Auxins and Cytokinins Regulate Phytohormone Homeostasis and Thiol-Mediated Detoxification in the Green Alga Acutodesmus obliquus Exposed to Lead Stress

Abstract

Phytohormones, such as auxins and cytokinins, take part in the integration of growth control and stress response, but their role in algal adaptation to heavy metal remains to be elucidated. The current research indicated that lead (Pb), one of the most toxic metals in nature, causes severe depletion of endogenous cytokinins, auxins, and gibberellin and an increase in abscisic acid content in the green alga Acutodesmus obliquus. Exogenous auxins and cytokinins alleviate Pb toxicity through the regulation of the endogenous phytohormones' levels. Exogenously applied auxins provoked the coordinated activation metal tolerance mechanisms leading to the increase in phytochelatin synthase activity and accumulation of phytochelatins and their precursors, which are essential for Pb sequestration. On the other hand, phytochelatin synthesis decreased in algal cells treated with cytokinins. Significant changes in the levels of low molecular weight metabolites, mainly involved in metal chelation and glutathione synthesis pathway under the influence of phytohormones in algal cells growing in the presence of Pb stress, were observed. This is the first report showing that auxins and cytokinins are important regulatory factors in algal adaptation strategies to heavy metal stress based on thiol-mediated compounds and the maintenance of phytohormone homeostasis.

Phytohormonal Roles in Plant Responses to Heavy Metal Stress: Implications for Using Macrophytes in Phytoremediation of Aquatic Ecosystems

“…Likewise, when O. sativa seedlings were grown in Cd‐contaminated soil, a supplement of tryptophan (an auxin precursor), improved plant growth and final yield (Farooq et al 2015). Similarly, beneficial effects of exogenously applied auxin were observed for green algae, Acutodesmus obliquus (Turpin) Hegewald & Hanagata exposed to Pb stress (Piotrowska‐Niczyporuk et al 2020). Together, these findings suggest that the promotion or recovery of cytokinins and auxin after heavy metal exposure could help plants to overcome stress and recover healthy growth and development.…”

“…Heavy metal stress affects the metabolism of most groups of phytohormones. The complex interaction among the endogenous phytohormones triggers defense and response mechanisms in plants and aquatic organisms (Thao et al 2015; Piotrowska‐Niczyporuk et al 2020). The mechanisms that plants use to cope with different heavy metal stresses are often species‐dependent, but, generally, ethylene and its conjugates are crucial for plant response under heavy metal exposure (Thapa et al 2012; Montero‐Palmero et al 2014a, 2014b).…”

“…ABA = abscisic acid; APX = ascorbate peroxidase; BR = brassinosteroid; CAT = catalase; CK = cytokinin; ETH = ethylene; GA = gibberellin; GR = glutathione reductase; GSH = glutathione; JA = jasmonic acid; PA = polyamine; PC = phytochelatin; POD = peroxidase; ROS = reactive oxygen species; SA = salicylic acid; SOD = superoxide dismutase. Piotrowska-Niczyporuk et al 2020). The mechanisms that plants use to cope with different heavy metal stresses are often species-dependent, but, generally, ethylene and its conjugates are crucial for plant response under heavy metal exposure (Thapa et al 2012;Montero-Palmero et al 2014a, 2014b.…”

“…Free carboxylic groups can provide binding sites for heavy metals, as can proteins for which atoms of nitrogen, oxygen, and sulfur (S) may behave as ligands (Suñe et al 2007). A range of ligands that plants synthesize in response to heavy metal exposure can act as chelators; these include proteins, polysaccharides, polynucleic acids, or polypeptides such as glutathione (GSH) or phytochelatins (Hayward et al 2013; Liu et al 2015; Piotrowska‐Niczyporuk et al 2020). The biosynthesis and distribution of organic ligands require a complex hormonal regulatory network (Cobbett 2000; Hayward et al 2013; Bücker‐Neto et al 2017).…”

“…Several reviews have described the underlying pathways of metal stress responses via phytohormone actions (Fahad et al 2015; Bücker‐Neto et al 2017; Vishwakarma et al 2017), and these have added to our understanding of how phytohormones can regulate the responses of plants to environmental stress. Recently, studies have also investigated the external application of phytohormones to plants or algae, to increase stress tolerance for phytoremediation purposes (Khan et al 2015; Bücker‐Neto et al 2017; Piotrowska‐Niczyporuk et al 2020). However, to date, research on phytohormones in aquatic macrophyte species has focused primarily on hormone metabolite profiling and their growth regulatory functions under nonstressful conditions (Stirk and Van Staden 2003; Wanke 2011).…”