NO signals in the haze: Nitric oxide signalling in plant defence
Introduction
Nitric oxide (NO) is a small gaseous radical with diverse signalling functions. In plants, NO was first found to play a crucial role in mediating defence reactions against bacterial pathogens [1] and is now well known to influence numerous physiological processes throughout the entire plant life cycle. To name a few, NO is involved in germination, leaf expansion, lateral root development, flowering, stomatal closure, cell death and defence against biotic and abiotic stresses [2•]. Whereas descriptions of NO-mediated processes are accumulating, the plant signalling pathways governed by NO are still largely unknown. NO-related signalling can be attributed to various NO derivatives, collectively referred to as reactive nitrogen species (RNS). RNS comprise not only the NO radical (NO) and its nitroxyl (NO−) and nitrosonium (NO+) ions, but also peroxynitrite (ONOO−), S-nitrosothiols, higher oxides of nitrogen and dinitrosyl–iron complexes; in short, all NO derivatives that can effect NO-dependent modifications [3]. Hence, the term NO-related signalling is used here to summarise effects caused by all these RNS.
In principle, NO-related functions are subject to different levels of control. Production and turnover regulate NO bioavailability; once the NO level increases in the system, it can affect signalling either directly via protein modifications or indirectly via activation of second messengers. In animals, second messengers, such as cGMP, are well-characterised components of NO signal transduction, whereas studies of NO-dependent posttranslational modifications are more recent. However, in research conducted in plants, knowledge of the cGMP-dependent pathways is restricted to data gained using pharmacological approaches. By contrast, the impact of NO-dependent protein modifications, especially of S-nitrosylation, is the best studied mode of action in plants to date.
Among the diverse physiological processes affected by NO, available data predominantly explain signalling related to plant defence responses—which is the focus of this review.
Section snippets
No simple answers to the question how NO is produced in plants
Three routes to yield NO have been described in plants: non-enzymatic conversion of nitrite to NO in the apoplast, nitrate reductase (NR)-dependent NO formation and NO synthase (NOS)-like activity, that is arginine-dependent NO formation. These pathways have been reviewed in detail [2•, 4•]. In a nutshell: since the enzymatic source(s) of NO in plant stress responses remains elusive, unbiased genetic tools are still lacking for non-invasive manipulations of NO levels in planta. Despite numerous
NO-associated protein modifications
RNS can directly react with diverse biomolecules [3]. Amongst them, proteins can be modified by RNS through reactions with different amino acids or prosthetic groups. More specifically, the main NO-associated protein modifications in the biological context are the covalent modifications of cysteine (S-nitrosylation) and tyrosine (tyrosine 3-nitration) residues and NO binding to transition metals (metal nitrosylation). To date, the best characterised of these is cysteine S-nitrosylation.
The missing link to cGMP
In animals, NO can initiate its biological effects through the activation of sGC and associated increase in the levels of the second messenger cGMP. Both a transient increase in cGMP and its involvement in several processes have also been demonstrated in plants [62]. Indeed, pharmacological and biochemical approaches showed that cGMP is involved in NO-dependent signalling, gene transcription modulation, root growth and gravitropism, pollen tube growth and orientation, hormone-dependent
Conclusions
We continue to gain new knowledge on NO-related signalling. However, the data available are still far from offering a comprehensive and consistent picture of NO function in plants. The lack of genetic tools substantially hinders research on NO production and functions. New findings, however, underline the importance of NO in plant cell physiology and the complexity of NO-related signalling networks. Particularly, the impact of S-nitrosylation on protein function has been clearly demonstrated,
References and recommended reading
Papers of particular interest, published within the period of review, have been highlighted as:
• of special interest
•• of outstanding interest
Acknowledgement
This work was supported by a grant to M.D. from the Ministero dell’Università e della Ricerca in the framework of the program ‘Components of the nitric oxide signalling pathways in plants’.
References (65)
- et al.
ABA-induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis
Plant J
(2006) - et al.
Nitrite accumulation and nitric oxide emission in relation to cellular signaling in nitrite reductase antisense tobacco
Planta
(2002) - et al.
S-nitrosoglutathione reductase affords protection against pathogens in Arabidopsis, both locally and systemically
Plant Physiol
(2007) - et al.
Inhibition of AtMYB2 DNA-binding by nitric oxide involves cysteine S-nitrosylation
Biochem Biophys Res Commun
(2007) - et al.
Nitric oxide plays a central role in determining lateral root development in tomato
Planta
(2004) - et al.
S-nitrosylated GAPDH initiates apoptotic cell death by nuclear translocation following Siah1 binding
Nat Cell Biol
(2005) - et al.
The chemistry of cell signaling by reactive oxygen and nitrogen species and 4-hydroxynonenal
Arch Biochem Biophys
(2008) - et al.
Regulated protein denitrosylation by cytosolic and mitochondrial thioredoxins
Science
(2008) - et al.
Proteolytic degradation of tyrosine nitrated proteins
Arch Biochem Biophys
(2000) - et al.
Peroxynitrite generation and tyrosine nitration in defense responses in tobacco BY-2 cells
Plant Cell Physiol
(2006)
Cytochrome c nitration by peroxynitrite
J Biol Chem
Nitric oxide mediates inactivation of glutathione S-transferase in suspension culture of Taxus cuspidata during shear stress
J Biotechnol
Peroxynitrite targets the epidermal growth factor receptor, Raf-1, and MEK independently to activate MAPK
J Biol Chem
The Arabidopsis thaliana brassinosteroid receptor (AtBRI1) contains a domain that functions as a guanylyl cyclase in vitro
PLoS ONE
Expression and characterization of the catalytic domains of soluble guanylate cyclase: interaction with the heme domain
Biochemistry
Lamb C: nitric oxide functions as a signal in plant disease resistance
Nature
Nitric oxide synthesis and signalling in plants
Plant Cell Environ
The moving frontier in nitric oxide-dependent signalling
Sci STKE
New insights into nitric oxide signaling in plants
Annu Rev Plant Biol
AtNOS/AtNOA1 is a functional Arabidopsis thaliana cGTPase and not a nitric-oxide synthase
J Biol Chem
A mutant impaired in the production of plastome-encoded proteins uncovers a mechanism for the homeostasis of isoprenoid biosynthetic enzymes in Arabidopsis plastids
Plant Cell
Decreased arginine and nitrite levels in nitrate reductase-deficient Arabidopsis thaliana plants impair nitric oxide synthesis and the hypersensitive response to Pseudomonas syringae
Plant Sci
Arginase-negative mutants of Arabidopsis exhibit increased nitric oxide signaling in root development
Plant Physiol
Nitric oxide represses the Arabidopsis floral transition
Science
Modulation of nitrosative stress by S-nitrosoglutathione reductase is critical for thermotolerance and plant growth in Arabidopsis
Plant Cell
Nitric oxide modulates ozone-induced cell death, hormone biosynthesis and gene expression in Arabidopsis thaliana
Plant J
Expression analysis of Arabidopsis vacuolar sorting receptor 3 reveals a putative function in guard cells
J Exp Bot
Nitric oxide synthase generates nitric oxide locally to regulate compartmentalized protein S-nitrosylation and protein trafficking
Proc Natl Acad Sci USA
S-nitrosylation of proteins at the leading edge of migrating trophoblasts by inducible nitric oxide synthase promotes trophoblast invasion
Exp Cell Res
Arabidopsis nonsymbiotic hemoglobin AHb1 modulates nitric oxide bioactivity
Plant Cell
Genetic elucidation of nitric oxide signaling in incompatible plant–pathogen interactions
Plant Physiol
A metabolic enzyme for S-nitrosothiol conserved from bacteria to humans
Nature
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