.3801559.v1	collection	January 2017

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SnRK2
abiotic stress
abscisic acid
crop plant
kinase regulation
sugarcane

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

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