Acclimation to Singlet Oxygen Stress in Chlamydomonas reinhardtii

Abstract

In an aerobic environment, responding to oxidative cues is critical for physiological adaptation (acclimation) to changing environmental conditions. The unicellular alga Chlamydomonas reinhardtii was tested for the ability to acclimate to specific forms of oxidative stress. Acclimation was defined as the ability of a sublethal pretreatment with a reactive oxygen species to activate defense responses that subsequently enhance survival of that stress. C. reinhardtii exhibited a strong acclimation response to rose bengal, a photosensitizing dye that produces singlet oxygen. This acclimation was dependent upon photosensitization and occurred only when pretreatment was administered in the light. Shifting cells from low light to high light also enhanced resistance to singlet oxygen, suggesting an overlap in high-light and singlet oxygen response pathways. Microarray analysis of RNA levels indicated that a relatively small number of genes respond to sublethal levels of singlet oxygen. Constitutive overexpression of either of two such genes, a glutathione peroxidase gene and a glutathione S-transferase gene, was sufficient to enhance singlet oxygen resistance. Escherichia coli and Saccharomyces cerevisiae exhibit well-defined responses to reactive oxygen but did not acclimate to singlet oxygen, possibly reflecting the relative importance of singlet oxygen stress for photosynthetic organisms.Reactive oxygen species (ROS) production is an unavoidable consequence of life in an aerobic environment, and reliance upon oxygenic photosynthesis presents plants and algae with sources of ROS not generally shared by their nonphotosynthetic counterparts. Nearly any form of biotic or abiotic stress affects the chloroplast, where the photosynthetic electron transport chain brings together photosensitizing pigments, redox-active electron carriers, and oxygen generation in a polyunsaturated lipid environment. Disruptions in the balance between incoming excitation energy and terminal electron acceptors can result in ROS production and eventual cell death. High-light (HL) stress, for example, leads to increased production of singlet oxygen ( 1 O 2 ‫,)ء‬ hydrogen peroxide, and superoxide in the chloroplast (31, 44), while hypersensitive responses to tobacco mosaic virus in tobacco result in down-regulation of the proteins necessary to repair ROS-mediated damage to photosystem II (71). Understanding how plants and algae respond to ROS and limit ROS-induced damage is therefore necessary to piece together responses to biotic and abiotic stress.As a result of the capacity of ROS for damaging cellular constituents, including proteins, nucleic acids, and membranes (41), ROS are often cast in a purely destructive role. Evidence is emerging, however, that sublethal levels of ROS can be important signaling intermediates (4, 30), activating pathways that bolster defense responses and enhance survival of subsequent stress (11,13,47,78). For example, in the yeast Saccharomyces cerevisiae, sublethal levels of hydrogen peroxide activate the YAP1 (yeast ...

Singlet Oxygen Is the Major Reactive Oxygen Species Involved in Photooxidative Damage to Plants

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Minor Antenna Proteins CP24 and CP26 Affect the Interactions between Photosystem II Subunits and the Electron Transport Rate in Grana Membranes of Arabidopsis

“…CP26 is a component of the PSII antenna in the most ancient green algae species in which photoprotection is mainly performed through Zea synthesis (Baroli et al, 2003) independently from qE (Ledford et al, 2007), which is strongly decreased in green algae with respect to higher plants (Finazzi et al, 2004). We propose that CP26, here shown to be largely responsible for qI, is specialized in Zea-mediated photoprotection (Dall'Osto et al, 2005).…”

Retrograde bilin signaling enables Chlamydomonas greening and phototrophic survival

“…Genes induced by light and suppressed by BV were enriched for protein families involved in high light stress (e.g., encoding LHCSR1, PSBS1, ELI3, HSP22, GPX, HSP70, and others). This suggests that the initial transcriptional response to light in C. reinhardtii is dominated by the response to oxidative stress, a combined effect of photosynthetic oxygen evolution and pigment photosensitization (47,48). We therefore attribute the "global" attenuation of this response by BV to its ability to target a regulatory network needed to reduce or prevent oxidative stress.…”