A Different Pattern of Production and Scavenging of Reactive Oxygen Species in Halophytic Eutrema salsugineum (Thellungiella salsuginea) Plants in Comparison to Arabidopsis thaliana and Its Relation to Salt Stress Signaling

Abstract

Isolated thylakoids from halophytic Eutrema salsugineum (Thellungiella salsuginea) produces more H2O2 in comparison to glycophytic Arabidopsis thaliana. The first objective of this study was to verify whether this feature is relevant also to the intact chloroplasts and leaves. Enhanced H2O2 levels in chloroplasts and leaves of E. salsugineum were positively verified with several methods (electron microscopy, staining with Amplex Red and with diaminobenzidine). This effect was associated with a decreased ratio of O2•–/H2O2 in E. salsugineum in comparison to A. thaliana as detected by electron paramagnetic resonance method. As a next step, we tested how this specific ROS signature of halophytic species affects the antioxidant status and down-stream components of ROS signaling. Comparison of enzymatic antioxidants revealed a decreased activity of ascorbate peroxidase (APX), enhanced activity of glutathione peroxidase, and the presence of thylakoid-bound forms of iron superoxide dismutase (FeSOD) and APX in E. salsugineum. These cues were, however, independent from application of salt stress. The typical H2O2-dependent cellular responses, namely the levels of glucosinolates and stress-related hormones were determined. The total glucosinolate content in E. salsugineum water-treated leaves was higher than in A. thaliana and increased after salinity treatment. Treatment with salinity up-regulated all of tested stress hormones, their precursors and catabolites [abscisic acid (ABA), dihydrophaseic acid, phaseic acid, 1-aminocyclopropane-1-carboxylic acid, salicylic acid, jasmonic acid, cis-(+)-12-oxo-phytodienoic acid and jasmonoyl-L-isoleucine] in A. thaliana, whereas in E. salsugineum only a stimulation in ethylene synthesis and ABA catabolism was noted. Obtained results suggest that constitutively enhanced H2O2 generation in chloroplasts of E. salsugineum might be a crucial component of stress-prepardeness of this halophytic species. It shapes a very efficient antioxidant protection (in which glucosinolates might play a specific role) and a fine tuning of hormonal signaling to suppress the cell death program directed by jasmonate pathway.

The outer membrane Omp85‐like protein P39 influences metabolic homeostasis in mature Arabidopsis thaliana

“…Oxidative stress is known to induce thylakoid swelling (e.g. Yamane et al 2012;Gao et al 2015;Meng et al 2016;Pilarska et al 2016) as seen in the p39 mutants (Fig. 3).…”

Halophytism: What Have We Learnt From Arabidopsis thaliana Relative Model Systems?

“…These findings led the authors to speculate that enhanced leakage of H 2 O 2 from E. salsugineum plastids preadapts the halophyte to salt stress by maintaining an up-regulated antioxidant system while preventing ROS damage. This hypothesis is further supported by the following observations: (1) the reduced activity of H 2 O 2 -detoxifying enzymes, such as ascorbate peroxidase (APX) in E. salsugineum and similar activities of catalase in E. salsugineum and Arabidopsis (Pilarska et al, 2016); and (2) the ability of E. salsugineum to sustain a highly reduced plastoquinone pool (Wiciarz et al, 2015(Wiciarz et al, , 2018. This could facilitate the persistence of the cellular H 2 O 2 signal (Bose et al, 2014).…”

“…A similar amount of H 2 O 2 production is induced in Arabidopsis and E. salsugineum leaves a few hours after a 400 mm NaCl shock treatment, whereas higher induction of H 2 O 2 is observed in E. salsugineum roots (Ellouzi et al, 2014). However, a more detailed analysis using plants adapted to milder saline conditions (150 mm for Arabidopsis and 300 mm for E. salsugineum), employing a variety of complementary methods, demonstrated that both isolated thylakoid membranes and chloroplasts from intact E. salsugineum leaf tissue produce more H 2 O 2 in both control and saline conditions compared with Arabidopsis (Pilarska et al, 2016). Furthermore, under control conditions, a lower amount of damaging superoxide is generated in E. salsugineum than in Arabidopsis, which is correlated with reduced lipid peroxidation in isolated thylakoids and intact leaves of the halophyte.…”

Dark period transcriptomic and metabolic profiling of two diverseEutrema salsugineumaccessions

“…Eutrema salsugineum (formerly Thellungiella halophila ) is a model species for the study of plant stress tolerance (Amtmann, 2009; Bressan et al, 2001; Griffith et al, 2007; Oh et al, 2010; Orsini et al, 2010; Pilarska et al, 2016; Taji et al, 2004; Volkov et al, 2003; Wong et al, 2005). The two most commonly studied accessions, Shandong (SH) and Yukon (YK), are native to the Yellow River region of China (Bressan et al, 2001; Inan et al, 2004) and the Yukon territories of Canada (Wong et al, 2005), respectively.…”