Nitric Oxide- and Hydrogen Peroxide-Responsive Gene Regulation during Cell Death Induction in Tobacco  

Abstract

Nitric oxide (NO) and hydrogen peroxide (H 2 O 2 ) are regulatory molecules in various developmental processes and stress responses. Tobacco (Nicotiana tabacum) leaves exposed to moderate high light dramatically potentiated NO-mediated cell death in catalase-deficient (CAT1AS) but not in wild-type plants, providing genetic evidence for a partnership between NO and H 2 O 2 during the induction of programmed cell death. With this experimental model system, the specific impact on gene expression was characterized by either NO or H 2 O 2 alone or both molecules combined. By means of genome-wide cDNA-amplified fragment length polymorphism analysis, transcriptional changes were compared in high light-treated CAT1AS and wild-type leaves treated with or without the NO donor sodium nitroprusside. Differential gene expression was detected for 214 of the approximately 8,000 transcript fragments examined. For 108 fragments, sequence analysis revealed homology to genes with a role in signal transduction, defense response, hormone interplay, proteolysis, transport, and metabolism. Surprisingly, only 16 genes were specifically induced by the combined action of NO and H 2 O 2 , whereas the majority were regulated by either of them alone. At least seven transcription factors were mutually up-regulated, indicating significant overlap between NO and H 2 O 2 signaling pathways. These results consolidate significant cross-talk between NO and H 2 O 2 , provide new insight into the early transcriptional response of plants to increased NO and H 2 O 2 levels, and identify target genes of the combined action of NO and H 2 O 2 during the induction of plant cell death.

Cross Talk between Reactive Nitrogen and Oxygen Species during the Hypersensitive Disease Resistance Response

“…Conversely, in plants ONOO 2 does not appear to be an essential mediator of NO-ROS-induced cell death, which is triggered by the interaction of NO with H 2 O 2 (Delledonne et al, 2001). Genetic studies provide additional support for this model, originally based on the extensive use of pharmacology: Arabidopsis (Arabidopsis thaliana) plants lowered in thylakoidal ascorbate peroxidase show enhanced symptoms of NO-induced cell death compared to wild-type plants (Tarantino et al, 2005) and catalasedeficient tobacco (Nicotiana tabacum) plants, which accumulate elevated H 2 O 2 levels under moderate light intensity, show a dramatically augmented cell death in comparison to wild-type plants when treated with NO (Zago et al, 2006).…”

“…A similar, wide modulation of gene expression has also been observed with NO, which has been found to modulate the expression of transcription factors, receptors, and several pathogen-induced genes in addition to genes known to respond to oxidative stress, such as glutathione peroxidase and glutathione-S-transferase (Grun et al, 2006). The combined action of NO and H 2 O 2 on gene expression was recently investigated in a collaborative effort between our group and that of Frank Van Breusegem by monitoring transcriptional changes during the early phases of cell death in catalase-deficient tobacco plants treated with NO and then exposed to otherwise ineffective moderate high light (Zago et al, 2006). The experimental conditions allowed the analysis of gene expression during NO-ROS-mediated cell death, identifying genes specifically induced by NO or by H 2 O 2 , as well as the set of genes regulated by both.…”

Reactive Oxygen Species and Nitric Oxide Mediate Actin Reorganization and Programmed Cell Death in the Self-Incompatibility Response of Papaver

“…This suggests that ROS and NO signal in concert/tandem to initiate SImediated PCD. As mentioned earlier, both ROS and NO are known to signal to PCD (Neill et al, 2002;Zago et al, 2006;Zaninotto et al, 2006), and it is well established that NO and H 2 O 2 operate in partnership during the hypersensitive response (Delledonne et al, 2001;de Pinto et al, 2002).…”

Reactive oxygen species, ABA and nitric oxide interactions on the germination of warm-season C4-grasses

“…An important link between ABA and NO action in plants are reactive oxygen species (ROS) (Neill 2005;Bright et al 2006) and plants appear to have redundancy in signaling mechanisms for these molecules (Kwak et al 2003;Apel and Hirt 2004;Shi et al 2005;Zago et al 2006). Therefore, cross-talk between diVerent elicitation pathways could result in identical biological outputs for diVerent stimuli.…”