Drought and Oxidative Load in the Leaves of C3 Plants: a Predominant Role for Photorespiration?

Abstract

Although active oxygen species are produced at high rates in both the chloroplasts and peroxisomes of the leaves of C3 plants, most attention has focused on the potentially damaging consequences of enhanced chloroplastic production in stress conditions such as drought. This article attempts to provide quantitative estimates of the relative contributions of the chloroplast electron transport chain and the glycolate oxidase reaction to the oxidative load placed on the photosynthetic leaf cell. Rates of photorespiratory H2O2 production were obtained from photosynthetic and photorespiratory flux rates, derived from steady-state leaf gas exchange measurements at varying irradiance and ambient CO2. Assuming a 10% allocation of photosynthetic electron flow to the Mehler reaction, photorespiratory H2O2 production would account for about 70% of total H2O2 formed at all irradiances measured. When chloroplastic CO2 concentration rates are decreased, photorespiration becomes even more predominant in H2O2 generation. At the increased flux through photorespiration observed at lower ambient CO2, the Mehler reaction would have to account for more than 35% of the total photosynthetic electron flow in order to match the rate of peroxisomal H2O2 production. The potential signalling role of H2O2 produced in the peroxisomes is emphasized, and it is demonstrated that photorespiratory H2O2 can perturb the redox states of leaf antioxidant pools. We discuss the interactions between oxidants, antioxidants and redox changes leading to modified gene expression, particularly in relation to drought, and call attention to the potential significance of photorespiratory H2O2 in signalling and acclimation.

Photosynthesis and antioxidant activity in Jatropha curcas L. under salt stress

“…However, the present results are not consistent with the findings of Hernandez et al (1995) in salt-tolerant pea plants. The excess H 2 O 2 produced in peroxisomes and chloroplasts might diffuse to the cytosol and be converted to hydroxyl radicals via Fenton reaction (Moller et al, 2007), exacerbating lipid peroxidation (Noctor et al, 2002;Hernandez et al, 1995).…”

Peroxisomal Hydrogen Peroxide Is Coupled to Biotic Defense Responses by ISOCHORISMATE SYNTHASE1 in a Daylength-Related Manner

“…It may indicate that peroxisomal H 2 O 2 does not make a major contribution to overall tissue contents of peroxides or that other antioxidative systems replace catalase in cat2. Engagement of other H 2 O 2 -metabolizing systems in catalasedeficient plants is evidenced by adjustments in intracellular redox state at the level of the glutathione pool (Willekens et al, 1997;Noctor et al, 2002;Rizhsky et al, 2002). Therefore, we quantified reduced and oxidized forms of glutathione as a sensitive indicator of intracellular redox status.…”

“…Peroxisomes are important in the production of signal molecules, including ROS (del Río et al, 2006;Nyathi and Baker, 2006). Particularly in the leaves of C 3 plants, these organelles can be a rich source of H 2 O 2 through the photorespiratory glycolate oxidase reaction (Noctor et al, 2002). A role for peroxisomal H 2 O 2 in pathogen responses is consistent with studies of mutants for Ser:glyoxylate aminotransferase (Taler et al, 2004), an enzyme immediately downstream of glycolate oxidase in the photorespiratory pathway, as well as effects of photorespiratory conditions on the phenotypes of the lsd1 mutant (Mateo et al, 2004).…”

“…Recent data indicate that chloroplast-linked oxidative stress is mainly attributable to singlet oxygen rather than hydrogen peroxide (H 2 O 2 ; Triantaphylidès et al, 2008), while modeling showed that the chloroplast electron transport chain would have to devote a very high proportion of electrons to oxygen in order to meet the high rates of photorespiratory H 2 O 2 production in the peroxisomes (Noctor et al, 2002;Foyer and Noctor, 2003). Peroxisomal H 2 O 2 is notably metabolized by catalases, although ascorbate peroxidases are also associated with peroxisomes (del Río et al, 2006;Narendra et al, 2006;Nyathi and Baker, 2006).…”

Salt-Induced Changes in Antioxidative Enzyme Activities in Shoot Tissues of Two Atriplex Varieties

“…It is generally accepted that stress-induced deregulation of plant metabolism leads to the enhanced production of ROS, the cellular titer of which is policed by the antioxidant system (Beak and Skinner, 2003). Both ROS and soluble antioxidants are involved in signaling processes in plants: the picture that is emerging suggests that relatively stable oxidants (H 2 O 2 ) and antioxidants (ascorbate, glutathione) act as sensors of the 'oxidative load' on the cell (Noctor et al, 2002). Salinity may lead to the production of ROS and tissue damage (Adams et al, 2004).…”