Reactive oxygen species (ROS) have multifaceted roles in the orchestration of plant gene expression and gene-product regulation. Cellular redox homeostasis is considered to be an “integrator” of information from metabolism and the environment controlling plant growth and acclimation responses, as well as cell suicide events. The different ROS forms influence gene expression in specific and sometimes antagonistic ways. Low molecular antioxidants (e.g., ascorbate, glutathione) serve not only to limit the lifetime of the ROS signals but also to participate in an extensive range of other redox signaling and regulatory functions. In contrast to the low molecular weight antioxidants, the “redox” states of components involved in photosynthesis such as plastoquinone show rapid and often transient shifts in response to changes in light and other environmental signals. Whereas both types of “redox regulation” are intimately linked through the thioredoxin, peroxiredoxin, and pyridine nucleotide pools, they ...

Redox Regulation in Photosynthetic Organisms: Signaling, Acclimation, and Practical Implications

AP2/ERF family transcription factors in plant abiotic stress responses.

Free radicals, reactive oxygen species, oxidative stress and its classification

Plants and algae often absorb too much light—more than they can actually use in photosynthesis. To prevent photo-oxidative damage and to acclimate to changes in their environment, photosynthetic organisms have evolved direct and indirect mechanisms for sensing and responding to excess light. Photoreceptors such as phototropin, neochrome, and cryptochrome can sense excess light directly and relay signals for chloroplast movement and gene expression responses. Indirect sensing of excess light through biochemical and metabolic signals can be transduced into local responses within chloroplasts, into changes in nuclear gene expression via retrograde signaling pathways, or even into systemic responses, all of which are associated with photoacclimation.

Sensing and responding to excess light.

As fixed organisms, plants are especially affected by changes in their environment and have consequently evolved extensive mechanisms for acclimation and adaptation. Initially considered by-products from aerobic metabolism, reactive oxygen species (ROS) have emerged as major regulatory molecules in plants and their roles in early signaling events initiated by cellular metabolic perturbation and environmental stimuli are now established. Here, we review recent advances in ROS signaling. Compartment-specific and cross-compartmental signaling pathways initiated by the presence of ROS are discussed. Special attention is dedicated to established and hypothetical ROS-sensing events. The roles of ROS in long-distance signaling, immune responses, and plant development are evaluated. Finally, we outline the most challenging contemporary questions in the field of plant ROS biology and the need to further elucidate mechanisms allowing sensing, signaling specificity, and coordination of multiple signals.

Reactive Oxygen Species in Plant Signaling

The regulation of the chloroplast antioxidant capacity depends on nuclear gene expression. For the 2-Cys peroxiredoxin-A gene (2CPA) a cis-regulatory element was recently characterized, which responds to photosynthetic redox signals. In a yeast-one-hybrid screen for cis-regulatory binding proteins, the transcription factor Rap2.4a was isolated. Rap2.4a controls the transcript abundance of the prominent chloroplast antioxidant enzyme through binding to the CGCG core of a CE3-like element. Rap2.4a activity is regulated by dithiol/disulfide transition of regulatory cysteinyl residues and subsequent changes in the quaternary structure. The mid-point redox potential of Rap2.4a activation is -269 mV (pH 7.0). The redox sensitivity of Rap2.4a establishes an efficient switch mechanism for redox control of nuclear gene activity of chloroplast antioxidants, in which Rap2.4 is a redox-sensor and a transducer of redox information.

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The redox-sensitive transcription factor Rap2.4a controls nuclear expression of 2-Cys peroxiredoxin A and other chloroplast antioxidant enzymes

The rimb1 (redox imbalanced 1) mutation was mapped to the RCD1 locus (radical-induced cell death 1; At1g32230) demonstrating that a major factor involved in redox-regulation genes for chloroplast antioxidant enzymes and protection against photooxidative stress, RIMB1, is identical to the regulator of disease response reactions and cell death, RCD1. Discovering this link let to our investigation of its regulatory mechanism. We show in yeast that RCD1 can physically interact with the transcription factor Rap2.4a which provides redox-sensitivity to nuclear expression of genes for chloroplast antioxidant enzymes. In the rimb1 (rcd1-6) mutant, a single nucleotide exchange results in a truncated RCD1 protein lacking the transcription factor binding site. Protein-protein interaction between full-length RCD1 and Rap2.4a is supported by H2O2, but not sensitive to the antioxidants dithiotreitol and ascorbate. In combination with transcript abundance analysis in Arabidopsis, it is concluded that RCD1 stabilizes the Rap2.4-dependent redox-regulation of the genes encoding chloroplast antioxidant enzymes in a widely redox-independent manner. Over the years, rcd1-mutant alleles have been described to develop symptoms like chlorosis, lesions along the leaf rims and in the mesophyll and (secondary) induction of extra- and intra-plastidic antioxidant defense mechanisms. All these rcd1 mutant characteristics were observed in rcd1-6 to succeed low activation of the chloroplast antioxidant system and glutathione biosynthesis. We conclude that RCD1 protects plant cells from running into reactive oxygen species (ROS)-triggered programs, such as cell death and activation of pathogen-responsive genes (PR genes) and extra-plastidic antioxidant enzymes, by supporting the induction of the chloroplast antioxidant system.

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The radical induced cell death protein 1 (RCD1) supports transcriptional activation of genes for chloroplast antioxidant enzymes.

The redox imbalanced 6 mutant (rimb6) of Arabidopsis thaliana was isolated in a genetic screening approach for mutants with defects in chloroplast-to-nucleus redox signalling. It has an atypically low activation status of the 2-Cys peroxiredoxin-A promoter in the seedling stage. rimb6 shows wildtype-like germination, seedling development and greening, but slower growth and reduced biomass in the rosette stage. Mapping of the casual mutation revealed that rimb6 carries a single nucleotide polymorphism in the gene encoding CONSTITUTIVE EXPRESSER OF PATHOGENESIS RELATED (PR) GENES 1, CPR1 (At4g12560), leading to a premature stop codon. CPR1 is known as a repressor of pathogen signalling and regulator of microtubule organization. Allelism of rimb6 and cpr1 revealed a function of CPR1 in chloroplast stress protection. Expression studies in pathogen signalling mutants demonstrated that CPR1-mediated activation of genes for photosynthesis and chloroplast antioxidant protection is, in contrast to activation of pathogen responses, regulated independently from PAD4-controlled salicylic acid (SA) accumulation. We conclude that the support of plastid function is a basic, SA-independent function of CPR1.

Heiko Hiltscher

Papers

The redox-sensitive transcription factor Rap2.4a controls nuclear expression of 2-Cys peroxiredoxin A and other chloroplast antioxidant enzymes

The radical induced cell death protein 1 (RCD1) supports transcriptional activation of genes for chloroplast antioxidant enzymes.

The Plant Immunity Regulating F-Box Protein CPR1 Supports Plastid Function in Absence of Pathogens.