NO signals in the haze: Nitric oxide signalling in plant defence

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Nitric oxide (NO) is gaining increasing attention as a regulator of diverse (patho-)physiological processes in plants. Although this molecule has been described as playing a role in numerous conditions, its production, turnover and mode of action are poorly understood. Recent studies on NO production have tended to highlight the questions that still remain unanswered rather than telling us more about NO metabolism. But regarding NO signalling and functions, new findings have given an impression of the intricacy of NO-related signalling networks. Different targets of protein S-nitrosylation have been characterised and enzymatic routes controlling this posttranslational modification are emerging, along with their physiological implications. Evidence is also accumulating for protein tyrosine nitration and cGMP as important components of NO-related signal transduction.

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 (NOradical dot) 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’.

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