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Iron deficiency affects nitrogen metabolism in cucumber (Cucumis sativus L.) plants.

Borlotti A, Vigani G, Zocchi G - BMC Plant Biol. (2012)

Bottom Line: Under Fe deficiency, only nitrate reductase (EC 1.7.1.1) activity decreased both at the root and leaf level, whilst for glutamine synthetase (EC 6.3.1.2) and glutamate synthase (EC 1.4.1.14) an increase was found.Accordingly, the transcript analysis for these enzymes showed the same behaviour except for root nitrate reductase which increased.Furthermore, it was found that amino acid concentration greatly decreased in Fe-deficient roots, whilst it increased in the corresponding leaves.

View Article: PubMed Central - HTML - PubMed

Affiliation: Dipartimento di Scienze Agrarie e Ambientali - Produzione, Territorio, Agroenergia, Università degli Studi di Milano, Milano, Italy.

ABSTRACT

Background: Nitrogen is a principal limiting nutrient in plant growth and development. Among factors that may limit NO3- assimilation, Fe potentially plays a crucial role being a metal cofactor of enzymes of the reductive assimilatory pathway. Very few information is available about the changes of nitrogen metabolism occurring under Fe deficiency in Strategy I plants. The aim of this work was to study how cucumber (Cucumis sativus L.) plants modify their nitrogen metabolism when grown under iron deficiency.

Results: The activity of enzymes involved in the reductive assimilation of nitrate and the reactions that produce the substrates for the ammonium assimilation both at root and at leaf levels in Fe-deficient cucumber plants were investigated. Under Fe deficiency, only nitrate reductase (EC 1.7.1.1) activity decreased both at the root and leaf level, whilst for glutamine synthetase (EC 6.3.1.2) and glutamate synthase (EC 1.4.1.14) an increase was found. Accordingly, the transcript analysis for these enzymes showed the same behaviour except for root nitrate reductase which increased. Furthermore, it was found that amino acid concentration greatly decreased in Fe-deficient roots, whilst it increased in the corresponding leaves. Moreover, amino acids increased in the xylem sap of Fe-deficient plants.

Conclusions: The data obtained in this work provided new insights on the responses of plants to Fe deficiency, suggesting that this nutritional disorder differentially affected N metabolism in root and in leaf. Indeed under Fe deficiency, roots respond more efficiently, sustaining the whole plant by furnishing metabolites (i.e. aa, organic acids) to the leaves.

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Schematic representation of nitrogen metabolism changes occurring in Fe-deficient cucumber plants. Orange arrows indicate the specific process investigate in this work, while the arrow thickness indicates an up- or down-activation of enzymatic activities. Red arrow indicates the possible recycle of protein and aa occurring under Fe deficiency in cucumber plants. Since NO3- assimilation (NR activity) decreases and GS/GOGAT cycle increases in both root and leaf, the source of ammonia might come from a recycling of aa deriving from protein degradation[9]as suggested in ). The aa might be partially translocated to the leaf sustaining its metabolism as supported by data presented in this work (Figures5 and7).
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Figure 8: Schematic representation of nitrogen metabolism changes occurring in Fe-deficient cucumber plants. Orange arrows indicate the specific process investigate in this work, while the arrow thickness indicates an up- or down-activation of enzymatic activities. Red arrow indicates the possible recycle of protein and aa occurring under Fe deficiency in cucumber plants. Since NO3- assimilation (NR activity) decreases and GS/GOGAT cycle increases in both root and leaf, the source of ammonia might come from a recycling of aa deriving from protein degradation[9]as suggested in ). The aa might be partially translocated to the leaf sustaining its metabolism as supported by data presented in this work (Figures5 and7).

Mentions: The general decrease in aa content observed in Fe-deficient roots could be caused by different factors: (i) a major utilization of aa in the protein synthesis, (ii) an increase in their translocation to the leaves and (iii) a degradation and/or recycling of aa. Direct evidence supporting the first hypothesis have been documented in Fe-deficient cucumber root[51]. Concerning the second hypotheses, an increase in the total aa concentration in the xylem sap was observed during the progression of Fe deficiency (this work, Figure6). Considering that the transpiration rate (E) determined did not change during this progression (Figure6 and[52]) it would mean that the aa concentration in the xylem sap increased under Fe deficiency accordingly with the decrease of aa in roots. Concerning the last hypothesis it remains speculative, being supported only by indirect evidence. In this work it was found that the activity of two enzymes involved in the recycling of aa, AST and ALT, increased in roots but not in leaves (Figure7). These data are also supported by proteomic studies conducted on cucumber[9] and Medicago truncatula[11] where the concentration of ALT and AST, respectively, were found to increase under Fe deficiency. Furthermore, a C-N hydrolase family protein has been identified in cucumber roots, and its concentration increased under Fe deficiency[9]. This family of enzymes is involved in N metabolism and catalyses the cleavage of the amino group from C skeletons (amino acid and protein)[53]. Hence, the amino groups released could be re-assimilated throughout the GS/GOGAT cycle into new aa. In Donnini et al.[9] an intriguing hypothesis, albeit speculative, was formulated: some proteins (e.g. actin, tubulin and globulin) might be used as a source of aa, carbon skeletons and N-NH4+ under Fe deficiency. We could hypothesise that in this condition a portion of the newly assimilated N might derive from proteins already present which are sacrificed for the survival of the plant. On the other hand, it appears that plants possess a regulated protein degradation machinery[54] and references therein that are particularly active during the stress response and senescence, leading to a continuous turnover of cellular proteins. As a consequence, the aa released in the roots could, in part, be transported to the leaves to keep N metabolism functioning (Figure8). Indeed, the N assimilation process (i.e. NR plus GS/GOGAT) was affected more in leaves than in roots, and so the increase in aa concentration apparently depends mainly on their translocation from the roots.


Iron deficiency affects nitrogen metabolism in cucumber (Cucumis sativus L.) plants.

Borlotti A, Vigani G, Zocchi G - BMC Plant Biol. (2012)

Schematic representation of nitrogen metabolism changes occurring in Fe-deficient cucumber plants. Orange arrows indicate the specific process investigate in this work, while the arrow thickness indicates an up- or down-activation of enzymatic activities. Red arrow indicates the possible recycle of protein and aa occurring under Fe deficiency in cucumber plants. Since NO3- assimilation (NR activity) decreases and GS/GOGAT cycle increases in both root and leaf, the source of ammonia might come from a recycling of aa deriving from protein degradation[9]as suggested in ). The aa might be partially translocated to the leaf sustaining its metabolism as supported by data presented in this work (Figures5 and7).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3539955&req=5

Figure 8: Schematic representation of nitrogen metabolism changes occurring in Fe-deficient cucumber plants. Orange arrows indicate the specific process investigate in this work, while the arrow thickness indicates an up- or down-activation of enzymatic activities. Red arrow indicates the possible recycle of protein and aa occurring under Fe deficiency in cucumber plants. Since NO3- assimilation (NR activity) decreases and GS/GOGAT cycle increases in both root and leaf, the source of ammonia might come from a recycling of aa deriving from protein degradation[9]as suggested in ). The aa might be partially translocated to the leaf sustaining its metabolism as supported by data presented in this work (Figures5 and7).
Mentions: The general decrease in aa content observed in Fe-deficient roots could be caused by different factors: (i) a major utilization of aa in the protein synthesis, (ii) an increase in their translocation to the leaves and (iii) a degradation and/or recycling of aa. Direct evidence supporting the first hypothesis have been documented in Fe-deficient cucumber root[51]. Concerning the second hypotheses, an increase in the total aa concentration in the xylem sap was observed during the progression of Fe deficiency (this work, Figure6). Considering that the transpiration rate (E) determined did not change during this progression (Figure6 and[52]) it would mean that the aa concentration in the xylem sap increased under Fe deficiency accordingly with the decrease of aa in roots. Concerning the last hypothesis it remains speculative, being supported only by indirect evidence. In this work it was found that the activity of two enzymes involved in the recycling of aa, AST and ALT, increased in roots but not in leaves (Figure7). These data are also supported by proteomic studies conducted on cucumber[9] and Medicago truncatula[11] where the concentration of ALT and AST, respectively, were found to increase under Fe deficiency. Furthermore, a C-N hydrolase family protein has been identified in cucumber roots, and its concentration increased under Fe deficiency[9]. This family of enzymes is involved in N metabolism and catalyses the cleavage of the amino group from C skeletons (amino acid and protein)[53]. Hence, the amino groups released could be re-assimilated throughout the GS/GOGAT cycle into new aa. In Donnini et al.[9] an intriguing hypothesis, albeit speculative, was formulated: some proteins (e.g. actin, tubulin and globulin) might be used as a source of aa, carbon skeletons and N-NH4+ under Fe deficiency. We could hypothesise that in this condition a portion of the newly assimilated N might derive from proteins already present which are sacrificed for the survival of the plant. On the other hand, it appears that plants possess a regulated protein degradation machinery[54] and references therein that are particularly active during the stress response and senescence, leading to a continuous turnover of cellular proteins. As a consequence, the aa released in the roots could, in part, be transported to the leaves to keep N metabolism functioning (Figure8). Indeed, the N assimilation process (i.e. NR plus GS/GOGAT) was affected more in leaves than in roots, and so the increase in aa concentration apparently depends mainly on their translocation from the roots.

Bottom Line: Under Fe deficiency, only nitrate reductase (EC 1.7.1.1) activity decreased both at the root and leaf level, whilst for glutamine synthetase (EC 6.3.1.2) and glutamate synthase (EC 1.4.1.14) an increase was found.Accordingly, the transcript analysis for these enzymes showed the same behaviour except for root nitrate reductase which increased.Furthermore, it was found that amino acid concentration greatly decreased in Fe-deficient roots, whilst it increased in the corresponding leaves.

View Article: PubMed Central - HTML - PubMed

Affiliation: Dipartimento di Scienze Agrarie e Ambientali - Produzione, Territorio, Agroenergia, Università degli Studi di Milano, Milano, Italy.

ABSTRACT

Background: Nitrogen is a principal limiting nutrient in plant growth and development. Among factors that may limit NO3- assimilation, Fe potentially plays a crucial role being a metal cofactor of enzymes of the reductive assimilatory pathway. Very few information is available about the changes of nitrogen metabolism occurring under Fe deficiency in Strategy I plants. The aim of this work was to study how cucumber (Cucumis sativus L.) plants modify their nitrogen metabolism when grown under iron deficiency.

Results: The activity of enzymes involved in the reductive assimilation of nitrate and the reactions that produce the substrates for the ammonium assimilation both at root and at leaf levels in Fe-deficient cucumber plants were investigated. Under Fe deficiency, only nitrate reductase (EC 1.7.1.1) activity decreased both at the root and leaf level, whilst for glutamine synthetase (EC 6.3.1.2) and glutamate synthase (EC 1.4.1.14) an increase was found. Accordingly, the transcript analysis for these enzymes showed the same behaviour except for root nitrate reductase which increased. Furthermore, it was found that amino acid concentration greatly decreased in Fe-deficient roots, whilst it increased in the corresponding leaves. Moreover, amino acids increased in the xylem sap of Fe-deficient plants.

Conclusions: The data obtained in this work provided new insights on the responses of plants to Fe deficiency, suggesting that this nutritional disorder differentially affected N metabolism in root and in leaf. Indeed under Fe deficiency, roots respond more efficiently, sustaining the whole plant by furnishing metabolites (i.e. aa, organic acids) to the leaves.

Show MeSH
Related in: MedlinePlus