H 2O 2 and NO: redox signals in disease resistance

Abstract

One of the earliest responses of plants to microbial pathogens is the production of active oxygen species (AOS) such as superoxide (O2−) and hydrogen peroxide (H2O2) (Ref. [ 1 Lamb C. Dixon R.A. The oxidative burst in plant disease resistance. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1997; 48: 251-275 Crossref PubMed Scopus (2522) Google Scholar ]). This so-called `oxidative burst' (the name was adopted from a similar process in mammalian macrophages) is triggered within minutes of infection. The process is initiated after pathogen recognition and involves a series of signal transduction events that typically include phospholipases, GTP-binding proteins, fluxes in Ca2+ and other ions, kinases and phosphatases[ 2 Yang Y. Shah J. Klessig D.F. Signal perception and transduction in plant defense responses. Genes Dev. 1997; 11: 1621-1639 Crossref PubMed Scopus (532) Google Scholar ]. Studies of various plant–pathogen combinations have revealed a striking correlation between the profile of AOS formation in cell cultures and the outcome of the interaction (resistance or susceptibility) in intact plants. Plant–pathogen interactions that induced a hypersensitive response (HR)—a resistance response of the host characterized by a rapid but strictly localized lesion formation, gave rise to a biphasic and sustained production of AOS, whereas interactions leading to disease provoked a monophasic oxidative burst. Similar AOS responses have now also been reported for intact plants[ 3 Draper J. Salicylate, superoxide synthesis and cell suicide in plant defence. Trends Plant Sci. 1997; 2: 162-165 Abstract Full Text PDF Scopus (227) Google Scholar ]. These observations led to the suggestion that sustained AOS formation is critical for establishing disease resistance during the HR. Consistent with this model, a number of studies revealed that AOS contribute to three major defense features of HR, namely hypersensitive cell death, cell wall strengthening and the activation of transcription-dependent responses against pathogens[ 1 Lamb C. Dixon R.A. The oxidative burst in plant disease resistance. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1997; 48: 251-275 Crossref PubMed Scopus (2522) Google Scholar , 4 Brisson L.F. Tenhaken R. Lamb C. Function of oxidative cross-linking of cell wall structural proteins in plant disease resistance. Plant Cell. 1994; 6: 1703-1712 PubMed Google Scholar , 5 Levine A. et al. H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell. 1994; 79: 583-593 Abstract Full Text PDF PubMed Scopus (2259) Google Scholar , 6 Jabs T. Dietrich R.A. Dangl J.L. Initiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide. Science. 1996; 273: 1853-1856 Crossref PubMed Scopus (677) Google Scholar , 7 Jabs T. et al. Elicitor-stimulated ion fluxes and O2− from the oxidative burst are essential components in triggering defense gene activation and phytoalexin synthesis in parsley. Proc. Natl. Acad. Sci. U. S. A. 1997; 94: 4800-4805 Crossref PubMed Scopus (496) Google Scholar ]. The precise role of AOS formation in disease resistance is nevertheless still controversial. For example, in some plant–pathogen interactions, the oxidative burst appears to be insufficient to trigger hypersensitive cell death[ 7 Jabs T. et al. Elicitor-stimulated ion fluxes and O2− from the oxidative burst are essential components in triggering defense gene activation and phytoalexin synthesis in parsley. Proc. Natl. Acad. Sci. U. S. A. 1997; 94: 4800-4805 Crossref PubMed Scopus (496) Google Scholar , 8 Glazener J.A. Orlandi E.W. Baker C.J. The active oxygen response of cell suspensions to incompatible bacteria is not sufficient to cause hypersensitive cell death. Plant Physiol. 1996; 110: 759-763 Crossref PubMed Scopus (100) Google Scholar ]. Furthermore, the defense genes that are induced by AOS are also up-regulated by abiotic stress, which may indicate that AOS production is part of a general stress defense pathway (possibly associated with necrosis) rather than of a specific response to pathogens. Is nitric oxide toxic or protective?Beligni et al.Trends in Plant ScienceAugust 01, 1999In Brief Full-Text PDF