Arabidopsis Chloroplastic Ascorbate Peroxidase Isoenzymes Play a Dual Role in Photoprotection and Gene Regulation under Photooxidative Stress

Abstract

Though two types of chloroplastic ascorbate peroxidase (APX) located in the thylakoid membrane (tAPX) and stroma (sAPX) have been thought to be key regulators of intracellular levels of H(2)O(2), their physiological significance in the response to photooxidative stress is still under discussion. Here we characterized single mutants lacking either tAPX (KO-tAPX) or sAPX (KO-sAPX). Under exposure to high light or treatment with methylviologen under light, H(2)O(2) and oxidized proteins accumulated to higher levels in both mutant plants than in the wild-type plants. On the other hand, the absence of sAPX and tAPX drastically suppressed the expression of H(2)O(2)-responsive genes under photooxidative stress. Interestingly, the most marked effect of photooxidative stress on the accumulation of H(2)O(2) and oxidized protein and gene expression was observed in the KO-tAPX plants rather than the KO-sAPX plants. The present findings suggest that both chloroplastic APXs, but particularly tAPX, are important for photoprotection and gene regulation under photooxidative stress in Arabidopsis leaves.

Oxidative Stress: Antagonistic Signaling for Acclimation or Cell Death?

“…We propose that H 2 O 2 , sourced from chloroplasts and plasma membrane-located NADPH oxidases, accelerates ABA signaling in BSCs. Null mutants in chloroplastic APX genes have been used to support the hypothesis that a specific H 2 O 2 signal from chloroplasts influences the rate of induction of APX2 and other high-light-responsive genes (Maruta et al, 2010). Within 10 min of exposure to high light, BSC chloroplasts produce H 2 O 2 , and this is not associated with irreversible photoinhibition or oxidative stress but is associated with rapid induction of APX2 expression (Fryer et al, 2003;Galvez-Valdivieso et al, 2009;Maruta et al, 2010).…”

“…Null mutants in chloroplastic APX genes have been used to support the hypothesis that a specific H 2 O 2 signal from chloroplasts influences the rate of induction of APX2 and other high-light-responsive genes (Maruta et al, 2010). Within 10 min of exposure to high light, BSC chloroplasts produce H 2 O 2 , and this is not associated with irreversible photoinhibition or oxidative stress but is associated with rapid induction of APX2 expression (Fryer et al, 2003;Galvez-Valdivieso et al, 2009;Maruta et al, 2010). However, H 2 O 2 accumulation is contained within BSC chloroplasts (Fryer et al, 2003;Galvez-Valdivieso et al, 2009), suggesting that any H 2 O 2 signal has to be transduced to a non-ROS signal to traverse the reducing environment of the cytosol.…”

Cellular redox regulation, signaling, and stress response in plants

“…79) Exposure to HL or a treatment with MV under illumination led to the accumulation of higher levels of H 2 O 2 and oxidized proteins in KO-sAPX and KO-tAPX plants than in wild-type plants. The most prominent effect of photooxidative stress on oxidative damage was observed in KO-tAPX plants, not in KO-sAPX plants.…”

“…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. Further expressional analyses and forward genetic approaches have revealed that the phytohormone abscisic acid (ABA), GSH, and 3′-phosphoadenosine 5′-phosphate (PAP), which acts as retrograde signal from chloroplasts to the nucleus, are also involved in regulating the expression of APX2 in Arabidopsis.…”

“…79,[90][91][92][93][94][95][96][97][98][99][100][101][102][103][104][105][106][107] Although chloroplasts, mitochondria, and peroxisomes are the significant sources of ROS, Arabidopsis knockout mutants lacking organellar APX isoenzymes showed very weak phenotypes against oxidative stress. 79,[102][103][104]107) cAPX is known to be more important for stress tolerance than other APX isoenzymes even though the cytosol is not a significant source of ROS. [90][91][92][93][94][95] Thus, the lack of APX1 in Arabidopsis enhanced its sensitivity to various types of stresses such as HL, treatment with MV, and a combination of drought and heat.…”