Rapid Induction of Distinct Stress Responses after the Release of Singlet Oxygen in Arabidopsis[W]

Abstract

The conditional fluorescent ( flu ) mutant of Arabidopsis accumulates the photosensitizer protochlorophyllide in the dark. After a dark-to-light shift, the generation of singlet oxygen, a nonradical reactive oxygen species, starts within the first minute of illumination and was shown to be confined to plastids. Immediately after the shift, plants stopped growing and developed necrotic lesions. These early stress responses of the flu mutant do not seem to result merely from physicochemical damage. Peroxidation of chloroplast membrane lipids in these plants started rapidly and led to the transient and selective accumulation of a stereospecific and regiospecific isomer of hydroxyoctadecatrieonic acid, free (13 S )-HOTE, that could be attributed almost exclusively to the enzymatic oxidation of linolenic acid. Within the first 15 min of reillumination, distinct sets of genes were activated that were different from those induced by superoxide/hydrogen peroxide. Collectively, these results demonstrate that singlet oxygen does not act primarily as a toxin but rather as a signal that activates several stress-response pathways. Its biological activity in Arabidopsis exhibits a high degree of specificity that seems to be derived from the chemical identity of this reactive oxygen species and/or the intracellular location at which it is generated.

Genomics-based dissection of the cross-talk of chloroplasts with the nucleus and mitochondria in Arabidopsis

“…In general, a low sugar status enhances photosynthesis and induces reserve mobilization and export, whereas an abundant supply of sugars promotes growth and carbohydrate storage. Dark-to-light shift experiments with the Arabidopsis flu mutant revealed that singlet oxygen, a nonradical reactive oxygen species, was confined to plastids and activates several stress-response pathways (op den Camp et al, 2003). The biological activity of this reactive oxygen species is highly specific, and seems to depend from the chemical identity of the molecule and/or the site at which it is generated (op den Camp et al, 2003).…”

“…Dark-to-light shift experiments with the Arabidopsis flu mutant revealed that singlet oxygen, a nonradical reactive oxygen species, was confined to plastids and activates several stress-response pathways (op den Camp et al, 2003). The biological activity of this reactive oxygen species is highly specific, and seems to depend from the chemical identity of the molecule and/or the site at which it is generated (op den Camp et al, 2003). Also photorespiratory H 2 O 2 has been suggested to have a direct impact on the transcription of nuclear genes (Vandenabeele et al, 2004).…”

Heterotrimeric G-protein is involved in phytochrome A-mediated cell death of Arabidopsis hypocotyls

“…It has been known that seedlings grown in the dark or in FR for prolonged periods of time will be photobleached upon exposure to WL due to over-accumulated Pchlide [25,[29][30][31]. There are two types of Pchlide, namely, photoconvertible (Pchlide 655 ) and nonphotoconvertible (Pchlide 633 ).…”

“…These two functions may be linked in vivo and can barely be distinguished in response to environmental stimuli. However, recent progress achieved as a result of studies on the flu seedlings, which rapidly accumulate Pchlide in the dark and generate singlet oxygen upon exposure to light, have shown that the primary effect of ROS is the activation of a broad range of signaling pathways without direct damage to chloroplast biogenesis [29,42].…”

Molecular components of stress-responsive plastid retrograde signaling networks and their involvement in ammonium stress

“…[2][3][4][5][6][7][8][9][10][11][12][13][14][15][16] More recently, several plastid retrograde signaling pathways have been identified to regulate the expression of stress-related nuclear genes during several stresses such as high light, drought, wounding, heat, and excess ammonium. [17][18][19][20][21][22][23][24][25][26][27][28][29][30][31] Based on the new stress-responsive plastid retrograde signaling pathways just reported in 2012 alone, this review will focus on properties of currently proposed molecular components in the plastid retrograde signaling network under stress. We also specifically discuss possible plastid retrograde signals involved in plant response to ammonium stress.…”