Two Distinct Redox Signaling Pathways for Cytosolic APX Induction under Photooxidative Stress

Abstract

The cross-talk of two redox factors, H2O2 accumulation and redox status of photosynthetic electron transport (PET) in tobacco chloroplasts, on the expression of cytosolic ascorbate peroxidase (cAPX) was studied. Transgenic tobacco plants, which expressed respectively the Escherichia coli catalase and spinach thylakoid-membrane-bound APX in chloroplasts and showed increased tolerance to photooxidative stress, were used for evaluation of the relationship between H2O2 accumulation or change of redox status of PET and cAPX induction under photooxidative stress condition. There was no difference in the increase in the transcript level of cAPX in the first 1 h after irradiation with high-intensity light between the wild-type and either of the transgenic plants. The transcript level of cAPX in the wild-type showed a steady gradual increase during the next 5 h, while that in the transgenic plants during this period was stable. The H2O2 level of wild-type plants increased after 1 h, while those of transgenic plants remained constant. The decrease in q(p) value in all types of plants occurred earlier than the increase in H2O2 level. These results indicate that the induction of cAPX expression is caused by a redox change in PET, probably through the plastquinone pool at an early stage and thereafter by an increase in the cellular H2O2 level.

Cellular redox regulation, signaling, and stress response in plants

“…The overexpression of tAPX markedly suppressed the MV treatment-induced expression of cAPX in tobacco plants, which suggests that H 2 O 2 produced by chloroplasts can also induce the expression of cAPX. 78) However, the overexpression of tAPX had no effect on the expression of cAPX at the early stage of HL illumination. 78) Furthermore, the induction of Arabidopsis APX2 by HL was significantly inhibited in single knockout mutants lacking sAPX or tAPX.…”

“…78) However, the overexpression of tAPX had no effect on the expression of cAPX at the early stage of HL illumination. 78) Furthermore, the induction of Arabidopsis APX2 by HL was significantly inhibited in single knockout mutants lacking sAPX or tAPX. 79) These findings suggested the existence of a complicated interaction between chloroplastic H 2 O 2 and HL signaling pathways for regulating the expression of cAPX.…”

“…76) In addition, a treatment with H 2 O 2 and methyl viologen (MV), a ROS-producing reagent, markedly enhanced the expression of APX2. [76][77][78] A treatment with 3-(3,4-dichlorophenyl)-l,l-dimethylurea (DCMU), an inhibitor of the reduction of the plastoquinone (PQ) pool, blocked the HL-response of APX2. On the other hand, a treatment with 2,5-dibromo-3-methyl-6-isopropyl-p-benzoquinone (DBMIB), an inhibitor of the oxidation of this pool, enhanced the expression of APX2 even under normal light conditions.…”

“…77) Expression of cAPX gene in tobacco was shown to be regulated in a similar manner. 78) Thus, the expression of cAPX genes appears to be regulated by ROS and the redox states of the PQ pool under photooxidative stress conditions. The overexpression of tAPX markedly suppressed the MV treatment-induced expression of cAPX in tobacco plants, which suggests that H 2 O 2 produced by chloroplasts can also induce the expression of cAPX.…”

Plant Organelles-to-Nucleus Retrograde Signaling

“…It follows that chloroplast-generated H 2 O 2 would represent a redox signal to activate cAPX expression in the nucleus. The initial induction observed under photooxidative stress conditions was related to the redox state of plastoquinone pool (see below for more details), whereas the subsequent mRNA accumulation was in line with continuous accumulation of H 2 O 2 (Yabuta et al, 2004 (Chang et al, 2004). This dye was shown to enhance the formation of singlet oxygen and hydrogen peroxide in chloroplasts, and the concomitant cAPX expression correlated with the methylviologen-generated H 2 O 2 accumulation in the cells.…”