Opposite fates of the purine metabolite allantoin under water and nitrogen limitations in bread wheat

Abstract

Key message Degradation of nitrogen-rich purines is tightly and oppositely regulated under drought and low nitrogen supply in bread wheat. Allantoin is a key target metabolite for improving nitrogen homeostasis under stress. Abstract The metabolite allantoin is an intermediate of the catabolism of purines (components of nucleotides) and is known for its housekeeping role in nitrogen (N) recycling and also for its function in N transport and storage in nodulated legumes. Allantoin was also shown to differentially accumulate upon abiotic stress in a range of plant species but little is known about its role in cereals. To address this, purine catabolic pathway genes were identified in hexaploid bread wheat and their chromosomal location was experimentally validated. A comparative study of two Australian bread wheat genotypes revealed a highly significant increase of allantoin (up to 29-fold) under drought. In contrast, allantoin significantly decreased (up to 22-fold) in response to N deficiency. The observed changes were accompanied by transcriptional adjustment of key purine catabolic genes, suggesting that the recycling of purine-derived N is tightly regulated under stress. We propose opposite fates of allantoin in plants under stress: the accumulation of allantoin under drought circumvents its degradation to ammonium (NH 4 +) thereby preventing N losses. On the other hand, under N deficiency, increasing the NH 4 + liberated via allantoin catabolism contributes towards the maintenance of N homeostasis.

The intersection of nitrogen nutrition and water use in plants: new paths toward improved crop productivity

“…Oxidation of the purine catabolite xanthine to glyoxylate liberates three molecules of CO 2 and four molecules of NH 4 + . Purine catabolism via turnover of RNA is also induced under nutrient depletion stress ( Taylor et al , 1993 ; Melino et al , 2018 ; Casartelli et al ., 2019 ). Nitrogen-starved wheat plants exogenously supplied with the purine catabolites xanthine and allantoin grew and photosynthesized as well as plants re-supplied with NO 3 – , suggesting that they can support plant growth ( Melino et al , 2018 ).…”

Nucleotide Metabolism in Plants

“…Purine catabolism can lead to the complete disintegration of the purine ring in plants (Fig. 5B; Werner and Witte, 2011) to recycle nitrogen (Soltabayeva et al, 2018), but it is also used to generate the intermediates uric acid and especially allantoin, which counteract stress by reducing reactive oxygen species (Brychkova et al, 2008;Watanabe et al, 2014;Todd, 2016, 2018;Lescano et al, 2016;Ma et al, 2016;Casartelli et al, 2019;Nourimand and Todd, 2019). Sometimes also the accumulation of allantoate has been observed (Alamillo et al, 2010).…”

“…One may speculate that allantoin accumulation under certain stress conditions might be caused in part by altered peroxisome-to-ER transport efficiency. However, one apparent reason for allantoin accumulation is an altered catalytic capacity for allantoin generation and degradation under stress (Irani and Todd, 2016;Lescano et al, 2016;Irani and Todd, 2018;Casartelli et al, 2019).…”

Transcripts of wheat at a target locus on chromosome 6B associated with increased yield, leaf mass and chlorophyll index under combined drought and heat stress

“…The majority of differentially expressed genes under drought were located on chromosome 4B with upregulated genes in NILs carrying the exotic allele being involved in alanine, aspartate and glutamate metabolism. All three amino acids have been observed to increase in developing grains of drought-resistant wheat plants when subjected to drought [49] and form part of the photorespiratory cycle [50,51]. Differentially expressed genes under combined drought and heat stress were dominantly located on chromosomes 1B, 6B and 7A and were associated with the metabolism of glutathione, a component of the antioxidative system in plants, which is synthetised from glycine, a by-product of photorespiration [51].…”