How do plants cope with oxidative stress in nature? A study on the dwarf bearded iris (Iris pumila)

Abstract

Oxidative stress results from incongruity between the generation of toxic reactive oxygen species (ROS) and the availability of their scavengers—antioxidants. Although the short-term effects of this phenomenon are attracting much scientific attention, oxidative stress may influence an organism’s metabolism over the long (evolutionary) time scale as well. To disentangle the impact of strong light intensity from co-occurring abiotic stresses in creating adaptive responses in antioxidants and heat shock proteins (Hsps), an environment manipulation experiment was performed using a xerophyte clonal monocot, Iris pumila, native to semi-arid grasslands at the Deliblato Sands. This species is very tolerant to the combined effect of extreme abiotic stressors such as high light intensity, elevated soil surface temperatures, and scarcity of water, which commonly takes place in its natural habitats during the summer. By shading half of each selected clone, leaving the other half sun-exposed, we contrasted short-term effects of reduced daylight intensity with long-term effects of photo-oxidative stress. In both light treatments, the enzymatic activities of SOD and APX antioxidants were similar in magnitude, whereas those of CAT and POD significantly decreased in exposed compared to shaded leaves. Moreover, exposed leaves expressed a unique CAT isoform that differed biochemically from two CAT isoforms observed in shaded leaves. The content of non-enzymatic antioxidants, carotenoids (Car), remained constant with the reduction of light intensity, but their ratio to total chlorophylls (Chl) significantly decreased compared to that expressed in full sunlight. The abundance of Hsps was considerably greater in exposed than in shaded leaves, especially regarding the inducible isoforms, Hsp70 and Hsp90a, as were their proportions in relation to the constitutively expressed Hsp90b isoform. The presented results, thus, indicate that adaptive metabolic responses of I. pumila leaves to photo-oxidative stress entailed the high activity of two key enzymatic antioxidants, SOD and APX and the expression of a light-resistant CAT—to counteract the stress-mediated ROS accumulation, the increased Car to Chl ratio—to adjust the photosynthetic apparatus to the high light conditions, as well as the accelerated biosynthesis of heat shock proteins Hsp70 and Hsp90—to preserve the cellular proteostasis.