Research paperDrought stress obliterates the preference for ammonium as an N source in the C4 plant Spartina alterniflora
Introduction
Under natural conditions of growth and development, plants are inevitably exposed to multiple stresses, such as drought, salinity, flooding, mineral deficiencies, and toxicity (Ben Hamed et al., 2013). Of these, drought is considered one of the most formidable challenges to agricultural productivity (Mahajan and Tuteja, 2005, Hessini et al., 2008, Hessini et al., 2009b), and the greatest losses in productivity occur in arid and semiarid regions, where, in addition to scarcity, the quality of irrigation water is often low (Fernández-Cirelli et al., 2009).
Drought inhibits plant growth by disturbing the uptake of ions and water, impeding N-metabolism, and causing oxidative stress (Gonzalez et al., 1998, Bhargava and Sawant, 2013). The extent of damage depends on plant genotype, the severity of the stress, and the type, quantity, and regime of fertilization (Hessini et al., 2009a, Waraich et al., 2011, Waraich et al., 2012). The use of fertilizer to enhance crop productivity has increased five-fold since the 1960s, and about 65% of it is used on cereals. However, inadequate or inefficient fertilization perturbs plant growth and contributes to soil degradation (Humbert et al., 2013), and it is predicted that access to fertilization will be one of the main challenges for crop production in drought-prone areas (Shiferaw et al., 2014).
Nitrogen (N), the most important macronutrient obtained by plant roots, is deficient in most soils, and in particular those in arid and semiarid regions (Hernández et al., 1997). It is critical to all principal metabolic processes, including those related to osmotic adjustment, and constitutes almost 80% of the total nutrients absorbed by plant roots (Marschner, 1995). Plants take up N mainly in two forms: nitrate (NO3−) and ammonium (NH4+), or as mixtures of the two. Great differences exist between species in their preference for the sources of N, with most species growing best on either NO3− or a mixed N source (Kronzucker et al., 1999), while only few perform best on NH4+ (Kronzucker et al., 1997, Britto and Kronzucker, 2002, Britto and Kronzucker, 2013).
Plant response to N fertilization under drought conditions varies with plant species, climate, N source, and fertilization regime (Waraich et al., 2011). Nitrate may not always be beneficial under drought, as it can accumulate in plant leaves without contributing to biomass or to increasing yield (Martinoia et al., 1981, Bernguer et al., 2009). However, the NO3− ion can also serve as an electron sink and potentially alleviate photosystem stress under water limitation conditions (Yi et al., 2014). Plants with high tissue NO3− levels also lose nutritional value because, when consumed in excess, NO3− can be harmful for human and livestock health (Britto and Kronzucker, 2002, Hessini et al., 2009b). Thus, there is interest in identification and development of drought-tolerant plant genotypes able to utilize NH4+ as their principal N source. Indeed, the addition of NH4+ to the nutrient solution has been reported to mitigate the adverse effects of drought on growth and development of rice (Gao et al., 2010). NH4+ has also been reported to mitigate the effects of salt stress on Hordeum vulgare, Citrange carrizo, and Spartina alterniflora (Kant et al., 2007, Fernández-Crespo et al., 2012, Hessini et al., 2013), although others have observed the opposite effect, as, for instance, in pea (Speer et al., 1994, Speer and Kaiser, 1994).
Although the mechanism by which NH4+ may enhance plant tolerance to osmotic stress is not clear, several authors consider it a result of: (i) NH4+ assimilation carrying a lower energy cost than that of NO3− (Kant et al., 2007); (ii) increased plant water absorption (Gao et al., 2010); (iii) the activation of antioxidant enzymes responsible for some mechanisms of early acclimation to stress (Misra and Gupta, 2006, Fernández-Crespo et al., 2012).
Spartina alterniflora is an interesting test species due to its C4 photosynthetic habit and high tolerance for environmental stresses. Due to these characteristics, Spartina is sometimes an invasive species that can disturb natural ecosystems. In this study, we explore the mechanism for drought tolerance in this species and report the effects of ammonium nutrition on the species in the light of the responsiveness of its antioxidant systems and shifts in N metabolism that may be required for acquisition of drought tolerance.
Section snippets
Plant material and propagation
The plants used in this experiment were obtained from 25-cm-high cuttings transplanted into 4-L blow-moulded pots (one cutting per pot) filled with sandy soil and irrigated with Hewitt (1966) nutrient solution for one month under well-watered conditions, in a greenhouse with an average air temperature of 25/18 °C day/-night, an air relative humidity ranging between 65 and 90%, an average irradiance at mid-day of ∼900/1800 μmol m−2 s−1 PAR, and a natural photoperiod of 12–15 h. In order to prevent
Growth
Under well-watered conditions (100% FC), plant biomass accrual responded strongly to the N source present in the root medium. The biomass of NO3−-fed plants was only half that of those fed with NH4+, while NH4NO3-fed plants had intermediate biomass (Fig. 1). Under drought conditions (soil moisture 50 or 25% FC), plant biomass accumulation became similar on all three N-source treatments, and at 50% FC no significant differences from control, NO3−-fed, plants were observed.
The effect of drought
Discussion
Drought is a major stress factor for most plants, even for C4 species, which have a water-use efficiency significantly superior to that of C3 plants under arid conditions, being able to maintain stomatal closure when water availability is low (Sage, 2004, Osborne and Beerling, 2006). S. alterniflora, a C4 grass, is able to thrive on, acclimate to, and tolerate salinity stress well (Hessini et al., 2013). It is also unique in that it grows best on NH4+ as an N source, rather than nitrate or
Conclusion
Although Spartina alterniflora is able to thrive on, acclimate to, and tolerate both ammonium and salinity stresses, it is unable to tolerate drought, even when provided with its preferred N form, NH4+. Indeed, in contrast to performance under salt stress, drought imposition completely nullifies any of the growth advantages observed in this C4 grass under normal conditions when provided with NH4+ as an N source. The sensitivity of the species to drought is in part due to low constitutive levels
Author contributions
HK and CC carried out experimental and analysis work.
HK, CC and AC: design and interpretation of all experiments.
HK and KHJ wrote the manuscript.
Acknowledgements
This work was supported by the Tunisian Ministry of Higher Education and Scientific Research (LR10CBBC02). Special thanks to Dr. Stephen Houghton for improving the English of the manuscript.
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