Abstract
Maize shoot development progresses from non-pigmented meristematic cells at the base of the leaf to expanded and non-dividing green cells of the leaf blade. This transition is accompanied by the conversion of promitochondria and proplastids to their mature forms and massive fragmentation of both mitochondrial DNA (mtDNA) and plastid DNA (ptDNA), collectively termed organellar DNA (orgDNA). We measured developmental changes in reactive oxygen species (ROS), which at high concentrations can lead to oxidative stress and DNA damage, as well as antioxidant agents and oxidative damage in orgDNA. Our plants were grown under normal, non-stressful conditions. Nonetheless, we found more oxidative damage in orgDNA from leaf than stalk tissues and higher levels of hydrogen peroxide, superoxide, and superoxide dismutase in leaf than stalk tissues and in light-grown compared to dark-grown leaves. In both mitochondria and plastids, activities of the antioxidant enzyme peroxidase were higher in stalk than in leaves and in dark-grown than light-grown leaves. In protoplasts, the amount of the small-molecule antioxidants, glutathione and ascorbic acid, and catalase activity were also higher in the stalk than in leaf tissue. The data suggest that the degree of oxidative stress in the organelles is lower in stalk than leaf and lower in dark than light growth conditions. We speculate that the damaged/fragmented orgDNA in leaves (but not the basal meristem) results from ROS signaling to the nucleus to stop delivering DNA repair proteins to mature organelles producing large amounts of ROS.
Highlights
Reactive oxygen species (ROS) can have both detrimental and beneficial effects on plants
We measured the levels of ROS, antioxidant agents, and organellar DNA (orgDNA) damage at three stages of maize development: stalk lower, stalk upper, and the blades from the first three leaves (Table 1 and see “Materials and Methods” section)
Chloroplasts and mitochondria are the main sites of ROS production, ROS profoundly influence the chemistry in peroxisomes, cytosol, and vacuoles (Asada, 2006; Noctor and Foyer, 2016; Kohli et al, 2019)
Summary
Reactive oxygen species (ROS) can have both detrimental and beneficial effects on plants. ROS can lead to oxidative stress by causing damage to various biomolecules. ROS are produced as unavoidable byproducts of electron transport reactions in both respiration and photosynthesis, and damage-defense measures are employed to ameliorate oxidative stress. ROS function in modifying the cell wall during development, as signaling molecules to maintain cellular and organismal homeostasis, and to regulate plant development (Mittler, 2017; Smirnoff and Arnaud, 2019). ROS can affect the distribution of chloroplasts within a cell and the ability to resist pathogen attack (Park et al, 2018; Ding et al, 2019), as well as the fate of stem cells (Zeng et al, 2017; Yang et al, 2018). Organellar ROS and DNA Damage in Maize
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