Nitric Oxide Interacts with Salicylate to Regulate Biphasic Ethylene Production during the Hypersensitive Response

Abstract

C2H4 is associated with plant defense, but its role during the hypersensitive response (HR) remains largely uncharacterized. C2H4 production in tobacco (Nicotiana tabacum) following inoculation with HR-eliciting Pseudomonas syringae pathovars measured by laser photoacoustic detection was biphasic. A first transient rise (C2H4-I) occurred 1 to 4 h following inoculation with HR-eliciting, disease-forming, and nonpathogenic strains and also with flagellin (flg22). A second (avirulence-dependent) rise, at approximately 6 h (C2H4-II), was only seen with HR-eliciting strains. Tobacco leaves treated with the C2H4 biosynthesis inhibitor, aminoethoxyvinylglycine, suggested that C2H4 influenced the kinetics of a HR. Challenging salicylate hydroxylase-expressing tobacco lines and tissues exhibiting systemic acquired resistance suggested that C2H4 production was influenced by salicylic acid (SA). Disrupted expression of a C2H4 biosynthesis gene in salicylate hydroxylase tobacco plants implicated transcriptional control as a mechanism through which SA regulates C2H4 production. Treating leaves to increase oxidative stress or injecting with SA initiated monophasic C2H4 generation, but the nitric oxide (NO) donor sodium nitroprusside initiated biphasic rises. To test whether NO influenced biphasic C2H4 production during the HR, the NO synthase inhibitor NG-nitro-l-arginine methyl ester was coinoculated with the avirulent strain of P. syringae pv phaseolicola into tobacco leaves. The first transient C2H4 rise appeared to be unaffected by NG-nitro-l-arginine methyl ester, but the second rise was reduced. These data suggest that NO and SA are required to generate the biphasic pattern of C2H4 production during the HR and may influence the kinetics of HR formation.

Nitric oxide counters ethylene effects on ripening fruits

“…The reciprocal control of NO and SA over each other was found to affect the ethylene metabolism in turn, which influenced the pattern of defense responses in tobacco, revealing the reciprocal antagonistic interplay of NO and ethylene. 65 In addition, NO and ROS redox signaling networks were affected by SA during biotic stress. 66 SA accumulation triggered by NO was found to suppress superoxide free radical and other ROS production 67 and thereby aiding in the maintenance of cell membrane integrity and tissue senescence.…”

Synergistic Biosynthesis of Biphasic Ethylene and Reactive Oxygen Species in Response to HemibiotrophicPhytophthora parasiticain Tobacco Plants

“…Conversely, ethylene is a virulence factor of many biotropic or semibiotrophic pathogens (Mur et al, 2008). Further, a previous study reported that ethylene production in tobacco (Nicotiana tabacum) leaves after inoculation with HR-inducing Pseudomonas syringae follows a biphasic pattern reminiscent of H 2 O 2 production (Mur et al, 2008). However, P. syringae pv tabaci, which causes disease symptoms in tobacco, elicits only a single peak in ethylene production.…”

“…It was demonstrated in an analysis of ethylene-insensitive2 (ein2) mutant in Arabidopsis (Arabidopsis thaliana) that ethylene plays, at best, a minor role in hypersensitive response (HR)-mediated cell death. Conversely, ethylene is a virulence factor of many biotropic or semibiotrophic pathogens (Mur et al, 2008). Further, a previous study reported that ethylene production in tobacco (Nicotiana tabacum) leaves after inoculation with HR-inducing Pseudomonas syringae follows a biphasic pattern reminiscent of H 2 O 2 production (Mur et al, 2008).…”

“…In a previous study, we reported that the biphasic accumulation of ROS in response to abiotic stress is significantly reduced in transgenic antisense plants expressing ACS gene (CAS-AS-2, 3, 4), thereby resulting in decreased necrosis and cell death (Wi et al, 2010). Prior studies have demonstrated the potential interplay of biphasic ROS production and ethylene biosynthesis during abiotic responses based upon the biphasic generation of ethylene in response to pathogen (Mur et al, 2008) and the response to oxidative stresses such as H 2 O 2 treatment (Wi et al, 2010). Here, we extend our previous investigations into biphasic ROS and ethylene production during the defense response against compatible hemibiotroph Phytophthora parasitica var nicotianae (Ppn) in susceptible tobacco.…”

Biosíntesis, señalización y modo de acción del óxido nítrico en Arabidopsis thaliana

“…El NO regula estos procesos, al menos en parte, mediante la interacción con las rutas de señalización de las diferentes hormonas (Delledonne et al, 1998;Dangl 1998;Tun et al, 2001;Desikan et al, 2002;Beligni et al, 2002;OrozcoCardenas y Ryan 2002;Guo et al, 2003;Pagnussat et al, 2004;Huang et al, 2004;Jovanovic et al, 2005;Bethke et al, 2006a;Lindermayr et al, 2006;Tun et al, 2006;Groppa et al, 2008). De una forma paralela, se ha descrito tanto la producción de NO tras la aplicación de diferentes hormonas como las auxinas (Pagnussat et al, 2002;Pagnussat et al, 2003;Kolbert et al, 2008b;a), citoquininas (Tun et al, 2001;Tun et al, 2008), ABA (Neill et al, 2002a;Bright et al, 2006), SA (Zottini et al, 2007), JA , GAs (Bethke et al, 2004a) y poliaminas (Tun et al, 2006), como la modulación de los niveles de diferentes hormonas por NO Xu et al, 2005;Gniazdowska et al, 2007;Mur et al, 2008;Liu et al, 2009b).…”