Is plastidic glutamine synthetase essential for C₃ plants? A tale of photorespiratory mutants, ammonium tolerance and conifers

Abstract

Summary Agriculture faces the considerable challenge of having to adapt to a progressively changing climate (including the increase in CO2 levels and temperatures); environmental impact must be reduced while at the same time crop yields need to be maintained or increased to ensure food security. Under this scenario, increasing plants’ nitrogen (N) use efficiency and minimizing the energy losses associated with photorespiration are two goals of crop breeding that are long sought after. The plastidic glutamine synthetase (GS2) enzyme stands at the crossroads of N assimilation and photorespiration, and is therefore a key candidate for the improvement of crop performance. The GS2 enzyme has long been considered essential for angiosperm survival under photorespiratory conditions. Surprisingly, in Arabidopsis GS2 is not essential for plant survival, and its absence confers tolerance towards ammonium stress, which is in conflict with the idea that NH4+ accumulation is one of the main causes of ammonium stress. Altogether, it appears that the ‘textbook’ view of this enzyme must be revisited, especially regarding the degree to which it is essential for plant growth under photorespiratory conditions, and the role of NH4+ assimilation during ammonium stress. In this article we open the debate on whether more or less GS2 is a desirable trait for plant productivity.

The carbon-concentrating mechanism of the extremophilic red microalga Cyanidioschyzon merolae

“…C. merolae has homologs to the nine enzymes of the A. thaliana photorespiratory pathway and to A. thaliana catalase, which detoxifies hydrogen peroxide produced by the photorespiratory pathway (Rademacher et al 2016 ). Though C. merolae does not have close homologs to the plastidic dicarboxylate transporters which function in photorespiratory nitrogen recycling in plants, this may be explained by some flexibility in the localization of photorespiratory nitrogen metabolism across organisms, like the flexible localization observed for ammonium assimilation in seed plants (Barbier et al 2005 ; Marino et al 2022 ). Overall, rubisco oxygenation is present in all studied oxygenic photosynthetic organisms, and there are likely evolutionary barriers to eliminating this process (Moroney et al 2013 ).…”

Effects of Biological Nitrogen Metabolism on Glufosinate-Susceptible and -Resistant Goosegrass (Eleusine indica L.)

“…The glutamine synthetase/[glutamate synthetase (glutamate 2-oxoglutarate aminotransferase), EC 1.4.1.13 and 1.4.1.14] (GS/GOGAT) cycle is the pathway responsible for the incorporation of inorganic nitrogen (N) into organic molecules. For example, GS2 is involved in the nitrogen deficiency of rice and ammonium tolerance in C 3 plants [ 17 , 18 , 19 ]. Meanwhile, the minor pathway of glutamate dehydrogenase (GDH, EC 1.4.1.3) links the carbon and nitrogen metabolisms as another way to assimilate ammonia into glutamate or deaminate glutamate into 2-oxoglutarate and ammonia, requiring NADPH [ 17 ].…”

The Association of Grain Yield and Agronomical Traits with Genes of Plant Height, Photoperiod Sensitivity and Plastid Glutamine Synthetase in Winter Bread Wheat (Triticum aestivum L.) Collection

“…The GS2 enzyme was shown to be essential for plant survival under photorespiration conditions. During photorespiration, the ammonium is released, while GS2 traps it and incorporates in glutamine, preventing its toxicity and depletion of organic nitrogen in the plant organism [ 31 ]. Increased plastid GS expression was shown to be favorable for plant growth and yield as it improves, among other traits, the nitrogen use efficiency.…”

“…Increased plastid GS expression was shown to be favorable for plant growth and yield as it improves, among other traits, the nitrogen use efficiency. The lines overexpressing GS2 were shown to be more tolerant to abiotic stresses such as drought or soil salinity, as higher GS activity favors the synthesis of osmolytes such as proline or polyamines [ 31 ]. Moreover, plants overexpressing GS2 showed increased tolerance to high-intensity light [ 32 ].…”