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Front. Plant Sci. | doi: 10.3389/fpls.2019.01103

Can ammonium stress be positive for plant performance?

  • 1University of the Basque Country, Spain
  • 2IKERBASQUE Basque Foundation for Science, Spain
  • 3Institute for Multidisciplinary Applied Biology Research, Public University of Navarre, Spain

Ammonium (NH4+) nutrition is considered as a universal stressful situation, virtually affecting every plant species (recently reviewed in Li et al., 2014; Esteban et al., 2016; Liu and von Wirén 2017). However, the degree of stress it generates is variable and high intra- and inter-specific variability towards ammonium nutrition has been reported. Some species/genotypes display ammonium preference while others show extreme sensitivity when growing with ammonium. Regarding the response of a certain genotype, as for almost every stress, there exists a continuum in the response upon ammonium nutrition, which mostly depends on the concentration of NH4+ in the root medium. Overall, ammonium tolerance could be defined as a situation where the plant is somehow sensing and responding towards ammonium stress prior to suffering a serious damage such as chlorosis or cell death. Regarding biomass, from a farmer’s point of view a moderate reduction in yield, could be compensated with an increase in the resistance of the crop against biotic or abiotic constraints, and also with the obtaining of products of higher quality. Moreover, the use of ammonium-based fertilizers together with inhibitors of nitrification has been extensively shown to mitigate the impact of nitrogen fertilizers on the environment (Sanz-Cobena et al., 2017). Although sophisticated management would be needed, avoiding ammonium stress could be reached by for instance fertigation or frequent additions of small amounts of ammonium-based fertilizers in water delivered through micro-irrigation
Ammonium nutrition may improve the quality of crops
The main cause of ammonium toxicity is probably the over-accumulation of free NH4+ in the cytosol and the problems derived from cell efforts to get rid of it. The cell has several logical strategies to keep NH4+ levels under control 1) NH4+ efflux to the apoplast/rhizosphere, 2) NH4+ storage in the vacuole and 3) NH4+ assimilation into organic compounds.
In line with the third strategy to avoid excessive cytosolic NH4+ accumulation, the induction of the synthesis of N-reduced compounds is a classical plant response to ammonium nutrition and indeed, the accumulation of total free amino acids can be considered as a marker of ammonium stress (Sarasketa et al., 2014). In general terms, crops quality is associated to the protein content of food products, notably in grains, which is dependent on the crops capacity to efficiently use the available nitrogen. In addition, the nutritional value and/or quality of food is associated with its content in minerals, and in health-promoting secondary metabolites such as antioxidants. In this line of evidence, several works have reported an improvement of the nutritional quality of a number of crops when they are grown under ammonium nutrition. A higher protein accumulation is common in plants grown with NH4+ supply and for instance a positive effect of ammonium nutrition respect to nitrate (NO3-) was reported in the protein content of wheat grain and in gliadins/glutenins ratio, overall increasing wheat bread-making quality (Fuertes-Mendizabal et al., 2013).
In Brassicaceae, glucosinolates (GLS) represent an abundant family of secondary metabolites derived from amino acids. GLS degradation products participate in cruciferous plants defense against herbivores. Moreover they are responsible of the characteristic flavor of the cruciferous vegetables. Importantly, certain GLS breakdown products possess health protective capacities, particularly anti-carcinogenic activity and hence, GLS content is associated with cruciferous nutritional quality. Currently, big efforts are dedicated to manipulate GLS levels in order to produce new and improved commercial cruciferous crop varieties (Traka et al., 2013). Regarding ammonium-based nutrition, recent studies have reported that the synthesis of GLS is stimulated in leaves of plants grown with NH4+ as N source, such as in broccoli, oilseed rape and Chinese kale (Coleto et al., 2017; Marino et al., 2016; La et al 2013). Notably, glucoraphanin content, whose degradation yields sulphoraphane, the most promising and characterized anticancer isothyocianate, increased in ammonium-fed broccoli and oilseed rape (Coleto et al., 2017; Marino et al., 2016). Whether GLS accumulation is just a consequence of ammonium assimilation increase or whether they possess a regulatory role during ammonium stress is a question for further elucidation.
Another aspect of crops quality is the control of NO3- accumulation in plant edible parts, notably in leafy vegetables such as spinach or lettuce. This is a subject of concern because it can turn to nitric compounds, which have been linked to increased risk of cancer and methemoglobinemia (Umar and Iqbal, 2007). Accordingly, growing plants with increased amounts of ammonium NH4+ respect to NO3- clearly reduces the quantity of NO3- accumulated in plant tissues and thus its associated risks (Irigoyen et al., 2006; Santamaria et al., 2001).
Ammonium nutrition may protect plants from pathogen attack
Nitrogen metabolism is closely connected to plant immunity. Among others, it provides the necessary building blocks to synthesize most of the defence-related secondary-metabolites and is central for NO production whose role in plant-pathogen interaction has been widely reported (Santana et al., 2017). Nitrogen source has been shown to have an impact on plant immunity. A number of studies have reported that plants grown with NO3- displayed increased resistance to pathogen attack respect to plants growth with NH4+; for instance, in tobacco exposed to Pseudomonas syringae (Gupta et al., 2013), cucumber infected with Fusarium oxyosporum (Wang et al., 2016) or rice attacked by Rhizoctonia solani (Chi et al., 2019). This higher resistance has been associated with higher NO production in nitrate-fed plants, hormone signaling or decreased citrate exudation, among others (Gupta et al., 2013; Mur et al., 2016; Wang et al., 2016). In contrast, several works have reported increased resistance in ammonium-fed plants such as tomato exposed to P. syringae (Fernández-Crespo et al., 2015) or to F. oxyosporum (López-Berges et al., 2010), and to potato facing Verticillium wilt (Huber, 1989). In this case, the beneficial priming effect of NH4+ has been related to an increased reactive oxygen species burst and polyamine synthesis in ammonium-fed plants (Fernández-Crespo et al., 2015). Moreover, transcriptomic analyses have reported that ammonium induces the up-regulation of genes associated with plant defense and immunity (Patterson et al., 2010; Vega-Mas et al., 2018). Interestingly, the overexpression of rice ammonium transporter AMT1;2 conferred resistance against R. solani (Chi et al., 2019). In contrast, Arabidopsis amt1.1 knockout mutant exhibited less disease symptoms that wild type plants infected with P. syringae and Plectosphaerella cucumerina (Pastor et al., 2014).
In another line of evidence the above reported increase in GLS synthesis might be also increasing the resistance of cruciferous plants notably against herbivores (Marino et al., 2015). Similarly, the stimulation of the synthesis of γ-aminobutyric acid (GABA) is also frequent under ammonium nutrition, for instance in tobacco plants (Gupta et al., 2013). GABA is a signal molecule common to animals and plants. Its accumulation reveals a stress-specific pattern consistent with a physiological response leading to stress mitigation and is also involved in plant response to pathogens (Kinnersley and Turano, 2000; Bown and Shelp, 2016). GABA accumulation appeared detrimental for plant defence (Gupta et al., 2013); nevertheless further experimentation is needed to fully decipher the role of GABA in the connection between N-source use and plant immunity. Overall, the interaction between NH4+ and plant defence is clear but the potential benefit of ammonium stress would be dependent of the plant pathosystem and therefore, no general rule can be drawn.
Ammonium nutrition may improve the cross-tolerance to other abiotic stresses
A number of the responses that ammonium nutrition may trigger are defensive mechanisms that are common to different abiotic stress situations. Interestingly, the onset of these mechanisms may prevent damage from other simultaneous or subsequent stresses. Salinity is one of the most detrimental abiotic stresses and the type of N nutrition differentially affects plants living under high salt contents. For example, the C4 halophyte Spartina alternatiflora displayed improved performance when grown with NH4+ as N source and NH4+ benefits were associated with higher antioxidant enzyme activities (Hessini et al 2013). Intriguingly, although antioxidant machinery induction was higher, S. alternatiflora ammonium preference was lost under drought (Hessini et al., 2017). While S. alternatiflora is a highly tolerant plant to ammonium nutrition, similar positive effects can be observed in other species. For instance, in the citrus citrange Carrizo, ammonium nutrition promoted its resistance to salinity conditions inducing, among other responses, lower Cl- uptake. The mechanisms of action again showed that plant antioxidant machinery, notably glutathione metabolism, was part of a common ammonium-response that primed resistance to subsequent salt stress (Fernandez-Crespo et al., 2014). Similarly, NH4+-induced cross-acclimation to salinity stress has also been reported in Sorghum bicolor (de Souza Miranda et al., 2017). . Ammonium nutrition improved K+/Na+ homeostasis notably by reducing Na+ loading into the xylem in agreement with the observed higher proton pumps and SOS1 Na+/H+ antiporters activity (Salt Overlay Sensitive 1). In general, NH4+ acted as an efficient signal to activate responses involved in the regulation of Na+ homeostasis leading to salt tolerance in sorghum plants (de Souza Miranda et al., 2017). More recently, the benefit of NH4+ as primer of resistance to salinity has also been reported in maize (Hessini et al., 2019).
Previous ammonium nutrition has also been shown to ameliorate water stress resistance. Thus, Gao et al (2010) showed important fresh weight increase in rice plants under PEG-induced water stress when ammonium nutrition was the source of N, while either nitrate or mixed sources significantly decreased fresh weight under water stress. This effect was suggested to be related to higher aquaporins activity, which takes place in ammonium grown plants independently of the water stress, and which relates to a better usage of water under NH4 + nutrition (Gao et al., 2010). Similarly, the alleviation of PEG-induced water stress in ammonium-fed rice seedlings has been related with sustained NH4+ uptake and assimilation (Cao et al., 2018). Indeed, it has been suggested that increasing nitrogen uptake and assimilation, among others in tomato (Sánchez-Rodriguez et al., 2011) and in Malus prunifolia (Huang et al., 2018) could increase the cell osmotic adjustment capacity to protect plants against water stress.
Ammonium nutrition has also been talked about in relation to its interaction with plants response to elevated atmospheric CO2 due to the hypothesis of Bloom et al., (2010) stating that C3 plants respond more positively to elevated CO2 under ammonium nutrition than under nitrate nutrition. It is suggested that elevated CO2 inhibits the plant photo-reduction of NO3− and consequently reduces total plant N assimilation and growth (Rubio-Asensio and Bloom, 2017). However, this hypothesis is today under great debate and a number of works do not support it (Vega-Mas et al., 2015; Andrews et al., 2018). On the whole, the magnitude of the challenge that climate change adaptation implies for agriculture deserves further research to discard or confirm the potential benefit of ammonium nutrition for plants performance.
Beyond drought and salinity, ammonium nutrition has also been suggested to contribute to other stressful situation such as to the tolerance of cucumber to phenantrene, a persistent polycyclic aromatic hydrocarbon commonly found in soil and sediments, again in relation with increased activity of antioxidative enzymes (Yang et al., 2012). Furthermore, ammonium nutrition has been shown to increment rice tolerance to Fe-deficiency through enhanced remobilization of Fe from root cell walls (Zhu et al., 2018).
Concluding remarks and future perspectives
In this article, we propose a change of paradigm where ammonium nutrition may be considered not exclusively as an undesirable situation for plant performance, but as a way to provoke changes in plant metabolism that can be beneficial for crops quality and plant physiology. While some of the positive effects of ammonium referred here still require further evaluation, the cross-tolerance induction of NH4+ to certain subsequent stresses, notably salinity, is clear. However, the molecular actors governing these interactions are almost completely unknown and future works will be essential in order to fully exploit the benefits of ammonium-based fertilizers.

Keywords: abiotic stress, ammonium, Climate chage, Crop nutritional quality, nitrate, nitrogen metabolism, Plant-pathogen interaction

Received: 25 Apr 2019; Accepted: 12 Aug 2019.

Copyright: © 2019 Marino and Moran. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence:
Dr. Daniel Marino, University of the Basque Country, Bilbao, Spain,
Dr. Jose F. Moran, Institute for Multidisciplinary Applied Biology Research, Public University of Navarre, Pamplona, Navarre, Spain,