RNA Catabolites Contribute to the Nitrogen Pool and Support Growth Recovery of Wheat

Abstract

Turn-over of RNA and catabolism of nucleotides releases one to four ammonia molecules; the released nutrients being reassimilated into primary metabolism. Preliminary evidence indicates that monocots store high levels of free nucleotides and nucleosides but their potential as a source of internal organic nitrogen for use and remobilization is uncharted. Early tillering wheat plants were therefore starved of N over a 5-day time-course with examination of nucleic acid yields in whole shoots, young and old leaves and roots. Nucleic acids constituted ∼4% of the total N pool of N starved wheat plants, which was comparable with the N available from nitrate (NO3-) and greater than that available from the sum of 20 proteinogenic amino acids. Methods were optimized to detect nucleotide (purine and pyrimidine) metabolites, and wheat orthologs of RNA degradation (TaRNS), nucleoside transport (TaENT1, TaENT3) and salvage (TaADK) were identified. It was found that N starved wheat roots actively catabolised RNA and specific purines but accumulated pyrimidines. Reduced levels of RNA corresponded with induction of TaRNS2, TaENT1, TaENT3, and TaADK in the roots. Reduced levels of GMP, guanine, xanthine, allantoin, allantoate and glyoxylate in N starved roots correlated with accumulation of allantoate and glyoxylate in the oldest leaf, suggesting translocation of allantoin. Furthermore, N starved wheat plants exogenously supplied with N in the form of purine catabolites grew and photosynthesized as well as those plants re-supplied with NO3-. These results support the hypothesis that the nitrogen and carbon recovered from purine metabolism can support wheat growth.

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 ).…”

“…Regulation of these processes may prevent loss of N as NH 3 gas when carbon skeletons are in short supply. In contrast, under low N conditions, allantoin is catabolized ( Melino et al , 2018 ) and recycled to NH 3 which can be reduced by N-assimilatory enzymes or instead serve as a cheap N storage form for translocation to the grain where it represents a significant portion of the soluble N pool ( Casartelli et al , 2019 ).…”

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

“…Downstream compounds of the purine catabolic pathway were recently analysed in more detail under N deprivation using the same wheat genotypes, RAC875 and Mace (Melino et al 2018) showing, in addition to reduced levels of allantoin, a significant reduction of allantoate in leaves and an accumulation of glyoxylic acid, the end product of purine degradation. The assumption that the N (and C) 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), although 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 NO 3 − starvation, grew and photosynthesised as well as those re-supplied with NO 3 − (Melino et al 2018). Taken together, 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 NH 4 + and possibly N losses due to volatilization (Fig.…”

Response of Soybean Root to Phosphorus Deficiency under Sucrose Feeding: Insight from Morphological and Metabolome Characterizations

“…Inosine was mapped on the purine metabolism pathway. It is known that nucleotides are composites of macronutrients (P, N, and C); therefore, possibly, the increased inosine in L13 roots is a P starvation response to increase P resources in roots experiencing P deficiency [51]. Most interestingly, the upaccumulation of gibberellin A12 is noteworthy in L13 as compared to T3.…”