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Effect of Low-Dose, Repeated Exposure of Contaminants of Emerging Concern on Plant Development and Hormone Homeostasis

Abstract

Treated wastewater is increasingly being utilized to meet agriculture’s water needs, however, treated wastewater contains numerous trace organic contaminants including constituents of emerging concern (CECs), such as pharmaceuticals and personal care products (PPCPs). With exposure and uptake of these compounds, phytotoxicity and health of crop plants is of concern, but is not well understood at present. This study simulated irrigation with treated wastewater and evaluated the effect of low-dose, chronic exposure to a mixture of 10 CECs, including 4 antibiotics, 3 analgesic anti-inflammatory drugs, 1 anti-epileptic, 1 beta-blocker, and 1 antimicrobial, on lettuce and cucumber plants, as well as the effect of the CEC mixture in conjunction with other abiotic stressors such as heat. The CEC mixture was added in nutrient media at 1-20X of their typical levels found in treated wastewater effluents. Relevant biological endpoints including germination, growth, phytohormone homeostasis, and CEC bioaccumulation into plant tissues were determined. Root length of lettuce seedlings significantly increased in a dose-dependent manner at the end of a 7 d germination study. However, a dose-dependent decrease in biomass was observed upon longer-term exposure (30 d) of cucumber seedlings to the CEC mixture, with the highest CEC treatment rate resulting in a relative percentage difference in average below-ground, above-ground, and total biomass of -51.2 ± 20.9, -26.3 ± 34.1, and -33.2 ± 41.7%, respectively. The response of selected phytohormones (auxins, jasmonic acid, and abscisic acid) were investigated to gain insight into the plant’s physiological response to CEC exposure, as well as in conjunction with heat stress, due to the involvement of these phytohormones in growth, nutrient allocation, transpiration, and defense. Levels of abscisic acid, a stress response hormone involved in stomatal closure, were found to be significantly elevated (p < 0.05) in the leaves with increasing exposure rates of CECs, but, decreased significantly (p < 0.05) in the roots at environmentally relevant CEC concentrations. Elevated abscisic acid in the leaves may cause stomatal closure, anti-transpiration activity, and reduced leaf expansion leading to slowed plant growth and impaired ability to adapt to additional stressors, such as extreme temperatures or salinity. The dose-response of auxin, a phytohormone involved in cell elongation and meristematic tissue growth, was characterized by a hormesis effect. A significant 6-fold increase was observed in stem auxin concentrations at the low CEC treatment rate as compared to the control, followed by a gradual decrease to 2-fold the control at the highest CEC treatment rate. Leaf auxin concentrations also significantly increased at the low CEC concentrations to 16-fold, followed by a decrease at the highest CEC treatment rate.

In nature, crops are simultaneously exposed to numerous biotic and abiotic stresses and therefore heat stress was chosen to investigate the interactive effects of simultaneous stresses on plants. Root auxin concentrations with heat, but no CEC exposure (59.8 ± 16.9 ng g-1, f.w.), were significantly (p < 0.05) elevated compared to root auxin concentrations from CEC exposure, demonstrating that different types of stress may have opposing effects on plant hormone homeostasis. Stem auxin concentrations were decreased significantly (p < 0.05) in the multi-stressed plants (65.3 ± 14.0 ng g-1, f.w.) as compared to those exposed only to the CEC mixture (132.6 ± 54.3 ng g-1, f.w.). In contrast, no significant differences in leaf abscisic or jasmonic acid contents due to heat stress was observed within the same CEC treatment.

Evaluating the potential impacts of CEC mixtures in recycled wastewater, biosolids and animal wastes on growth and development of plants is important in ensuring food security and sustainability. The results of this study have implications for the beneficial reuse of treated wastewater, biosolids, and animal wastes in agriculture as they contribute to the promotion of safe reuse practices and improve agricultural sustainability.

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