Drought stress obliterates the preference for ammonium as an N source in the C4 plant Spartina alterniflora

Abstract

The C4 grass Spartina alterniflora is known for its unique salt tolerance and strong preference for ammonium (NH4+) as a nitrogen (N) source. We here examined whether Spartina’s unique preference for NH4+ results in improved performance under drought stress. Manipulative greenhouse experiments were carried out to measure the effects of variable water availability and inorganic N sources on plant performance (growth, photosynthesis, antioxidant, and N metabolism). Drought strongly reduced leaf number and area, plant fresh and dry weight, and photosynthetic activity on all N sources, but the reduction was most pronounced on NH4+. Indeed, the growth advantage seen on NH4+ in the absence of drought, producing nearly double the biomass compared to growth on NO3−, was entirely obliterated under both intermediate and severe drought conditions (50 and 25% field capacity, respectively). Both fresh and dry weight became indistinguishable among N sources under drought. Major markers of the antioxidant capacity of the plant, the activities of the enzymes superoxide dismutase, catalase, ascorbate peroxidase, and glutathione reductase, showed higher constitutive levels on NH4+. Catalase and glutathione reductase were specifically upregulated in NH4+-fed plants with increasing drought stress. This upregulation, however, failed to protect the plants from drought stress. Nitrogen metabolism was characterized by lower constitutive levels of glutamine synthetase in NH4+-fed plants, and a rise in glutamate dehydrogenase (GDH) activity under drought, accompanied by elevated proline levels in leaves. Our results support postulates on the important role of GDH induction, and its involvement in the synthesis of compatible solutes, under abiotic stress. We show that, despite this metabolic shift, S. alterniflora’s sensitivity to drought does not benefit from growth on NH4+ and that the imposition of drought stress equalizes all N-source-related growth differences observed under non-drought conditions.