All of the nitrogen in a plant, whether derived initially from nitrate, nitrogen fixation, or ammonium ions, is converted to ammonia, which is rapidly incorporated into organic compounds through a number of metabolic pathways beginning with the activity of the enzyme glutamine synthetase (GS), which catalyzes formation of the amino acid glutamine from ammonia and glutamic acid.
An individual nitrogen atom may pass many times through the GS reaction, following uptake from the soil, assimilation, remobilization, and delivery to growing roots and leaves, and ultimately, deposition in seed as storage proteins. Thus GS is likely to be a major check-point controlling plant growth and crop productivity.
In research reported in The Plant Cell, scientists Antoine Martin and Bertrand Hirel from the National Institute of Agronomic Research (INRA) in Versailles, France, together with colleagues from institutions in the U.K., Spain, and Japan, present new information on the roles of two forms (isoenzymes) of cytosolic glutamine synthetase (GS) in maize, which underscores the importance of this enzyme and nitrogen metabolism in cereal crop productivity. Improving nitrogen use efficiency of crop plants, i.e. reducing the amount of costly nitrogen fertilizer inputs that farmers need to apply to crops while at the same time maintaining and even improving yields, is an important goal in crop research. As noted by Dr. Hirel, “a more complete understanding of the roles of GS enzymes in nitrogen metabolism and grain yield in maize and other crop plants (including rice, wheat and barley) may lead to improvements in fertilizer usage and crop yield, thus mitigating the detrimental effects of the overuse of fertilizers on the environment“.
The roles of these two GS isoenzymes, products of the Gln1-3 and Gln1-4 genes, were investigated by examining the impact of knock-out mutations on kernel yield. GS gene expression was impaired in the mutants, resulting in reduced levels of GS1 protein and activity. The gln1-4 phenotype displayed reduced kernel size whereas gln1-3 had reduced kernel number, and both phenotypes were evident in the gln1-3 gln1-4 double mutant. Shoot biomass production at maturity was not affected in either the single mutants or double mutants, suggesting that both gene products play a specific role in grain production. Levels of asparagine increased in the leaves of the mutants during grain filling, most likely as a mechanism for circumventing toxic ammonium buildup resulting from abnormally low GS1 activity. Phloem sap analysis revealed that, unlike glutamine, asparagine is not efficiently transported to developing maize kernels, which could account for the reduced kernel production in the mutants. Constitutive overexpression of Gln1-3 in maize leaves resulted in a 30% increase in kernel number relative to wild type, providing further evidence that GS1 plays a major role in kernel yield.
Some of the major cereals, such as maize, sorghum, and sugar cane, exhibit C4 photosynthesis, which enhances the efficiency of photosynthesis at high temperature (most C4 plants originated in tropical climates). In standard C3 photosynthesis (present in rice, wheat, and most temperate crop plants), CO2 entering the leaf is converted to a 3-carbon compound via the C3 pathway, utilizing energy derived from the light reactions of photosynthesis. In plants that have C4 photosynthesis, the C3 pathway enzymes are localized in specialized “bundle sheath” cells which surround the vascular tissue in the interior of the leaf. CO2 entering mesophyll cells at the leaf surface initially is converted to a 4-carbon compound, which is shuttled into the bundle sheath cells and then decarboxylated to release CO¬2. CO2 released into bundle sheath cells then enters the standard C3 pathway. This CO2-concentrating mechanism allows plants in a hot and dry climate to take up CO2 at night and store it, and release it again inside bundle sheath cells during the day, thus solving the problem of how to maintain a high concentration of CO2 inside the leaf during the daylight hours, when stomata often must be kept closed to prevent water loss. Using cytoimmunochemistry and in situ hybridization, Martin et al. found that GS1-3 is present in maize mesophyll cells whereas GS1-4 is specifically localized in the bundle sheath cells. Thus the two GS1 isoenzymes play non-redundant roles with respect to their tissue-specific localization, and the activity of both is required for optimal grain yield. This work illustrates the close coordination between nitrogen and carbon metabolism in photosynthetic tissues, and reveals that nitrogen metabolism plays a critical role in optimizing grain yields.
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