Nitrate regulation of metabolism and growth

Current Opinion in Plant Biology

Volumn 2, Issue 3, 1999, Pages 178-186

  Stitt, Mark ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

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EID: 0033151521     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1369-5266(99)80033-8     Document Type: Article

References (79)

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6. Scheible W-R, Lauerer M, Schulze E-D, Caboche M, Stitt M: Accumulation of nitrate in the shoot acts as signal to regulate shoot-root allocation in tobacco. Plant J 1997, 11:671-691. Tobacco mutants and transformants with decreased expression of NIA were grown at various nitrogen supplies, and the levels of nitrate, amino acids, protein, overall growth and shoot-root allocation investigated. Accumulation of nitrate in low-NIA genotypes inhibited root growth, resulting in a higher shoot - root ratio than in nitrogen-replete wild-type plants, even though amino acid and protein levels and overall growth rates resembled those in nitrogen-deficient wild-type plants. Split-root experiments showed that root growth was decreased due to accumulation of nitrate in the shoot. High local levels of nitrate in the rooting medium stimulated growth, also via mechanisms that did not require metabolism of nitrate.
7. Scheible W-R, Gonzales-Fontes A, Lauerer M, Müller-Röber B, Caboche M, Stitt M: Nitrate acts as a signal to induce organic acid metabolism and repress starch metabolism in tobacco. Plant Cell 1997, 9:783-798. Tobacco mutants and transformants with decreased NIA expression were grown on low and high nitrate and investigated with respect to transcripts, enzyme activities and metabolites in nitrogen and carbon metabolism in leaves and roots. Accumulation of nitrate led to increased expression and activity of genes involved in nitrate and ammonium assimilation (NIA, NII, GLN1, GLN2, GLU) and organic acid synthesis (PPC, cytosolic PK, CS, ICDH-1) and accumulation of malate and α-oxoglutarate, and to decreased expression of AGPS and decreased levels of starch. The changes in transcripts were independent of the metabolism of the nitrate, and occurred within 2-4 h after supplying nitrate to the roots of whole plants.
8. Stitt M, Feil R: Lateral root frequency decreases when nitrate accumulates in tobacco transformants with low nitrate reductase activity: Consequences for the regulation of biomass partitioning between shoots and roots. Plant Soil 1999, in press In a sequel to [6••], low-NIA tobacco transformants were grown on nutrient agar at various nitrate supplies in the presence or absence of sucrose. The inhibition of root growth when nitrate accumulates in the plant was accompanied by a marked decrease in the frequency of growing lateral roots, which was not relieved by including sucrose in the medium.
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12. Hoff T, Truong H-N, Caboche M: The use of mutants and transgenic plants to study nitrate metabolism. Plant Cell Environ 1994, 17:486-506.
13. Krapp A, Fraisier V, Scheible W-R, Quesada A, Gojon A, Stitt M, Caboche M, Daniel-Vedele F: Expression studies of Nrt2:1Np, a putative high affinity nitrate transporter: Evidence for its role in nitrate uptake. Plant J 1998, 6:723-732. Investigations in wild-type tobacco and low-NIA transformants showed that NRT2:1Np (encoding a high affinity nitrate transporter) is induced by nitrate, and repressed by ammonium or a product of ammonium metabolism.
14. Filleur S, Danielle-Vedele F: Expression analysis of a high-affinity nitrate transporter isolated from Arabidopsis thaliana by differential display. Planta 1998, 207:461-489.
15. 3-uptake systems by N- and C-status of Arabidopsis plants. Plant J 1999, in press. Transcript levels for NRT2:1 and NRT1 (encoding a high and low affinity nitrate transporter) and nitrate uptake rates were studied in wild-type Arabidopsis and low-NIA mutants growing at various nitrogen supplies. Diurnal changes and the response to added sugar were also analysed. Nitrate induces both transporters, whereas ammonium or products of ammonium assimilation repress both transporters, and sugars lead to increased expression of both transporters. Further, it is shown that the changes in transcript levels correlate with changes in the rates of nitrate uptake.
16. Migge A, Carrayol E, Kunz C, Hirel B, Fock H, Becker T: The expression of the tobacco genes encoding plastidic glutamine synthetase or ferredoxin-dependent glutamate synthase does not depend on the rate of nitrate reduction, and is unaffected by suppression of photorespiration. J Exp Bot 1997, 48:1175-1184. Inhibition of nitrate assimilation by addition of tungsten led to increased expression of NIA and NII but did not alter expression of GS2 and GLU, indicating that downstream products of nitrate assimilation exert feed-back control on the nitrate assimilation pathway, but not on the ammonium assimilation pathway.
17. Redinbaugh MG, Campbell WH: Glutamine synthetase and ferredoxin-dependent glutamate synthase expression in the maize (Zea mays) root: Primary response to nitrate. Plant Physiol 1993, 101:1249-1255.
18. Gowri G, Ingemarsson B, Redinbaugh MG, Campbell WH: Nitrate reductase transcript is expressed in the primary response of maize to environmental nitrate. Plant Mol Biol 1992, 18:55-64.
19. (+) oxidoreductase. Plant Mol Biol 1994, 26:679-690.
20. Redinbaugh MG, Campbell WH: Nitrate regulation of the oxidate pentose phosphate pathway in maize root plastids: Induction of 6-phosphogluconate activity, protein and transcript levels. Plant Science 1998, 134:129-140. Addition of nitrate to maize plants leads to a rapid increase of transcript encoding 6-phosphogluconate dehydrogenase via a mechanism that does not require the intervening synthesis of new proteins. Longer treatments lead to an increase of 6-phosphogluconate protein and activity. This is the first report directly linking nitrate to regulation of the oxidative pentose phosphate pathway, which is required to supply reducing equivalents for nitrate assimilation in roots.
21. Amarasingh BHRR, De Bruxelles GL, Braddon M, Onyeocha I, Forde BG, Udvardi MK: Regulation of GmNRT2 expression and nitrate transport activity in roots of soybean (Glycine max). Planta 1998, 206:44-52.
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24. 2+ and protein phosphorylation in the signalling mechanism
25. 3- uptake and reduction in Nicotiana plants. Plant Cell Environ 1998, 21:43-53. Increased expression of NIA leads to decreased nitrate uptake, whereas decreased expression leads to accumulation of nitrate in the plants. These results indicate that a downstream metabolite of nitrate metabolism represses nitrate uptake, and provide direct evidence that changes in the rate of nitrate assimilation in the leaves have consequences for the rate of nitrate uptake in the roots. Possible molecular mechanisms for this interaction are presented in [15••].
26. Matsumara T, Sakaibara H, Nakano R, Kimata Y, Sugiyama T, Hase T: A nitrate-inducible ferredoxin in maize roots: Genomic organisation and differential expression of two non-photosynthetic ferredoxin apoproteins. Plant Physiol 1997, 114:653-660. Reduction of nitrate to ammonium in the roots requires reduced ferredoxin for the plastid-localised NII step. This paper shows that nitrate induces a non-photosynthetic ferredoxin genes in maize roots. Together with [20••], it shows that nitrate re-programmes root cells to increase the delivery of redox equivalents in the appropriate form to support nitrate assimilation.
27. 2 are triggered by changes in the nitrogen status, including nitrate. This challenges the wide-spread view that these changes in carbon metabolism are caused by sugar-regulation of gene expression.
28. Stitt M, Krapp A: The molecular physiological basis for the interaction between elevated carbon dioxide and nutrients. Plant Cell Environ 1999, in press.
29. Scheible W-R, Gonzalez-Fontes A, Morcuende R, Lauerer M, Geiger M, Glaab J, Gojon A, Schulze E-D, Stitt M: Tobacco mutants with a decreased number of functional nia genes compensate by modifying the diurnal regulation of transcription, post-translational modification and turnover of nitrate reductase. Planta 1997, 203:304-319. It is well established in several species that mutants with a 50-90% decrease in maximum NIA activity grow at similar rates to wild-type plants. This study of tobacco mutants shows that they compensate by altering the diurnal regulation of NIA protein levels and post-translational regulation of NIA, whereas the diurnal changes of NIA transcript levels were not markedly modified. Comparison of the in vivo changes in NIA protein and activation and the endogenous changes in glutamine as well as the effect of feeding exogenous glutamine provide indirect evidence that glutamine or related metabolites exert feed-back regulation on the activation and stability of NIA protein.
30. Geiger M, Walch-Piu L, Harnecker J, Schulze E-D, Ludewig F, Sonnewald U, Scheible W-R, Stitt M: Enhanced carbon dioxide leads to a modified diurnal rhythm of nitrate reductase activity in older plants, and a large stimulation of nitrate reductase activity and higher levels of amino acids in higher plants. Plant Cell Environ 1998, 21:253-268. NIA transcript typically declines dramatically during the photoperiod, even when the leaves still retain a considerable nitrate pool. One finding in this article is that re-irrigation with a high nitrate concentration late in the photoperiod partially reverses this inhibition, indicating that the influx rather than the total pool of nitrate is critical for the regulation of NIA expression.
31. Vincentz M, Moureaux T, Leydecker MT, Vaucheret H, Caboche M: Regulation of nitrate and nitrite reductase expression in Nicotiana plumbaginifolia leaves by nitrogen and carbon metabolites. Plant J 1993, 3:313-324.
32. Sivaskar S, Rothstein S, Oaks A: Regulation of the accumulation and reduction of nitrate by nitrogen and carbon metabolites in maize seedlings. Plant Physiol 1997, 114:583-589. In roots of maize seedlings, NIA transcript and NIA activity are increased by sugars and reduced by amino acids including glutamine and asparagine.
33. Tillard P, Passama L, Gojon A: Are amino acids involved in the shoot to root control of nitrate uptake in Ricinus communis plants? J Exp Bot 1998, 49:1371-1379. It has been widely assumed that amino acids moving in the phloem from the shoot to the roots are responsible for an inhibition of nitrate uptake. This article shows, using a split-root system, that addition of nitrate to one root sector leads to inhibition of nitrate uptake in the other root sector, even though the levels of amino acids in the low-nitrogen sector do not increase.
34. 2. Despite a large accumulation of glutamine, NIA transcript responded as in wild-type plants. The authors conclude that glutamine does not exert feed-back regulation on NIA, and argue that the repression reported in earlier studies after adding exogenous glutamine may be an indirect effect, due to glutamine inhibiting nitrate uptake.
35. Koch KE: Carbohydrate-modulated gene expression in plants. Annu Rev Plant Mol Biol Plant Physiol 1996, 47:509-540.
36. Jang JC, Sheen J: Sugar sensing in higher plants. Trends Plant Sci 1997, 2:208-214.
37. Morcuende R, Krapp A, Hurry V, Stitt M: Sucrose feeding leads to increased rates of nitrate assimilation, increased rates of α-oxoglutarate synthesis, and increased synthesis of a wide spectrum of amino acids in tobacco leaves. Planta 1998, 206:394-409.
38. MacKintosh C: Regulation of cytosolic enzymes in primary metabolism by reversible protein phosphorylation. Curr Opin Plant Sci 1998, 1:224-229. A provocative review of the role of protein phosphorylation and of 14-3-3 proteins in regulating primary metabolism and proton pumping at the plasmalemma, that highlights possible interactions between carbon metabolism, nitrogen metabolism and pH regulation.
39. Matt P, Schurr U, Krapp A, Stitt M: Growth of tobacco in short day conditions leads to high starch, low sugars, altered diurnal changes of the nia transcript and low nitrate reductase activity, and an inhibition of amino acid synthesis. Planta 1998, 207:27-41. It was well established that sugar addition leads to an increase of NIA transcript and activity in detached leaves, but the situations in which sugars exert an over-riding influence on nitrate assimilation were previously unclear. By investigating the effects of an increasingly long dark period in combination with petiole cooling to inhibit phloem export, it is shown that when sugars fall below a critical level (5-10 μmol/g fresh weight) they strongly inhibit NIA expression and activity, over-riding signals derived from nitrate and nitrogen metabolism. Measurements of amino acid levels indicate that sugars also exert a global inhibition on the amino acid biosynthesis pathways.
40. Botrel A, Kaiser W: Nitrate reductase activation status in barley roots in relation to the energy and carbohydrate status. Planta 1997, 201:496-501. In studies investigating the stimulatory effect of anaerobiosis on post-translational regulation of nitrate reductase, it was shown that the activation is due to acidification, rather than to changes in the energy status. It is also shown that the decline of NIA activity in prolonged darkness can be prevented by sugar addition.
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44. Zhang H, Forde BG: An Arabidopsis MADS-box gene controlling nutrient-induced changes in root architecture. Science 1998, 279:407-409. A MADS-box transcription factor ANR1 was identified in a screen for nitrate-induced genes, and its function investigated in antisense Arabidopsis transformants. The overall frequency of lateral root formation in wild-type Arabidopsis (see also [6••] and [8•]) decreases when plants are grown in high nitrate, whereas local application of nitrate leads to increased lateral root proliferation at the site of application. Antisense inhibition of ANR1 expression increased the sensitivity with which high nitrate inhibited lateral root development, and decreased the effectiveness with which localised applications increased lateral root development. It is also shown that local application of nitrate still induces lateral root formation in severely NIA-deficient mutants, showing that nitrate acts as a signal rather than via metabolism to promote growth via increased local availability of amino acids.
45. Zhang H, Jennins A, Barlow P, Forde BG: Dual pathways for regulation of root branching by nitrate. Proc Natl Acad Sci USA 1999, in press. The mechanisms whereby nitrate modulates lateral root formation are further investigated. High nitrate does not inhibit initiation but, rather, acts at the stage where they emerge from the root, apparently delaying final activation of the meristem. This inhibition is accentuated in low-NIA mutants, indicating that tissue nitrate levels are involved in generating the signal.
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56. Jiang P, Peliska JA, Ninfa AJ: Enzymological characterisation of the signal-transducing uridyltransferase/uridyl-removing enzyme of Eschericia coli and its interaction with the PII protein. Biochemistry 1998, 37:12782-12794.
57. Atkinson MR, Ninfa AJ: Role of the Glnk singnal transduction protein in the regulation of nitrogen assimilation in Eschericia coli. Mol Microbiol 1998, 29:431-477.
58. Xu YB, Cheah E, Carr DD, van Heeswijk WC, Westerhoff HV, Vasudevan SG, Ollis DL: GlnK, a P-II homologue: Structure reveals ATP binding site and indicates how the T-loops may be involved in molecular recognition. J Mol Biol 1998, 282:149-165.
59. Garcia Dominguez M, Florencia FJ: Nitrogen availability and electron transport control the expression of glnB gene encoding PII protein in the cyanobacterium Synechocystis sp. PCC 6803. Plant Mol Biol 1997, 35:723-734.
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61. Hsieh M-H, Lam H-M, van de Loo FJ, Coruzzi G: A PII-like protein in Arabidopsis: Putative role in nitrogen sensing. Proc Natl Acad Sci USA 1998, 95:13965-13970. This is the first report of a PII protein in plants. It was identified from a EST in Arabidopsis, and is shown to be a nuclear encoded protein whose sequence indicates a plastid localisation. It differs from the classical E. coli PII system but resembles several recently reported PII homologs in E. coli and other organisms in showing transcriptional regulation in response to sugars and nitrogen metabolites (see [57-59,60•]) rather than being regulated post-translationally via uridenylation/de-uridenylation (see [54-56]).
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67. Rastogi R, Bate NJ, Sivanskar S, Rothstein SJ: Footprinting of the spinach nitrite reductase gene promotor reveals the preservation of nitrate regulatory elements between fungi and higher plants. Plant Mol Biol 1997, 34:465-476. Following earlier investigations showing that a 130 bp upstream region of the spinach nii promotor suffices to confer nitrate-induction of gus expression, a 50 bp region was identified by deletion studies that contained two adjacent gata elements, and bound in vitro a fusion protein containing the zinc finger domain of neurospora crassa nit2. These results indicate that nii expression is mediated by nitrate-specific binding of trans-acting factors to sequences that are preserved between fungi and plants.
68. Truong HN, Caboche M, Daniel-Vedele F: Sequence and characterization of two Arabidopsis thaliana cDNAs isolated by functional complementation of a yeast gln3 gdh1 mutant. FEBS Lett 1997, 410:213-218. Two Arabidopsis cDNA sequences were identified that are able to functionally complement a yeast gln3 mutant. GLN3 is related to the positive control genes that mediate repression of nitrate assimilation when preferred nitrogen sources like ammonium or glutamine are available - AREA and NIT2 in Aspergillus nidulans and Neurospora crassa, respectively. The Arabidopsis genes (termed RGA1 and RGA2, restore growth on ammonium) are members of a multigene family whose other members include SCARECROW that regulates pattern formation in roots. They are identical (see [69]) to GAI and RGA, that are involved in gibberellin signal transduction.
69. Daniel-Vedele F, Filleur S, Caboche M: Nitrate transport: A key step in nitrate assimilation. Curr Opin Plant Biol 1998, 1:235-239.
70. Navarro MT, Prieto R, Fernandez E, GalvAn A: Constitutive expression of nitrate reductase changes the regulation of nitrate and nitrate transporters in Chlamydomonas reinhardtii. Plant J 1996, 9:819-827.
71. Prieto R, Dubus A, Galvan A, Fernandez E: Isolation and characterisation of two new negative regulatory mutants for nitrate assimilation in Chlamydomonas obtained by insertional mutagenesis. Mol Gen Genet 1996, 251:461-471.
72. Murry LE, Rowley N, Dawes IW, Johnston GC, Singer RA: A yeast glutamine tRNA signals nitrogen status for regulation of dimorphic growth and sporulation. Proc Natl Acad Sci USA 1998, 95:8619-8624. This intriguing article reports that a glutamine tRNA isoform is involved in nitrogen-signalling in yeast. Mutants lacking this isoform impair nitrogen sensing without impairing protein synthesis, leading to pseudohyphal growth, sporulation even in the presence of preferred nitrogen sources.
73. Kobayashi M, Rodriguez R, Lara C, Omata T: Involvement of the C-terminal domain of an ATP-binding subunit in the regulation of the ABC-type nitrate/nitrite transporter of the cyanobacterium Synecoccus sp. Strain PCC 7942. J Biol Chem 1997, 272:27197-27201.
74. Lorenz MC, Heitman J: The MEP2 ammonium permease regulates pseudohyphal differentiation in Saccharomyces cerevisiae. EMBO J 1998, 17:1236-1247.
75. Iraqui J, Vissers S, Bernard F, De Craene J-O, Boles E, Urrestarazu A, André B: Amino acid signaling in Saccharomyces cerevisiae: A permease-like sensor of external amino acids and the F-box protein Grr1p are required for transcriptional induction of the AGP1 gene encoding a broad-specificity amino acid permease. Mol Cell Biol 1999, 19:989-1001.
76. Didion T, Regenberg B, Jorgensen MU, Kielland-Brandt MC, Andersen HA: The permease homologue Ssy1p controls the expression of amino acid and peptide transporter genes in Saccharomyces cerevisiae. Mol Microbiol 1998, 27:643-650.
77. Sakakibara H, Suzuki M, Takei M, Deji A, Taniguchi M, Sugiyama T: A response-regulator homolog possibly involved in nitrogen signal transduction mediated by cytokinin in maize. Plant J 1998, 14:337-344. Addition of nitrate or ammonium to the roots of intact maize plants leads to induction of PPC in the leaves, whereas addition of nitrogen sources to the leaves does not. This paper implicates the synthesis of cytokinins in the roots and cytokinin-induction of a response-regulator homolog ZmCIP1 in the leaf signalling pathway in the signalling pathway.
78. Chandok MR, Sopory SK: ZmcPKC70, a protein kinase-type enzyme from maize- biochemical characterisation, regulation by phorbol 12-myristate 13-acetate and its possible involvement in nitrate reductase gene expression. J Biol Chem 1998, 273:19235-19242.
79. Taniguchi M, Kiba T, Sakakibara H, Ueguchi C, Mizuno T, Sugiyama T: Expression of Arabidopsis response regulator homologs is induced by cytokinins and nitrate. FEBS Lett 1998, 429:259-262. In a sequel to [74], five response regulator homologs are identified in Arabidopsis whose expression is increased by addition of nitrate or cytokinins. The identity of the ligand for the response regulators is still unknown, but they could represent a self-amplification loop or a change in sensitivity to further unidentified signalling components.