No single way to understand singlet oxygen signalling in plants

Abstract

When plant cells are under environmental stress, several chemically distinct reactive oxygen species (ROS) are generated simultaneously in various intracellular compartments and these can cause oxidative damage or act as signals. The conditional flu mutant of Arabidopsis, which generates singlet oxygen in plastids during a dark-to-light transition, has allowed the biological activity of singlet oxygen to be determined, and the criteria to distinguish between cytotoxicity and signalling of this particular ROS to be defined. The genetic basis of singlet-oxygen-mediated signalling has been revealed by the mutation of two nuclear genes encoding the plastid proteins EXECUTER (EX)1 and EX2, which are sufficient to abrogate singlet-oxygen-dependent stress responses. Conversely, responses due to higher cytotoxic levels of singlet oxygen are not suppressed in the ex1/ex2 background. Whether singlet oxygen levels lower than those that trigger genetically controlled cell death activate acclimation is now under investigation.

Figure 1

Cytotoxicity versus signalling of ¹O₂ in Arabidopsis seedlings. In etiolated flu and executer1/flu (ex1/flu) seedlings, similar excess amounts of free protochlorophyllide (Pchlide) accumulate that, on excitation with blue light, emit a strong red fluorescence (D). In pre-illuminated flu seedlings exposed to 16 h: 8 h light:dark cycles (L/D) inactivation of the EX1 protein abrogates bleaching. However, in etiolated flu seedlings, which accumulate four- to fivefold the amounts of free Pchlide in seedlings grown in continuous light and transferred to the dark for 8 h, the ¹O₂-mediated collapse during re-illumination is not suppressed by the ex1 mutation (D→L). All three plant lines grew equally well under continuous light (LL). Adapted from Przybyla et al (2008) and reprinted with permission from Wiley–Blackwell Publishing Ltd. Wt, wild type.

Figure 2

Proposed model of plant responses to various levels of ¹O₂. Constantly changing environmental factors can lead to the generation of variable levels of ¹O₂ that can be mimicked in the flu mutant by modulating the length of exposure to darkness. Increasing dark incubation of flu plants leads to a proportional increase of free protochlorophyllide in the dark and of ¹O₂ generation on illumination. When the production of ¹O₂ is low, an acclimatory response might be activated that allows a plant to survive at subsequent higher levels of ¹O₂. Greater amounts of ¹O₂, for example in flu plants treated with 8 h of darkness and re-illuminated, trigger genetically controlled cell death through EXECUTER-dependent pathways. Most enzymatically oxidized lipid derivatives are produced under these conditions. When the level of ¹O₂ increases further, plants die owing to chemical damage caused by ¹O₂ and a massive production of non-enzymatically oxidized lipid is observed. EX, EXECUTER protein; PCD, programmed cell death.

Chanhong Kim

Rasa Meskauskiene

Klaus Apel

Christophe Laloi