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Chilling-enhanced photooxidation: The production, action and study of reactive oxygen species produced during chilling in the light

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Abstract

Chilling-enhanced photooxidation is the light- and oxygen-dependent bleaching of photosynthetic pigments that occurs upon the exposure of chilling-sensitive plants to temperatures below approximately 10 °C. The oxidants responsible for the bleaching are the reactive oxygen species (ROS) singlet oxygen (1O2), superoxide anion radical (O ∸2 ,hydrogen peroxide (H2O2), the hydroxyl radical (OH·), and the monodehydroascorbate radical (MDA) which are generated by a leakage of absorbed light energy from the photosynthetic electron transport chain. Cold temperatures slow the energy-consuming Calvin-Benson Cycle enzymes more than the energy-transducing light reactions, thus causing leakage of energy to oxygen. ROS and MDA are removed, in part, by the action of antioxidant enzymes of the Halliwell/Foyer/Asada Cycle. Chloroplasts also contain high levels of both lipid- and water-soluble antioxidants that act alone or in concert with the HFA Cycle enzymes to scavenge ROS. The ability of chilling-resistant plants to maintain active HFA Cycle enzymes and adequate levels of antioxidants in the cold and light contributes to their ability to resist chilling-enhanced photooxidation. The absence of this ability in chilling-sensitive species makes them susceptible to chilling-enhanced photooxidation. Chloroplasts may reduce the generation of ROS by dissipating the absorbed energy through a number of quenching mechanisms involving zeaxanthin formation, state changes and the increased usage of reducing equivalents by other anabolic pathways found in the stroma. During chilling in the light, ROS produced in chilling-sensitive plants lower the redox potential of the chloroplast stroma to such a degree that reductively-activated regulatory enzymes of the Calvin Cycle, sedohepulose 1,7 bisphosphatase (EC 3.1.3.37) and fructose 1,6 bisphosphatase (EC 3.1.3.11), are oxidatively inhibited. This inhibition is reversible in vitro with a DTT treatment indicating that the enzymes themselves are not permanently damaged. The inhibition of SBPase and FBPase may fully explain the inhibition in whole leaf gas exchange seen upon the rewarming of chilling-sensitive plants chilled in the light. Methods for the study of ROS in chilling-enhanced photooxidation and challenges for the future are discussed.

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Abbreviations

ASP:

ascorbate-specific peroxidase

α-TH:

reduced α-tocopherol

DTT:

dithiothreitol

FBP:

fructose 1,6 bisphosphate

FBPase:

fructose 1,6 bisphosphatase (EC 3.1.3.11)

HFA Cycle:

the Halliwell/Foyer/Asada Cycle responsible for the enzymatic removal of ROS in the chloroplast stroma

MDA:

monodehydroascorbate radical

MDAR:

monodehydroascorbate reductase

ROS:

reactive oxygen species

SBP:

sedohepulose 1,7 bisphosphate

SBPase:

sedohepulose 1,7 bisphosphatase (EC 3.1.3.37)

SOD:

superoxide dismutase

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  1. Department of Biology and Microbiology, University of Wisconsin Oshkosh, 800 Algoma Blvd., 54901, Oshkosh, WI, USA

    Robert R. Wise

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Wise, R.R. Chilling-enhanced photooxidation: The production, action and study of reactive oxygen species produced during chilling in the light. Photosynth Res 45, 79–97 (1995). https://doi.org/10.1007/BF00032579

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