Review: Mechanisms of ammonium toxicity and the quest for tolerance

Abstract

Ammonium sensitivity of plants is a worldwide problem, constraining crop production. Prolonged application of ammonium as the sole nitrogen source may result in physiological and morphological disorders that lead to decreased plant growth and toxicity. The main causes of ammonium toxicity/tolerance described until now include high ammonium assimilation by plants and/or low sensitivity to external pH acidification. The various ammonium transport-related components, especially the non-electrogenic influx of NH3 (related to the depletion of (15)N) and the electrogenic influx of NH4(+), may contribute to ammonium accumulation, and therefore to NH3 toxicity. However, this accumulation may be influenced by increasing K(+) concentration in the root medium. Recently, new insights have been provided by "omics" studies, leading to a suggested involvement of GDP mannose-pyrophosphorylase in the response pathways of NH4(+) stress. In this review, we highlight the cross-talk signaling between nitrate, auxins and NO, and the importance of the connection of the plants' urea cycle to metabolism of polyamines. Overall, the tolerance and amelioration of ammonium toxicity are outlined to improve the yield of ammonium-grown plants. This review identifies future directions of research, focusing on the putative importance of aquaporins in ammonium influx, and on genes involved in ammonium sensitivity and tolerance.

Time-Course of Metabolic and Proteomic Responses to Different Nitrate/Ammonium Availabilities in Roots and Leaves of Maize

“…Finally, the concomitant increases of the triose phosphate/phosphate translocator (L212), which mediates the export of fixed carbon from chloroplast to cytosol [40], of two nucleoside diphosphate kinases (L130 and L236), cytosolic enzymes involved in balancing between the pools of ATP and the nucleosides [41], as well as of two glycolytic enzymes (L192 and L191) and of the mitochondrial malate dehydrogenase (L110) suggested a general upsurge in energy production and in respiratory metabolism (Table 4, Figure 5). On the whole, considering that in plants the maintenance of low levels of NH 4 + in tissues is one of the main strategies to avoid metabolic stresses [11], it is possible to propose that, at 54 h, the NH 4 + accumulation in leaves led to an increment of the photosynthetic machinery and of C metabolism to sustain the synthesis of amino acids. In this regard, the high content of reducing sugars in the roots of the (a) plants at 54 h could indicate that a massive allocation of photoassimilates in this organ occurred when NH 4 + was provided as the sole N nutrient (Figure 3C).…”

“…Considering that both protein families are involved in the NH 4 +/ NH 3 transport [11], it is possible to conceive some relationship between their induction by NO 3 − and the highest NH 4 + content in roots in co-provision (Figure 2D).…”

“…Considering the theoretical metabolic costs [8] and the demand for reducing equivalents [9], the use of NH 4 + by plants seems to be advantageous compared to that of NO 3 − , but this prediction does not often coincide with empirical observations [3]. An exclusive, or excessive, NH 4 + nutrition could have adverse impacts on plants, including alterations in root metabolism, plant ionic imbalances, and foliar oxidative stress [10,11]. Plant responses also significantly depend on the relative proportion between the NH 4 + and the NO 3 − available in the soil.…”

“…Overall, these interactions improve the capabilities of the plants for N acquisition and assimilation [13]. Large-scale approaches have turned out to be very useful to investigate the complexity of N nutrition in plants, as proven by many transcriptomic studies conducted in Arabidopsis thaliana [11,14]. However, several aspects have yet to be fully elucidated, such as the interactions and communications between NO 3 − and NH 4 + and between roots and leaves.…”

Densely rooted rhizosphere hotspots induced around subsurface NH4 +-fertilizer depots: a home for soil PGPMs?

“…In contrast to plant and animal cells, bacteria preferentially use NH 4 + as a source of N and can be tolerant even to molar concentrations of NH 4 -N, at which point growth limiting effects may be related more to osmotic or ionic imbalances than to direct toxic effects of NH 4 + ions per se [38]. The threshold concentration range of 50-250 mM NH 4 -N at which cultured PGPMs showed that inhibited growth is above the range for NH 4 + toxicity in sensitive crop species like barley (Hordeum vulgare L.) and tolerant ones like rice (Oryza sativa L.) grown hydroponically [39][40][41]. The NH 4 + tolerance threshold for our tested PGPMs (50-250 mM NH 4 -N) is also above the range of 2-20 mM that can be common in soil solution of most agricultural soils [42].…”