The halophytic model plant Thellungiella salsuginea exhibited increased tolerance to phenanthrene-induced stress in comparison with the glycophitic one Arabidopsis thaliana: Application for phytoremediation

Abstract

Polycyclic aromatic hydrocarbons constitute a large family of organic environmental pollutants. Hence, a particular attention has been attributed to all approaches involved in the reduction of their contamination in water and natural ecosystems. Plant tolerance, absorption, accumulation, and likely biodegradation of these pollutants, known as phytoremediation, have emerged as an efficient technique to remediate environments contaminated with polycyclic aromatic hydrocarbons. The present work was aimed to compare the tolerance to phenanthrene (a polycyclic aromatic hydrocarbon) in the two model plants: Arabidopsis thaliana (glycophyte) and Thellungiella salsuginea (halophyte). Our study showed that the development of these two species was reduced under phenanthrene stress, the effect being more pronounced in Arabidopsis thaliana than in Thellungiella salsuginea. In parallel, results from the intrinsic quantum yield of photosystem II and chlorophyll concentrations were concomitant with those of growth and phenotypic changes, and confirmed the higher tolerance of Thellungiella salsuginea compared to that of Arabidopsis thaliana. The intrinsic quantum yield of photosystem II was drastically decreased in the glycophyte, which indicates a marked disturbance in photosystem II performance. This induced a severe oxidative stress as shown by the utilization of specific reactive oxygen species probes. In parallel, the activities of glutathione reductase, gaiacol peroxidase, and superoxide dismutase were increased by 95, 73, and 36%, respectively, which indicates a marked phenanthrene-induced oxidative stress. In Thellungiella salsuginea, photosystem II performance was not significantly affected. This species showed less accumulated reactive oxygen species than Arabidopsis thaliana. Its enzymatic antioxidant system showed few changes as superoxide dismutase was the only enzyme whose activity was enhanced (+34%). A 3 much higher capacity of recovery was also noticed in this halophyte as compared to the glycophyte. Indeed, it seems that Thellungiella salsuginea accumulated phenanthrene in stomata, which suggests its possible volatilization. All these data, taken together, add new insight to the mechanisms involved in halophytic plant tolerance to abiotic stresses and their potential use in phytoremediation. Graphical abstract Phenanthrene Glycophytic

Increased tolerance to organic xenobiotics following recent allopolyploidy in Spartina (Poaceae)

“…NBT allowed the observation of O2compounds which precipitate in blue color on plant tissues [34,46]. ROS production detected in leaf tissues reflects oxidative stress damages related to phenanthrene exposure.…”

“…Xenobiotics affect the plant physiology by reducing major metabolic functions such as photosynthesis and respiration [31][32][33]. Moreover, PAHs are described to induce oxidative stress, through ROS (Reactive Oxygen Species) accumulation in plant cells, which in turn reduce plant development and growth, chlorophyll levels, and lead to trichome deformation and necrosis [31,32,34]. Oxidative stress damages induced by ROS under PAH stress are balanced by antioxidant enzymes, that are most likely limiting xenobiotic tolerance abilities [32].…”

Comparative Transcriptomic Approaches Exploring Contamination Stress Tolerance in Salix sp. Reveal the Importance for a Metaorganismal de Novo Assembly Approach for Nonmodel Plants

“…Nevertheless, in terms of what could be predicted to be differentially expressed (DE) in leaves of willow due to petroleum hydrocarbon contamination in soil, the following would be expected: general stress responses (potentially including oxidative stress from overproduction of reactive oxygen species; Yurekli and Porgali, 2006), indirect treatment-specific interactions (such as salinity and drought response interactions; Popko et al, 2010;Bauddh and Singh, 2012), and direct responses to petroleum hydrocarbons. In terms of a direct response, there is little evidence suggesting similar organic contaminates are often absorbed and mobilized to above-ground tissue (Alkio et al, 2005;Watts et al, 2006;El Amrani et al, 2015;Shiri et al, 2015) or metabolized to any degree by willow directly. There is, however, a growing body of evidence pertaining to metaorganismal interactions whereby a multitude of organisms collectively exploit these unique environmental conditions (Weyens et al, 2009;Kang et al, 2012;Bell et al, 2014a;Yergeau et al, 2014;Gonzalez et al, 2015).…”

Recent hybridization and allopolyploidy reprogrammedSpartinamicroRNA expression under xenobiotic induced stress

“…Among the organic xenobiotic compounds, PAHs (Polycyclic Aromatic Hydrocarbons) represent widespread pollutants, alarming by their environmental toxicity with ecological and public health issues. Physiological impact of PAHs on plant physiology is well documented, mainly in the plant model Arabidopsis (Alkio et al ., 2005; Liu et al ., 2009; Shiri et al ., 2015; Dumas et al ., 2016). Absorption of xenobiotics by plant roots occurs through passive or active transport mechanisms (Pilon-Smits, 2005; Zhan et al ., 2012).…”

“…In plants, PAHs reduce growth and development by disrupting major metabolic functions like photosynthesis. Depending on plant tolerance abilities, PAHs may induce necrosis and promote oxidative stress by ROS (Reactive Oxygen Species) production, that may limit plant tolerance (Alkio et al ., 2005; Shiri et al ., 2015; Dumas et al ., 2016).…”