Nitric Oxide

Nitric oxide in plant-pathogen interactions

Nitric oxide (NO) is a highly reactive molecule that rapidly diffuses and permeates cell membranes. In animals, NO is implicated in a number of diverse physiological processes such as neurotransmission, vascular smooth muscle relaxation, and platelet inhibition. It may have beneficial effects, for example as a messenger in immune responses, but is also potentially toxic when the antioxidant system is weak and an excess of reactive oxygen intermediates (ROI) accumuates. During the last few years NO has been detected also in several plant species, and the increasing number of reports on its function in plants have implicated NO as an important effector of growth, development, and defense. The broad chemistry of NO involves an array of interrelated redox forms with different chemical reactivities, and numerous potential targets of NO action exist in plants. NO signaling functions depend on its reactivity and ROI are key modulators of NO in triggering cell death, although through mechanisms different from those commonly observed in animals

Between 1995 and 1998, in the lab of ChrisLamb at the Salk Institute we made pioneering work towards the discovery of NO function during the plant hypersensitive disease resistance response. We found that during the hypersensitive response plant cells accumulate NO, which co-operates with reactive oxygen species in the induction of hypersensitive cell death, and functions independently of such intermediates in the induction of defence related genes. We then demonstrated that the rates of production and dismutation of O2- generated during the oxidative burst play a crucial role in the modulation and integration of NO/H2O2 signalling in the hypersensitive response.

Due to the many possible mechanisms of NO action, a clear picture of its involvement in plant resistance to pathogens was far from being achieved. I have then dedicated about 10 years to the characterization and modulation of the signal transduction pathways leading to the hypersensitive disease resistance response. My lab went in deep in the analysis of genes involved in the hypersensitive cell death and in the establishment of disease resistance whose expression is under control of NO.

We also focussed on the mechanisms regulating NO level in plant, and on the identification and characterization of signalling mechanisms that operate downstream of NO accumulation. In particular, we analysed the occurrence of NO-dependent posttranslational modifications of proteins (S-nitrosylation and Tyr-nitration) to clarify their biological function and to understand their functional consequences in physiological and pathophysiological conditions.

Selected publications

Delledonne M. et al (1998). Nitric oxide functions as a signal in plant disease resistance. Nature 394:585-558
Delledonne M. et al (2001). Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proc. Natl. Acad. Sci. USA 98:13454-13459
Polverari A. et al (2003). Nitric oxide-mediated transcriptional changes in Arabidopsis thaliana.Mol. Plant-Microbe Interact. 16: 1094-1105
Perazzolli M. et al (2004) Arabidopsis non-symbiotic hemoglobin AHb1 modulates nitric oxide bioactivity. Plant Cell 16: 2785-2794
Zeier J. et al (2004) Genetic elucidation of nitric oxide signaling in incompatible plant-pathogen interactions. Plant Physiol. 136: 2875-2886
Romero-Puertas M.C. et al (2004) Nitric oxide signaling functions in plant-pathogen interactions. Cell. Microbiol. 6: 795-803
Boccara M. et al (2005) Flavohaemoglobin HmpX from Erwinia chrysanthemi confers nitrosative stress tolerance and affects the plant hypersensitive reaction by intercepting nitric oxide produced by the host. Plant J. 43:226-237
Perazzolli M. et al (2006). Modulation of nitric oxide bioactivity by plant haemoglobins. J. Exp. Bot. 57:479-488
Zaninotto F. et al (2006). Cross-talk between reactive nitrogen and oxygen species during the hypersensitive disease resistance response. Plant Physiol. 141: 379-383
Zago E. et al (2006) Nitric oxide- and hydrogen peroxide-responsive gene regulation during cell death induction in tobacco. Plant Physiol. 141: 404-411
Romero-Puertas M.C. et al (2007). S-nitrosylation of peroxiredoxin II E promotes peroxynitrite-mediated tyrosine nitration. Plant Cell 19: 4120-4130
Belenghi B. et al (2007). Metacaspase activity of Arabidopsis thaliana is regulated by S-nitrosylation of a critical cysteine residue. J Biol. Chem. 282: 1352-1358
Ferrarini A. et al (2008). Expression of Medicago truncatula genes responsive to nitric oxide, in pathogenic and symbiotic conditions. Mol. Plant-Microbe Interact. 21: 781-790
Boscari A. et al (2013). Expression dynamics of the Medicago truncatula transcriptome during the symbiotic interaction with Sinorhizobium meliloti: which role for nitric oxide? Plant Physiol 161: 425-439
Ling T. et al (2017). Host-Mediated S-Nitrosylation Disarms the Bacterial Effector HopAI1 to Reestablish Immunity. Plant Cell 11:2871-2881