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  Section: Molecular Biology of Plant Pathways » Metabolic Organization in Plants
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Impact of Metabolic Change on Network Structure


Finally, although most efforts to manipulate metabolism focus on the immediate metabolic effects of adjusting the amount of a specific enzyme, there is appreciable evidence that altering the amount of an enzyme can also influence metabolism through its impact on network structure brought about via metabolite signaling or perturbation of nutritional status. The complexity of the physiological and metabolic responses brought about by regulation at this level is highlighted in a study that examined the relationship between photosynthesis, nitrogen assimilation, and secondary metabolism (Matt et al., 2002). This investigation showed that inhibition of photosynthesis by decreasing Rubisco led to a preferential decrease in the amounts of amino acids relative to sugars, a disproportionate decline in the absolute levels of secondary metabolites, and a shift in the proportions of carbon- and nitrogen-rich secondary metabolites. Many of these effects were most apparent in plants grown in high nitrate. Under these conditions, the fall in amino acid levels despite the availability of nitrate can be explained, at least in part, by a reduction in nitrate reductase activity occurring as a consequence of a decrease in the levels of sugars that are required to maintain expression of the genes encoding nitrate reductase and to promote posttranslational activation of the enzyme (Klein et al., 2000). In turn, the reported decrease in chlorogenic acid was probably a direct consequence of low levels of phenylalanine restricting flux into phenylpropanoid metabolism, while the decrease in nicotine was presumably related to the general inhibition of primary nitrogen metabolism and associated decreases in amino acids. The disproportionately large decrease in amino acid levels in the lines in which Rubisco expression was suppressedmay also provide the explanation for the seemingly counterintuitive observation that accumulation of nitrogen-rich nicotine was preferentially inhibited relative to carbon-rich chlorogenic acid when photosynthetic carbon assimilation was inhibited under nitrogen-replete conditions (Matt et al., 2002).

Analysis of the response of nitrogen metabolism and the consequential changes in secondary metabolism to decreased photosynthesis in plants grown under conditions of low nitrogen availability revealed a further layer of complexity. Many of the effects seen in high nitrate were obscured under limiting nitrogen conditions. The likely explanation for this is that because of lower rates of photosynthesis, and hence a decreased requirement for organic nitrogen, the Rubisco antisense lines were less nitrogen-limited
than wild-type plants when grown in low nitrogen. This indirect amelioration of nitrogen deficiency masked the direct inhibitory effects of low Rubisco activity on nitrogen assimilation. Thus, wild-type tobacco grown on low nitrogen had low levels of nitrate and glutamine, and a low glutamine:glutamate ratio typical for nitrogen-limited plants, whereas the plants with decreased Rubisco had increased nitrate and glutamine and a higher glutamine: glutamate ratio. As a result of these differences, the decrease in nicotine accumulation in the transgenic lines relative to wild type observed under nitrogen-replete conditions was diminished or even reversed in low nitrogen fertilizer (Matt et al., 2002). Such considerations provide a compelling reminder of the difficulties in interpretation of metabolic comparisons between plant lines even under seemingly carefully defined growth conditions and of the danger in ascribing a metabolic change to a single direct effect.

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