Light-Induced Acclimation of the Arabidopsis chlorina1 Mutant to Singlet Oxygen  

Abstract

Singlet oxygen ( 1 O 2 ) is a reactive oxygen species that can function as a stress signal in plant leaves leading to programmed cell death. In microalgae, 1 O 2 -induced transcriptomic changes result in acclimation to 1 O 2 . Here, using a chlorophyll b-less Arabidopsis thaliana mutant (chlorina1 [ch1]), we show that this phenomenon can also occur in vascular plants. The ch1 mutant is highly photosensitive due to a selective increase in the release of 1 O 2 by photosystem II. Under photooxidative stress conditions, the gene expression profile of ch1 mutant leaves very much resembled the gene responses to 1 O 2 reported in the Arabidopsis mutant flu. Preexposure of ch1 plants to moderately elevated light intensities eliminated photooxidative damage without suppressing 1 O 2 formation, indicating acclimation to 1 O 2 . Substantial differences in gene expression were observed between acclimation and high-light stress: A number of transcription factors were selectively induced by acclimation, and contrasting effects were observed for the jasmonate pathway. Jasmonate biosynthesis was strongly induced in ch1 mutant plants under high-light stress and was noticeably repressed under acclimation conditions, suggesting the involvement of this hormone in 1 O 2 -induced cell death. This was confirmed by the decreased tolerance to photooxidative damage of jasmonatetreated ch1 plants and by the increased tolerance of the jasmonate-deficient mutant delayed-dehiscence2.

Singlet Oxygen Signatures Are Detected Independent of Light or Chloroplasts in Response to Multiple Stresses

“…Indeed, only 3.5% of the genes were downregulated in the ex1/ex2 seedlings in mild light stress (Kim and Apel, 2013). In addition, EX genes do not appear to modulate the chlorina1 photosystem mutant (Ramel et al, 2013) or the induction of genes by b-cyclocitral, a product of singlet oxygen activity (Ramel et al, 2012b). As shown here, wounding, which also generated singlet oxygen and induced CGS expression, was not controlled by EX genes.…”

“…In their absence, the transcriptomic response and cell death of the flu mutant in the dark-to-light shift is diminished (Wagner et al, 2004;Lee et al, 2007;Kim et al, 2012). The signaling competence of singlet oxygen is further illustrated by the induction of an acclimation response to singlet oxygen originating from applied chemicals or in mutants (Fischer et al, 2012;Ramel et al, 2013). In another example in the chlorina1 mutant, deficient in chlorophyll b, excess levels of singlet oxygen are generated in the thylakoids under light stress.…”

“…In another example in the chlorina1 mutant, deficient in chlorophyll b, excess levels of singlet oxygen are generated in the thylakoids under light stress. The transcriptome of this mutant shows high resemblance to that generated by the flu mutant although it seems to operate in a distinct manner and does not depend on EX1 activity (Ramel et al, 2013).…”

Singlet oxygen- and EXECUTER1-mediated signaling is initiated in grana margins and depends on the protease FtsH2

“…(7). Nonenzymatic oxidative breakdown products of β-carotene such as β-cyclocitral activate stress defense responses (7) and stress acclimation (8). In contrast, EX1-dependent signaling is triggered under nonphotoinhibitory light conditions.…”

“…Under such mild stress conditions the release of 1 O 2 induces a rapid bleaching of flu seedlings, whereas in mature flu plants ready to bolt generation of 1 O 2 leads to growth inhibition and stress acclimation (5,6). All these (7) or stress acclimation (8). Collectively, these results emphasize a key role of PSII as a major target of environmental stress that upon its damage leads to a significant reduction of plant productivity but at the same time is also involved in initiating 1 O 2 -mediated signaling that allows plants to adapt to these stress conditions.…”