Melatonin ameliorates aluminum toxicity through enhancing aluminum exclusion and reestablishing redox homeostasis in roots of wheat

Abstract

Melatonin is a universal regulator modulating plant development and responses to abiotic stresses. The alteration and potential roles of melatonin in mediating aluminum (Al) tolerance were investigated in two wheat genotypes differing in Al resistance. Using the high‐resolution mass spectrometry, we observed that melatonin contents in Xi Aimai‐1 were 1.7‐fold higher than that in Yangmai‐5. Application of melatonin conferred Al resistance in both genotypes. Melatonin treatment scavenged reactive oxygen species (ROS) accumulation and alleviated Al‐induced oxidative damage to lipids and proteins by stimulating antioxidant enzymes and augmenting antioxidants. Additionally, melatonin treatment decreased root tip‐Al contents by 19.0% and 15.5% in Xi Aimai‐1 and Yangmai‐5, respectively. Malate efflux, however, was not altered by melatonin under Al stress. The amount of cell wall polysaccharide and pectin methylesterase activity was significantly increased by Al treatment; but suppressed by melatonin. Melatonin synthesis inhibitor, p‐CPA, significantly increased the amount of the Al binding in cell walls of the tolerant genotype, whereas exogenous melatonin decreased cell wall Al content in the sensitive genotype. These results suggest that melatonin alleviated Al toxicity through augmenting antioxidants and inducing antioxidant enzymes to control ROS and enhancing exclusion of Al from root apex by altering cell wall polysaccharides in wheat.

Melatonin: A master regulator of plant development and stress responses

“…Ambient temperature is a primary factor affecting the rate of plant development (Sung et al, 2003; Penfield, 2008; Liu et al, 2018). Both cold and heat stress can alter the redox status, inducing ROS accumulation and causing peroxidative damage to membranes.…”

“…Melatonin is generally maintained at a relatively constant level in plants under normal growth conditions. However, melatonin levels are strongly affected by unfavorable conditions such as high light intensity, cold, heat, drought, and heavy metal stress (Arnao and Hernández-Ruiz, 2014;Zhang et al, 2015;Sun et al, 2020). For instance, barley and lupine seedlings treated with chemical agents such as NaCl, ZnSO 4 , and H 2 O 2 showed increased melatonin levels Hernández-Ruiz, 2009a, 2014).…”

“…Melatonin improves heavy metal tolerance primarily by enhancing antioxidant activity (Rodriguez et al, 2004). For instance, exogenous melatonin treatment stimulated the activity of antioxidant enzymes, increased antioxidant levels, and inhibited ROS production in wheat seedlings under aluminum stress (Sun et al, 2020).…”

“…Melatoninmediated nitric oxide signaling improves tolerance to cadmium and lead by reducing oxidative stress in plants (Kaya et al, 2019;Okant and Kaya, 2019), and melatonin biosynthesis induced by heavy metal stress requires NO . Melatonin affects biological processes not only by improving antioxidant defense systems but also by facilitating the exclusion or sequestration of heavy metals in plant cells (Hasan et al, 2015(Hasan et al, , 2019Nawaz et al, 2018;Cao et al, 2019;Sun et al, 2020). Melatonin decreases cadmium accumulation in Arabidopsis by modulating the expression of several heavy metal transporter genes, including ABC transporter genes and PCR2 (Gu et al, 2017;He et al, 2020).…”

“…More recently, the identification of the first putative plant melatonin receptor in Arabidopsis (Arabidopsis thaliana) suggested that melatonin could be a phytohormone Hernández-Ruiz 2019a, 2020b). In addition to this key piece of evidence, melatonin exhibits many hormone-like activities including regulating seed germination, root growth and development, leaf senescence, circadian rhythms, postharvest fruit ripening, and the responses of plants to adverse environmental conditions (Li et al, 2012;Yin et al, 2013;Zhang et al, 2014a;Arnao and Hernández-Ruiz 2015;Shi et al, 2015cShi et al, , 2016bSun et al, 2015;Li et al, 2019;Sun et al, 2020). In this review, we explore the biosynthetic and possible degradation pathways of melatonin, the myriad roles of melatonin, and the molecular mechanisms underpinning its many functions in plants.…”