Chloroplasts of Arabidopsis Are the Source and a Primary Target of a Plant-Specific Programmed Cell Death Signaling Pathway

Abstract

Enhanced levels of singlet oxygen ( 1 O 2 ) in chloroplasts trigger programmed cell death. The impact of 1 O 2 production in chloroplasts was monitored first in the conditional fluorescent (flu) mutant of Arabidopsis thaliana that accumulates 1 O 2 upon a dark/light shift. The onset of 1 O 2 production is rapidly followed by a loss of chloroplast integrity that precedes the rupture of the central vacuole and the final collapse of the cell. Inactivation of the two plastid proteins EXECUTER (EX1) and EX2 in the flu mutant abrogates these responses, indicating that disintegration of chloroplasts is due to EX-dependent signaling rather than 1 O 2 directly. In flu seedlings, 1 O 2 -mediated cell death signaling operates as a default pathway that results in seedlings committing suicide. By contrast, EX-dependent signaling in the wild type induces the formation of microlesions without decreasing the viability of seedlings. 1 O 2 -mediated and EX-dependent loss of plastid integrity and cell death in these plants occurs only in cells containing fully developed chloroplasts. Our findings support an as yet unreported signaling role of 1 O 2 in the wild type exposed to mild light stress that invokes photoinhibition of photosystem II without causing photooxidative damage of the plant.

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

“…Thus, both DCMU and flu-generated signaling have been shown to be attenuated in ex1 and ex1/ex2 mutants (Wagner et al, 2004;Lee et al, 2007). However, the role of the EX genes appears to be limited to moderate states of chloroplast oxidative stress (Lee et al, 2007;Kim et al, 2012). Indeed, only 3.5% of the genes were downregulated in the ex1/ex2 seedlings in mild light stress (Kim and Apel, 2013).…”

“…Singlet oxygen has previously been implicated as the major toxicity factor in chloroplast-driven photooxidative cell death. It is also a causal agent in hypersensitive immune responses that occur in the light (Triantaphylidès et al, 2008;Triantaphylidès and Havaux, 2009;Kim et al, 2012;Zoeller et al, 2012). In addition, singlet oxygen is the major ROS agent produced in the flu mutant during dark-to-light transition (op den Camp et al, 2003).…”

“…The response is not the result of direct toxicity of singlet oxygen, because the process is mediated through two chloroplast proteins, EX1 and EX2. 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).…”

Reactive oxygen species and plant resistance to fungal pathogens

“…ROS-induced PCD has been described as a mechanism of photooxidative damage during photosynthesis, since plants under severe light stress show PCD induced by an increase in the level and toxicity of singlet oxygen 1 O 2 (Triantaphylides et al, 2008). Interestingly, a recent analysis indicates that under non-stress light conditions 1 O 2 can also play a role as signalling molecule, regulating the PCD pathway and generating microscopic lesions in the leaf (Kim et al, 2012). Concerning plantpathogen interactions, NO and ROS participate in a coordinated way in regulated HR (Bellin et al, 2012).…”

An ecological implication of glandular trichome-sequestered artemisinin: as a sink of biotic/abiotic stress-triggered singlet oxygen

“…In A. thaliana, two kinds of nucleus-encoded and chloroplast-targeted proteins, Executer 1 (EX1) and Executer 2 (EX2), were identified to transduce 1 O2 from chloroplast to nuclei, i.e., so-called 'retrograde 1 O2 signaling' (Lee et al 2007;Kim et al 2008). Upon enhanced 1 O2 burst, programmed cell death is triggered, leading to the bleaching of seedlings and the growth retardation of mature plants in the flu mutant of A. thaliana (Kim et al 2012).…”