Control of Nitrate Uptake by Phloem-Translocated Glutamine in Zea mays L. Seedlings

Abstract

The putative role of glutamine, exported from leaves to roots, as a negative feedback signal for nitrate uptake was investigated in Zea mays L. seedlings. Glutamine (Gln) was supplied by immersion of the tip-cut leaves in a concentrated solution. Nitrate (NO₃ ^-) uptake was measured by its depletion in amino acid-free medium. The treatment with Gln resulted in a strong inhibition of nitrate uptake rate, accompanied by a significant enrichment of amino compounds in root tissue. The effect of N-availability on NO₃ ^- uptake was determined in split-root cultures. The plants were subjected to complete or localized N supply. Inducible NO₃ ^- uptake systems were also induced in N-deprived roots when the opposite side of the root system was supplied with KNO₃. The inhibitory effect of Gln was unaffected by localized N supply on one side of the split-root. The potential role of Gln in the shoot-to-root control of NO₃ ^- uptake is discussed.

Glutamine - maize roots - nitrate uptake - split-root cultures

References

• 01 Aslam,  M.,, Travis,  R. L.,, and Huffaker,  R. C.. (1992);  Comparative kinetics and reciprocal inhibition of nitrate uptake in root of uninduced and induced barley (Hordeum vulgare L.) seedlings.  Plant Physiol.. 99 1124-1133
• 02 Aslam,  M.,, Travis,  R. L.,, and Rains,  D. W.. (2001);  Differential effect of amino acids on nitrate uptake and reduction systems in barley roots.  Plant Science. 160 219-228
• 03 Barneix,  A. J., and Causin,  H. F.. (1996);  The central role of amino acids on nitrogen utilisation and plant growth.  J. Plant Physiol.. 149 358-362
• 04 Caputo,  C., and Barneix,  A. J.. (1997);  Export of amino acids to the phloem in relation to N supply in wheat.  Physiol. Plant. 101 853-860
• 05 Cerezo,  M.,, Flors,  V.,, Legaz,  F.,, and García-Agustín,  P.. (2000);  Characterization of the low affinity transport system for NO₃ ^- uptake by Citrus roots.  Plant Sci.. 160 95-104
• 06 Chrispeels,  M. J.,, Crawford,  N. M.,, and Schroeder,  J. I.. (1999);  Proteins for transport of water and mineral nutriens across the membranes of plant cells.  Plant Cell. 11 661-675
• 07 Cooper,  H. D., and Clarkson,  D. T.. (1989);  Cycling of amino-nitrogen and other nutrients between shoots and roots in cereals. A possible mechanism integrating shoot and root in the regulation of nutrient uptake.  J. Exp. Bot.. 40 733-762
• 08 Crawford,  N. M., and Glass,  A. D. M.. (1998);  Molecular and physiological aspects of nitrate uptake in plants.  Trends Plant Sci.. 3 389-395
• 09 Drew,  M. C., and Saker,  L. R.. (1975);  Nutrient supply and the growth of the seminal root system in barley II. Localized, compensatory increases in lateral root growth and rates of nitrate uptake when nitrate supply is restricted to only part of the root system.  J. Exp. Bot.. 26 79-90
• 10 Gansel,  X.,, Muňos,  S.,, Tillard,  P.,, and Gojon,  A.. (2001);  Differential regulation of the NO₃ ^- and NH₄ ⁺ transporter genes AtNrt2.1 and AtAmt1.1 in Arabidopsis: relation with long-distance and local controls by N status of the plant.  Plant J.. 26 143-155
• 11 Gessler,  A.,, Schultze,  M.,, Schrempp,  S.,, and Rennenberg,  H.. (1998);  Interaction of phloem-translocated amino compounds with nitrate net uptake by the roots of beech (Fagus sylvatica) seedlings.  J. Exp. Bot.. 49 1529-1537
• 12 Glass,  A. D. M.,, Siddiqi,  M. Y.,, Ruth,  T. J.,, and Rufty,  T. W.. (1990);  Studies of the nitrate uptake in barley II. Energetics.  Plant Physiol.. 93 1585-1589
• 13 Gojon,  A.,, Soussana,  J. F.,, Passama,  L.,, and Robin,  P.. (1986);  NItrate reduction in roots and shoots of barley (Hordeum vulgare L.) and corn (Zea mays L.) seedlings.  Plant Physiol.. 82 254-260
• 14 Hole,  D. J.,, Emran,  A. M.,, Fares,  Y.,, and Drew,  M. C.. (1990);  Induction of nitrate transport in maize roots and kinetics of influx measured with nitrogen-13.  Plant Physiol.. 93 642-647
• 15 Huang,  N.-Ch.,, Chiang,  C.-S.,, Crawford,  N. M.,, and Tsay,  Y. F.. (1996);  CHL1 encodes a component of the low-affinity nitrate uptake system in Arabidopsis and shows cell type-specific expression in roots.  Plant Cell. 8 2183-2191
• 16 Hutta,  M.,, Chalányová,  M.,, and Góra,  R.. (2001) Fast RPHPLC Analysis of diethylethoxymethylenemalonate derivatized amino acids by the use of chromolith monolithic-type column.  Bratislava, Slovak Republic; Proceedings 11th International Symposium, Advances and applications of chromattography in industry, August 27 - 31, 2001 ISSN 1335-8413 Poster B-03
• 17 Imsande,  J., and Touraine,  B.. (1994);  N demand and the regulation of nitrate uptake.  Plant Physiol.. 105 3-7
• 18 Kallarackal,  J.,, Orlich,  G.,, Schobert,  C.,, and Komor,  E.. (1989);  Sucrose transport into the phloem of Ricinus communis L. seedlings as measured by the analysis of sieve-tube sap.  Planta. 177 327-335
• 19 King,  B. J.,, Siddiqi,  M. Y.,, Ruth,  T. J.,, Warner,  R. L.,, and Glass,  A. D. M.. (1993);  Feedback regulation of nitrate influx in barley roots by nitrate, nitrite and ammonium.  Plant Physiol.. 102 1279-1286
• 20 Lainé,  P.,, Ourry,  A.,, and Boucand,  J.. (1995);  Shoot control of nitrate uptake rates by roots of Brassica napus L.: Effects of localized nitrate supply.  Planta. 196 77-83
• 21 Lam,  H.-M.,, Coschigano,  K. T.,, Oliveira,  I. C.,, Melo-Oliveira,  R.,, and Coruzzi,  G. M.. (1996);  The molecular-genetics of nitrogen assimilation into amino acids in higher plants.  Annu. Rev. Plant Physiol. Plant Mol. Biol.. 47 569-593
• 22 Larsson,  C. M.,, Larsson,  M.,, Purves,  J. V.,, and Clarkson,  D. T.. (1991);  Translocation and cycling through roots of recently absorbed nitrogen and sulphur in wheat (Triticum aestivum) during vegetative and generative growth.  Physiol. Plantarum. 82 345-352
• 23 Lee,  R. B.,, Purves,  J. V.,, Ratcliffe,  R. G.,, and Saker,  L. R.. (1992);  Nitrogen assimilation and the control of maize roots.  J. Exp. Bot.. 43 1385-1396
• 24 Liu,  K.-H.,, Huang,  Ch.-Y.,, and Tsay,  Y. F.. (1999);  CHL1 is a dual affinity nitrate transporter of Arabidopsis involved in multiple phases of nitrate uptake.  Plant Cell. 11 865-874
• 25 Macduff,  J. H., and Jackson,  S. B.. (1992);  Influx and efflux of nitrate and ammonium in Italian ryegrass and white clover roots: compartmentations between effects of darkness and defoliation.  J. Exp. Bot.. 43 525-535
• 26 Mistrík,  I.. (1997);  Nitrate uptake and assimilation by individual roots of Zea mays. .  Biologia, Bratislava. 52 567-571
• 27 Muller,  B., and Touraine,  B.. (1992);  Inhibition of NO₃ ^- uptake by various phloem-translocated amino acids in soybean seedlings.  J. Exp. Bot.. 43 617-623
• 28 Pal'ove-Balang,  P., and Mistrík,  I.. (2002);  Differential effect of amino acids on the uptake of nitrate by roots of maize seedlings.  Biologia, Bratislava. 57 119-124
• 29 Pate,  J. S.. (1971) Movement of nitrogenous solutes in plants. Nitrogen 15 in soil-plant studies. Vienna; International Atomic Energy Agency pp. 165-187
• 30 Peuke,  A. D.,, Hartung,  W.,, and Jeschke,  W. D.. (1994);  The uptake and flow of C, N and ions between roots and shoots in Ricinus communis L. II. Growth with low or high nitrate supply.  J. Exp. Bot.. 45 733-740
• 31 Siddiqi,  M. Y.,, Glass,  A. D. M.,, Ruth,  T. J.,, and Rufty,  T. W.. (1990);  Studies of the uptake of nitrate in barley I. Kinetics of ¹³NO₃ ^- influx.  Plant Physiol.. 93 1426-1432
• 32 Tillard,  P.,, Passama,  L.,, and Gojon,  A.. (1998);  Are phloem amino acids involved in the shoot to root control of NO₃ ^- uptake in Ricinus communis plants?.  J. Exp. Bot.. 49 1371-1379
• 33 Vidmar,  J. J.,, Zhuo,  D.,, Siddiqi,  M. Y.,, Schjoerig,  J. K.,, Touraine,  B.,, and Glass,  A. D. M.. (2000);  Regulation of high-affinity nitrate transporter genes and high-affinity nitrate influx by nitrogen pools in roots of barley.  Plant Physiol.. 123 307-318
• 34 Wintner,  H.,, Lohaus,  G.,, and Heldt,  H. W.. (1992);  Phloem transport of amino acids in relation to their cytosolic levels in barley leaves.  Plant Physiol.. 99 996-1004
• 35 Zhuo,  D.,, Okamoto,  M.,, Vidmar,  J. J.,, and Glass,  A. D. M.. (2000);  Regulation of putative high-affinity nitrate transporter (Nrt2;1At) in roots of Arabidopsis thaliana. .  Plant J.. 17 563-568

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