Protein phosphatases meet reactive oxygen species in plant signaling networks

doi:10.1016/j.envexpbot.2018.10.032

Environmental and Experimental Botany

Volume 161, May 2019, Pages 26-40

https://doi.org/10.1016/j.envexpbot.2018.10.032 Get rights and content

Highlights

•
Cellular redox levels exist in a dynamic state.
•
Oxidative damage is a common observation in biotic and abiotic stresses.
•
ROS has a dual nature, as a damage control agent and as a signal transducer.
•
Protein phosphatases act as regulatory molecules in diverse signaling cascades.
•
Phosphatases are inhibited directly by ROS.

Abstract

The cellular redox state is vital for the survival of all living systems. The dynamic nature of reactive oxygen species (ROS) are reflected in their functioning both as a damage causal and control agent. They are known primarily for causing oxidative damage and induction of programmed cell death (PCD) in case of pathogen attacks to prevent pathogen proliferation, while at low levels, they act as signal transducer(s) in different signaling pathways. Protein phosphatase(s) and kinase(s) co-ordinate the reversible post-translational modification of proteins, thereby, regulating a number of signaling pathways. In plant systems, protein kinases outnumber the protein phosphatases, which is countered by the diverse functional assemblage of the latter. Protein phosphatases are redox-regulated through reversible oxidation of critical Cysteine (Cys) residues leading to their activation and inactivation. Thus, their diversity and critical involvement in a number of cellular processes, which require redox homeostasis as a crucial element, brings them under the control of redox regulation. The observations made with regard to their involvement in photo-oxidative stress and responses involving ROS as signaling molecules, make a strong case for the potential of protein phosphatases in ROS signaling, with an emphasis on stress biology. In this review, we present the common ground on which ROS and protein phosphatases operate in view of their regulatory functions.

Graphical abstract

Introduction

Protein phosphorylation, an important reversible post-translational modification involved in the regulation of a number of critical cellular processes, occurs in a coordinated manner through two classes of enzymes, the kinases and the phosphatases. The kinases transfer the γ-phosphoryl group of donor ATP to the acceptor protein side chains, while the phosphatases dephosphorylate the phosphoproteins (Barford, 1996). At least two-thirds of human cellular proteins are phosphorylated with phosphorylation on Serine (86.4%), Threonine (11.8%) and Tyrosine (1.8%), respectively (Olsen et al., 2010, 2006). The eukaryotic protein phosphatases are classified as the phosphoprotein phosphatases (PPP), metallo-dependent protein phosphatases (PPM), protein tyrosine phosphatases (PTP), and Aspartate-dependent phosphatases (Kerk et al., 2008; Uhrig et al., 2013a). The PPP and PPM families are Ser/Thr-specific phosphatases (STPs) while PTP are Tyr specific. Dual-specificity phosphatases (DSP’s) dephosphorylate all three phosphoresidues (Keyse, 1995; Stone and Dixon, 1994; Tonks and Neel, 1996). The PPP family includes PP1, PP2A, PP2B (Calcineurin, found in fungi and animal systems only), distantly related PP4-7 with unknown functions while the PPM family includes PP2C phosphatases and other Mg²⁺ or Mn²⁺-dependent protein phosphatases (Kerk et al., 2008). The classical PPP family in eukaryotes also includes Shewanella-like (SLP) phosphatases, Rhizobiales-like (RLPH) phosphatases and ApaH-like (ALPH) phosphatases that are highly similar to PPP-like protein phosphatases with a prokaryotic origin (Andreeva and Kutuzov, 2004; Uhrig et al., 2013b; Uhrig and Moorhead, 2011). The molecular evolution of these bacterial-like PPP classes identified in eukaryotes involve ancient mitochondrial/archaeal origin and lateral gene transfer. SLP phosphatases are absent in red alga, cyanobacteria, amoebozoa, animalia and archaea, but found in plants, mosses, and green algae (Uhrig and Moorhead, 2011). Homologs of eukaryotic protein phosphatases, PTPs, low molecular weight PTP (LMWPTP), PPPs and PPMs are present in archaea as well as bacteria and function as translation factor(s), small ribosome-associated GTPase, phosphotransferase system, stress responses, phosphoprotein anti-anti-sigma factor, sigma B regulator, negative effector of development, purine biosynthesis, transcriptional regulator and histone-like protein(s) (Pereira et al., 2011). The human proteome encodes up to 255 phosphatases (Sacco et al., 2012), having implications in cancers, auto-immune disorders and inherited genetic diseases (Mustelin, 2007). The Arabidopsis genome has been reported to have 130 PPs with 26 PPPs, 80 PP2Cs, 1 PTP, 22 DSPs and 1 LMWPTP while in rice, 90 PP2Cs, 23 DSPs, 17 PP2 As, 1PTP and 1 LMWPTP (Kerk et al., 2008; Singh et al., 2010; Xue et al., 2008). Protein phosphatases assume importance as regulators in critical cellular pathways widely.

Plant growth and development as well as responses under a number of stresses in the environment, both biotic and abiotic, are regulated by complex signaling pathways at multiple levels resulting in cross-talk(s) between pathways with some of the components overlapping or functioning in contrasting roles. ROS is a distress call for the system to respond to both biotic and abiotic challenges. Both threats converge at enhanced ROS generation under pathogen attacks as well as the stress on the host system from abiotic factors. Protein phosphatases regulate a number of signaling pathways in different scenarios. Both ROS and protein phosphorylation are subjects of global research with a focus on their regulation and impact on the functioning and survival in microbial, plant and animal systems. It is in this context, that we trace the role of protein phosphatases, which are known majorly for their negative regulation, in the events that are known to either generate or regulate ROS. In this review; we present the function of protein phosphatases within the purview of ROS signaling in plants.

Section snippets

Reactive oxygen species

Reactive oxygen species (ROS), the activated derivatives of oxygen such as singlet oxygen (¹O₂), superoxide anion (O₂⁻), hydrogen peroxide (H₂O₂) and hydroxyl radical (OH), are the by-products of aerobic metabolism, which cause oxidative damages to cellular components such as lipids, proteins and DNA at high levels. At low levels, ROS mediate physiological intracellular signaling by acting as signaling molecules to adapt to environmental stresses (Das and Roychoudhury, 2014). ROS have been

PP2As: Role in intracellular oxidative stress

PP2A family has been implicated in the regulation of a number of cellular pathways. PP2A phosphatases are made up of three subunits, a ∼65-kDa scaffolding subunit, “A”, a regulatory subunit, “B” and a ∼36-kDa catalytic subunit, “C” in both plants and animals (Janssens and Goris, 2001). The B subunit has been classified as 55 kDa B (B55), 54–74 kDa B’ (B56), 72–130 kDa B” and B”’ families based on sequence homology (Mayer-Jaekel and Hemmings, 1994). The C and A subunits make up the core enzyme,

PP2Cs and ROS: Connecting through phytohormonal pathways

The PP2C family has diversified throughout evolution and is sub-divided into 11 (A–K) sub-families in rice and Arabidopsis and 13 in tomato and hot-pepper (Kim et al., 2014; Singh et al., 2010). The PP2Cs do not show amino acid sequence homology to other types of PPPs, but have similar three-dimensional structures indicating a similar catalytic mechanism (Das et al., 1996). All PP2Cs have a common feature of the presence of 11 characteristic subdomains in the catalytic domain (Bork et al., 1996

Finding PTPs in oxidative signaling

Protein tyrosine (Tyr) phosphorylation is involved in diverse signaling pathways resulting in cell growth and differentiation in animals. ROS and reactive nitrogen species (RNS) facilitate the activation of tyrosine kinases (Östman et al., 2011; Tanner et al., 2011). The PTPs act as critical regulators of cellular signaling pathways by dephosphorylating the protein tyrosine kinases and interfere with the downstream signaling. The PTPs are classified into receptor‐like transmembrane PTPs,

MAPK Phosphatases in MAPK signaling

Mitogen‐activated protein kinase phosphatases (MKPs) act as negative regulators in the MAPK signaling pathways, thereby, playing crucial roles in plant growth, development and stress responses. MAP kinases are activated through the phosphorylation of the conserved TEY motif in their activation loop by a dual specificity MAPK kinase (MAPKK) on both Thr and Tyr residues (Anderson et al., 1990; Kyriakis and Avruch, 2001; Widmann et al., 1999). The same is reversed through dephosphorylation by

Reactive nitrogen species (RNS): a parallel perspective

RNS fall into two categories: non-radicals and radicals. The non-radical and radical RNS further are of two kinds: inorganic and organic. The inorganic non-radical molecules include Nitroxyl anion (NO⁻), Nitrosonium cation (NO⁺), Nitrous acid (HNO₂), Dinitrogen trioxide (N₂O₃), Dinitrogen tetroxide (N₂O₄), Peroxynitrite (ONOO⁻), Peroxynitrous acid (ONOOH) while non-radical organic molecules include Nitrotyrosine (Tyr-NO₂), Nitrosoglutathione (GSNO), Nitrosothiols (SNOs), Nitro-γ-tocopherol and

Conclusion and Future perspectives

Cellular processes utilize a number of signaling pathways to reel over the demands of the host system in the basal state as well as under stress to adapt and survive. In this process, a number of pathways crossover leading to cross-tolerance, making it difficult to elucidate all the cascades at a given point of time. A given set of responses may be due to a combination of stresses or due to the susceptibility of the host system. ROS represent themselves in multiple dimensions; therefore, it is

Author contribution statement

GKP conceived and planned this article. MB and GKP wrote the manuscript.

Funding

Research work in GKP’s lab is supported by Department of Biotechnology (DBT), Department of Science and Technology (DST-PURSE grant), University Grant Commission (UGC-DRSIII grant), India.

Declaration of Interest

Authors declare no conflict of interest.

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^☆: This article is part of a special issue entitled is “Revisiting the role of ROS and RNS in plants under a changing environment” published at the journal Environmental and Experimental Botany 161.

View full text

Protein phosphatases meet reactive oxygen species in plant signaling networks☆

Highlights

Abstract

Graphical abstract

Introduction

Section snippets

Reactive oxygen species

PP2As: Role in intracellular oxidative stress

PP2Cs and ROS: Connecting through phytohormonal pathways

Finding PTPs in oxidative signaling

MAPK Phosphatases in MAPK signaling

Reactive nitrogen species (RNS): a parallel perspective

Conclusion and Future perspectives

Author contribution statement

Funding

Declaration of Interest

Cell

Phytochemistry

J. Biol. Chem.

Trends Biochem. Sci.

FEBS Lett.

Environ. Exp. Bot.

J. Biol. Chem.

Biochim. Biophys. Acta (BBA)/Protein Struct. Mol.

Mol. Cell.

J. Biol. Chem.

J. Biol. Chem.

J. Biol. Chem.

J. Plant. Physiol.

Chemosphere

Cell

Fungal Genet. Biol.

J. Biol. Chem.

Biochim. Biophys. Acta

Mol. Plant

Structural and functional characterization of a novel phosphatase from the Arabidopsis thaliana gene locus At1g05000

Proteins

Stress hormone-independent activation and nuclear translocation of mitogen-activated protein kinases in Arabidopsis thaliana during ozone exposure

Plant. J.

S-nitrosylation triggers ABI5 degradation to promote seed germination and seedling growth

Nat. Commun.

Two distinct sources of elicited reactive oxygen species in tobacco epidermal cells

Plant. Cell. Online

Functional analysis in Arabidopsis of FsPTP1, a tyrosine phosphatase from beechnuts, reveals its role as a negative regulator of ABA signaling and seed dormancy and suggests its involvement in ethylene signaling modulation

Planta

Requirement for integration of signals from two distinct phosphorylation pathways for activation of MAP kinase

Nature

Arabidopsis MAP kinase phosphatase 1 (AtMKP1) negatively regulates MPK6-mediated PAMP responses and resistance against bacteria

Plant. J.

Widespread presence of “bacterial-like” PPP phosphatases in eukaryotes

BMC Evol. Biol.

Selective inhibition of clade A phosphatases type 2C by PYR/PYL/RCAR abscisic acid receptors

Plant. Physiol.

PYRABACTIN RESISTANCE1-LIKE8 plays an important role for the regulation of abscisic acid signaling in root

Plant. Physiol.

REACTIVE OXYGEN SPECIES: metabolism, oxidative stress, and Signal transduction

Annu. Rev. Plant. Biol.

MAPK signaling regulates nitric oxide and NADPH oxidase-dependent oxidative bursts in Nicotiana benthamiana

Plant. Cell. Online

Nitric oxide signalling in plants: Cross-talk with Ca2+, protein kinases and reactive oxygen species

Nitrogen Metabolism in Plants in the Post-Genomic Era

MAP KINASE PHOSPHATASE1 and PROTEIN TYROSINE PHOSPHATASE1 are repressors of salicylic acid synthesis and SNC1-mediated responses in Arabidopsis

Plant. Cell. Online

ROS as key players in plant stress signalling

J. Exp. Bot.

Mechanisms for the generation of reactive oxygen species in plant defence - A broad perspective

Physiol. Mol. Plant. Pathol.

Atypical protein phosphatase 2A gene families do not expand via paleopolyploidization

Plant. Physiol.

The protein phosphatase 2C (PP2C) superfamily: detection of bacterial homologues

Protein Sci.

ABA-induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis

Plant. J.

To die or not to die? Lessons from lesion mimic mutants

Front. Plant. Sci.

ABA activation of an MBP kinase in Pisum sativum epidermal peels correlates with stomatal responses to ABA

J. Exp. Bot.

Inactivation of PYR/PYL/RCAR ABA receptors by tyrosine nitration may enable rapid inhibition of ABA signaling by nitric oxide in plants

Sci. Signal.

Peroxisomal hydrogen peroxide Is coupled to biotic defense responses by ISOCHORISMATE SYNTHASE1 in a daylength-related manner

Nitric oxide signalling in plants: Cross-talk with Ca²⁺, protein kinases and reactive oxygen species

ABA-induced NO generation and stomatal closure in Arabidopsis are dependent on H₂O₂ synthesis