Abstract
Key messageDegradation 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.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 (NH4+) thereby preventing N losses. On the other hand, under N deficiency, increasing the NH4+ liberated via allantoin catabolism contributes towards the maintenance of N homeostasis.
Highlights
Nitrogen (N) is a macronutrient required in large quantities for plant development and growth with N deficiency causing chlorosis in older leaves and significant yield losses
The TaAS genes were identified on chromosome group 4 and the TaUAH genes were localised on chromosome group 5 (TaUAH-5AS/TaUAH5BS/TaUAH-5DS)
The assumption that the N remobilised from allantoin supports plant growth is supported by studies showing that Arabidopsis and rice seedlings could grow with ureides as a sole N source (Desimone et al 2002; Brychkova et al 2008; Lee et al 2018), growth was delayed in comparison to plants supplied with inorganic N. This is in contrast to wheat seedlings that, resupplied with allantoin and xanthine as a sole source of N after N O3− starvation, grew and photosynthesised as well as those re-supplied with NO3− (Melino et al 2018). These findings suggest that the enhanced activity of the purine catabolic pathway provides an internal source of organic N used to maintain homeostasis under low N conditions whereas the accumulation of allantoin under drought releases pressure from the GS-GOGAT cycle thereby preventing accumulation of toxic levels of N H4+ and possibly N losses due to volatilization (Fig. 9)
Summary
Nitrogen (N) is a macronutrient required in large quantities for plant development and growth with N deficiency causing chlorosis in older leaves and significant yield losses. Under N deficiency and natural senescence plants translocate available N from source tissues to sink tissues, such as young leaves (Masclaux-Daubresse et al 2010) and developing grains, accounting for 60–92% of total grain N (Barbottin et al 2005). The glutamine synthetase–glutamate synthase (GS-GOGAT) cycle plays an important role in this process since it recycles N liberated from the catabolism of N-rich macromolecules, such as protein and nucleic acids, into lowmolecular-weight organic compounds for long-distance N transport (Lea and Miflin 2010). Purines are the most abundant N heterocyclic compounds in nature and are found in nucleic acids (DNA, RNA) and many other cellular components, such as ATP, GTP or NADH (Werner and Witte 2011). Ureidoglycolate amidohydrolase (UAH) converts ureidoglycolate to hydroxyglycine and, lastly, hydroxyglycine decays to glyoxylate by a nonenzymatic reaction (Werner et al 2010)
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