Lipid Peroxide-Derived Short-Chain Carbonyls Mediate Hydrogen Peroxide-Induced and Salt-Induced Programmed Cell Death in Plants  

Abstract

Lipid peroxide-derived toxic carbonyl compounds (oxylipin carbonyls), produced downstream of reactive oxygen species (ROS), were recently revealed to mediate abiotic stress-induced damage of plants. Here, we investigated how oxylipin carbonyls cause cell death. When tobacco (Nicotiana tabacum) Bright Yellow-2 (BY-2) cells were exposed to hydrogen peroxide, several species of short-chain oxylipin carbonyls [i.e. 4-hydroxy-(E)-2-nonenal and acrolein] accumulated and the cells underwent programmed cell death (PCD), as judged based on DNA fragmentation, an increase in terminal deoxynucleotidyl transferase dUTP nick end labeling-positive nuclei, and cytoplasm retraction. These oxylipin carbonyls caused PCD in BY-2 cells and roots of tobacco and Arabidopsis (Arabidopsis thaliana). To test the possibility that oxylipin carbonyls mediate an oxidative signal to cause PCD, we performed pharmacological and genetic experiments. Carnosine and hydralazine, having distinct chemistry for scavenging carbonyls, significantly suppressed the increase in oxylipin carbonyls and blocked PCD in BY-2 cells and Arabidopsis roots, but they did not affect the levels of ROS and lipid peroxides. A transgenic tobacco line that overproduces 2-alkenal reductase, an Arabidopsis enzyme to detoxify a,b-unsaturated carbonyls, suffered less PCD in root epidermis after hydrogen peroxide or salt treatment than did the wild type, whereas the ROS level increases due to the stress treatments were not different between the lines. From these results, we conclude that oxylipin carbonyls are involved in the PCD process in oxidatively stressed cells. Our comparison of the ability of distinct carbonyls to induce PCD in BY-2 cells revealed that acrolein and 4-hydroxy-(E)-2-nonenal are the most potent carbonyls. The physiological relevance and possible mechanisms of the carbonyl-induced PCD are discussed.

Suppression of Chloroplastic Alkenal/One Oxidoreductase Represses the Carbon Catabolic Pathway in Arabidopsis Leaves during Night

“…Therefore, lipid-derived RCS also could affect various molecular targets, which were not examined in this study in plant cells because of their reactivities, and aor mutants might cause the decrease of carbon utilization during the night and the growth retardation as a result of the modification of plant cell components. Moreover, lipid-derived RCS have been reported to be involved in signaling processes such as auxin signaling and cell division (Farmer and Mueller, 2013;Biswas and Mano, 2015;Yamauchi et al, 2015). Based on these reports, lipid-derived RCS diffused in plant cells might modify the gene expression network, which is not analyzed in this study, and cause the decrease of carbon utilization during the night and the growth retardation in aor mutants.…”

“…Combining the results of Mano et al (2014a) and our study, we concluded that chloroplasts are a major production site of lipid-derived RCS and might be an initiator for lipidderived RCS-dependent signaling cascades in plant cells. Accordingly, further intensive studies are required to elucidate the molecular targets of lipidderived RCS, especially the receptors of lipid-derived RCS triggering the signal cascade in plant cells (Farmer and Mueller, 2013;Biswas and Mano, 2015).…”

“…These facts indicate that the production and the accumulation of lipid-derived RCS should be dangerous for plants. On the other hand, recent studies have also shown that lipid-derived RCS play an important role in the signaling process and modify the gene expression of several important cellular processes, including detoxification, heat stress, cell division, auxin signaling, and programmed cell death (Farmer and Mueller, 2013;Biswas and Mano, 2015). Indeed, Yamauchi et al (2015) reported that exposure to lipid-derived RCS modifies the expression of transcriptional factors in plant cells, and the modification of gene expression networks provides tolerance to the heat stress.…”

Aldehyde Oxidase 4 Plays a Critical Role in Delaying Silique Senescence by Catalyzing Aldehyde Detoxification

“…In addition, there is an increasing body of evidence for the generation of toxic levels of aldehyde in response to environmental stresses, especially lipid peroxidation-derived reactive carbonyl species (RCS) such as malondialdehyde (MDA), acrolein, and 4-hydroxyl-2-nonenal (HNE; Mano, 2012, Biswas andMano, 2015). The detoxification of aldehydes by plant AAO4 or by other AAO family members has never been shown.…”

“…Aldehydes can be extremely toxic when produced in excess because of their inherent chemical reactivity (Bartels, 2001;Kotchoni et al, 2006;Zhang et al, 2012;Biswas and Mano, 2015). These toxic compounds also may lead to lipid peroxidation and reactive oxygen species (ROS) enhancement (Lamb and Dixon, 1997;Bolwell, 1999) to levels that could damage biomolecules such as proteins, lipids, carbohydrates, and DNA, which, in extreme cases, can lead to plant death (Gratao et al, 2005, for review, see Gill and Tuteja, 2010;Mano, 2012).…”