Adaptation to environmental changes is crucial for plant growth and survival. However, the molecular and biochemical mechanisms of adaptation are still poorly understood and the signaling pathways involved remain elusive. Active oxygen species (AOS) have been proposed as a central component of plant adaptation to both biotic and abiotic stresses. Under such conditions, AOS may play two very different roles: exacerbating damage or signaling the activation of defense responses. Such a dual function was first described in pathogenesis but has also recently been demonstrated during several abiotic stress responses. To allow for these different roles, cellular levels of AOS must be tightly controlled. The numerous AOS sources and a complex system of oxidant scavengers provide the flexibility necessary for these functions. This review discusses the dual action of AOS during plant stress responses.

In plants, reactive oxygen species and, more particularly, hydrogen peroxide (H2O2) play a dual role as toxic by-products of normal cell metabolism and as regulatory molecules in stress perception and signal transduction. Peroxisomal catalases are an important sink for photorespiratory H2O2. Using ATH1 Affymetrix microarrays, expression profiles were compared between control and catalase-deficient Arabidopsis (Arabidopsis thaliana) plants. Reduced catalase levels already provoked differences in nuclear gene expression under ambient growth conditions, and these effects were amplified by high light exposure in a sun simulator for 3 and 8 h. This genome-wide expression analysis allowed us to reveal the expression characteristics of complete pathways and functional categories during H2O2 stress. In total, 349 transcripts were significantly up-regulated by high light in catalase-deficient plants and 88 were down-regulated. From this data set, H2O2 was inferred to play a key role in the transcriptional up-regulation of small heat shock proteins during high light stress. In addition, several transcription factors and candidate regulatory genes involved in H2O2 transcriptional gene networks were identified. Comparisons with other publicly available transcriptome data sets of abiotically stressed Arabidopsis revealed an important intersection with H2O2-deregulated genes, positioning elevated H2O2 levels as an important signal within abiotic stress-induced gene expression. Finally, analysis of transcriptional changes in a combination of a genetic (catalase deficiency) and an environmental (high light) perturbation identified a transcriptional cluster that was strongly and rapidly induced by high light in control plants, but impaired in catalase-deficient plants. This cluster comprises the complete known anthocyanin regulatory and biosynthetic pathway, together with genes encoding unknown proteins.

SummaryIn plants, hydrogen peroxide (H 2 O 2 ) plays a major signaling role in triggering both a defense response and cell death. Increased cellular H 2 O 2 levels and subsequent redox imbalances are managed at the production and scavenging levels. Because catalases are the major H 2 O 2 scavengers that remove the bulk of cellular H 2 O 2 , altering their levels allows in planta modulation of H 2 O 2 concentrations. Reduced peroxisomal catalase activity increased sensitivity toward both ozone and photorespiratory H 2 O 2 -induced cell death in transgenic catalase-de®cient Arabidopsis thaliana. These plants were used as a model system to build a comprehensive inventory of transcriptomic variations, which were triggered by photorespiratory H 2 O 2 induced by high-light (HL) irradiance. In addition to an H 2 O 2 -dependent and -independent type of transcriptional response during light stress, microarray analysis on both control and transgenic catalase-de®cient plants, exposed to 0, 3, 8, and 23 h of HL, revealed several speci®c regulatory patterns of gene expression. Thus, photorespiratory H 2 O 2 has a direct impact on transcriptional programs in plants.