Ureide metabolism in plant-associated bacteria: purine plant-bacteria interactive scenarios under nitrogen deficiency

Abstract

The erratic alterations in climate being experienced in agriculture, such as extended periods of drought or heavy rainfalls, are bringing increasing concerns about nitrogen (N) management. Even in high-input farming systems, unpredictable weather patterns can cause N deficiencies and result in nutrient losses that contribute to major pollution issues in groundwater, lakes, and even the oceans. Our present understanding of the beneficial interactions between N-deficient-challenged plants and plant-associated bacteria (PAB), mainly of the phyla Actinobacteria, Bacteroidetes, Firmicutes, and Proteobacteria, is largely based on studies performed at the level of whole-plant fitness and impacts of crop yields via the abilities of bacteria to synthesize indole acetic acid and/or produce the enzyme 1-aminocyclopropane-1-carboxylate deaminase which reduces endogenous ethylene levels. Much less is known about the complex interaction that occur from the PAB’s abilities to produce N ureide (allantoin and allantoate) and how these purine intermediaries function as an N source and prime stress signals for the growth of both partners. This review examines the noteworthy progress made on understanding the bacterial ureide pathway with the aim to elaborate possible scenarios to unravel the complex nature of PAB-plant interactions at the purine level. Tables with updated information on PAB growth-promoting activities, N metabolism, and abilities to hydrolyze purine intermediates as well as allantoin for colony growth are included. As in plants, the metabolism of ureides in PAB covers the pathways from the deamination of the nucleobase guanine up to its conversion into glyoxylate, NH4+, and/or NH3 to recycle C and N. More important, in PAB, the full set of riboswitch-modulated genes encoding the enzymes involved in the synthesis and catabolism of ureides, as well as purine transporters, is expressed primarily under stressful conditions leading to N deficiency. Thus, PAB might act as a stress-induced source of purines for the plant N metabolism, or could become scavengers of the plant-synthesized purines for colony replication. Consumption of purine intermediaries or ureides by PAB may hinder the symbiotic efficiency of rhizobia-nodulated N2-fixing legumes. The impact of soil xanthine, hypoxanthine, and allantoin pools on the plants or PAB ureide synthesis is also discussed. Given widespread concerns for crop losses due to the drastically changing climate and prevailing agricultural practices, the understanding of the interactive signaling for the purine metabolisms between PAB and plants takes on a major importance, as it may support management decisions necessary to maintain PAB biodiversity and the agricultural services provided by PAB to crops.