Allantoin Increases Cadmium Tolerance in Arabidopsis via Activation of Antioxidant Mechanisms

Abstract

Plants apply various molecular, physiological and morphological strategies in response to undesirable environmental conditions. One of the possible responses which may contribute to surviving stressful conditions is the accumulation of ureides. Ureides are recognized as important nitrogen-rich compounds involved in recycling nitrogen in plants to support growth and reproduction. Amongst them, allantoin not only serves as a transportable nitrogen-rich compound, but has also been suggested to protect plants from abiotic stresses via minimizing oxidative damage. This work focuses on the effect of cadmium (Cd) on ureide metabolism in Arabidopsis, in order to clarify the potential role of allantoin in plant tolerance to heavy metals. In response to Cd treatment, allantoin levels increase in Arabidopsis thaliana, ecotype Col-0, due to reduced allantoinase (ALN) gene expression and enzyme activity. This coincides with increases in uricase (UO) transcripts. UO and ALN encode the enzymes for the production and degradation of allantoin, respectively. ALN-negative aln-3 Arabidopsis mutants with elevated allantoin levels demonstrate resistance to soil-applied CdCl, up to 1,500 μM. Although aln-3 mutants take up and store more Cd within their leaf tissue, they contain less damaging superoxide radicals. The protective mechanism of aln-3 mutants appears to involve enhancing the activity of antioxidant enzymes such as superoxide dismutase and ascorbate peroxidase.

Source and sink mechanisms of nitrogen transport and use

“…However, transporters involved in vacuolar import and efflux of ureides have not yet been identified. Ureides are also present in nonleguminous, amino acid-transporting plant species, where increased ureide/allantoin concentrations seem to trigger a general response to abiotic and biotic stress (Watanabe et al, 2014;Nourimand & Todd, 2016;Takagi et al, 2016).…”

“…Research using amino acid or ureide transporter mutants or overexpressors has demonstrated that modifications in organic N transport processes and associated alterations in symplasmic, subcellular or apoplastic N pools induce complex physiological changes in source and sink. The signals inducing these changes are still unknown but might involve specific amino acids such as glutamine/glutamate (Gutierez et al, 2008) and proline Biancucci et al, 2015), or related N compounds such as S-methyl-methionine or allantoin Nourimand & Todd, 2016;Takagi et al, 2016). In addition, changes in the C : N ratio (Wang & Ruan, 2016), amino acid imbalance (Liu et al, 2010;Yu et al, 2015) or other factors including mRNAs, small RNAs, peptides, proteins and hormones (Lee et al, 2016;Bellegarde et al, 2017) may present signals causing plant responses via complex transduction pathways.…”

NmeA, a novel efflux transporter specific for nucleobases and nucleosides, contributes to metal resistance in Aspergillus nidulans

“…The protective mechanism in aln‐3 mutants involves enhanced activity of superoxide dismutase and ascorbate peroxidase, confirming that Cd causes oxidative stress (Nourimand and Todd, ). Thus, the importance of purine breakdown to uric acid and ureides might also be related to scavenging of reactive ROS (Brychkova et al ., , Takagi et al ., ; Nourimand and Todd, ). Other studies have further shown that various abiotic stresses activate allantoin and allantoate accumulation, conferring increased stress resistance to plants (Yesbergenova et al ., , Alamillo et al ., , Watanabe et al ., , Irani and Todd, ).…”

“…Additionally, aln‐3 loss‐of‐function mutants, which have elevated allantoin levels, show increased resistance to Cd, as they seem to contain less damaging superoxide radicals. The protective mechanism in aln‐3 mutants involves enhanced activity of superoxide dismutase and ascorbate peroxidase, confirming that Cd causes oxidative stress (Nourimand and Todd, ). Thus, the importance of purine breakdown to uric acid and ureides might also be related to scavenging of reactive ROS (Brychkova et al ., , Takagi et al ., ; Nourimand and Todd, ).…”

Influence of Nitrogen Deficiency on Ureide Mediated Stress Resistance in Arabidopsis thaliana

“…The purpose of this study was to analyze the interaction between varying concentrations of environmental nitrogen and cadmium, and determine how this interaction may affect the growth of wild type (WT) and mutant aln A. thaliana seedlings. Nourimand and Todd (2016) have observed enhanced growth of aln--3 mutant lines in both agar and soil environments subjected to cadmium. In addition, the increased tolerance of aln mutants to other abiotic stresses such as high osmoticum and enhanced drought has been attributed to their high levels of allantoin (Watanabe et al, 2014).…”