Skip to main content
SpringerLink
Log in

Molecular aspects of nitrogen mobilization and recycling in trees

  • Review
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

Plants have developed a variety of molecular strategies to use limiting nutrients with a maximum efficiency. N assimilated into biomolecules can be released in the form of ammonium by plant metabolic activities in various physiological processes such as photorespiration, the biosynthesis of phenylpropanoids or the mobilization of stored reserves. Thus, efficient reassimilation mechanisms are required to reincorporate liberated ammonium into metabolism and maintain N plant economy. Although the biochemistry and molecular biology of ammonium recycling in annual herbaceous plants has been previously reported, the recent advances in woody plants need to be reviewed. Moreover, it is important to point out that N recycling is quantitatively massive during some of these metabolic processes in trees, including seed germination, the onset of dormancy and resumption of active growth or the biosynthesis of lignin that takes place during wood formation. Therefore, woody plants constitute an excellent system as a model to study N mobilization and recycling. The aim of this paper is to provide an overview of different physiological processes in woody perennials that challenge the overall plant N economy by releasing important amounts of inorganic N in the form of ammonium.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • I Allona C Collada R Casado C Aragoncillo (1994) ArticleTitle2S arginine-rich proteins from Pinus pinaster seeds Tree Physiol 14 211–218 Occurrence Handle14967715

    PubMed  Google Scholar 

  • AM Anterola NG Lewis (2002) ArticleTitleTrends in lignin modification: a comprehensive analysis of the effects of genetic manipulations/mutations on lignification and vascular integrity Phytochemistry 61 221–294 Occurrence Handle10.1016/S0031-9422(02)00211-X Occurrence Handle12359514

    Article  PubMed  Google Scholar 

  • C Avila A García-Gutiérrez R Crespillo FM Cánovas (1998) ArticleTitleEffects of phosphinothricin treatment on glutamine synthetase isoforms in Scots pine seedlings Plant Physiol Biochem 36 857–863 Occurrence Handle10.1016/S0981-9428(99)80003-5

    Article  Google Scholar 

  • C Avila R Muñoz-Chapuli C Plomion JM Frigerio FM Cánovas (2000) ArticleTitleTwo genes encoding distinct cytosolic glutamine synthetases are closely linked in the pine genome FEBS Lett 477 237–243 Occurrence Handle10.1016/S0014-5793(00)01796-8 Occurrence Handle10908727

    Article  PubMed  Google Scholar 

  • C Avila MF Suárez J Gómez-Maldonado FM Cánovas (2001) ArticleTitleSpatial and temporal expression of two cytosolic glutamine synthetase genes in Scots pine: functional implications on nitrogen metabolism during early stages of conifer development Plant J 25 93–102 Occurrence Handle10.1046/j.1365-313x.2001.00938.x Occurrence Handle11169185

    Article  PubMed  Google Scholar 

  • RL Barnes (1963) ArticleTitleOrganic nitrogen compounds in tree xylem sap For Sci 9 98–102

    Google Scholar 

  • J Bewley A Makus (1990) ArticleTitleGene expression in seed development and germination Prog Nucleic Acid Res Mol Biol 38 165–193 Occurrence Handle2183293

    PubMed  Google Scholar 

  • N Brugière F Dubois C Masclaux RS Sangwan B Hirel (2000) ArticleTitleImmunolocalization of glutamine synthetase in senescing tobacco (Nicotiana tabacum L.) leaves suggests that ammonia assimilation is progresively shifted to the mesophyll cytosol Planta 211 519–527 Occurrence Handle10.1007/s004250000309 Occurrence Handle11030551

    Article  PubMed  Google Scholar 

  • SL Butland ML Chow BE Ellis (1998) ArticleTitleA diverse family of phenylalanine ammonia-lyase genes expressed in pine trees and cell cultures Plant Mol Biol 37 15–24 Occurrence Handle10.1023/A:1005941228246 Occurrence Handle9620261

    Article  PubMed  Google Scholar 

  • FM Cánovas FR Cantón F Gallardo A García-Gutiérrez A Vicente Particlede (1991) ArticleTitleAccumulation of glutamine synthetase during early development of maritime pine (Pinus pinaster) seedlings Planta 185 372–378

    Google Scholar 

  • FM Cánovas FR Cantón A García-Gutiérrez F Gallardo R Crespillo (1998) ArticleTitleMolecular physiology of glutamine and glutamate biosynthesis in developing conifer seedlings Physiol Plant 103 287–294 Occurrence Handle10.1034/j.1399-3054.1998.1030217.x

    Article  Google Scholar 

  • FR Cantón A García-Gutiérrez F Gallardo A Vicente Particlede FM Cánovas (1993) ArticleTitleMolecular characterization of a cDNA clone encoding glutamine synthetase from a gymnosperm: Pinus sylvestris Plant Mol Biol 22 819–828 Occurrence Handle10.1007/BF00027368 Occurrence Handle8102906

    Article  PubMed  Google Scholar 

  • FR Cantón MF Suárez M José-Estanyol FM Cánovas (1999) ArticleTitleExpression analysis of a cytosolic glutamine synthetase gene in cotyledons of Scots pine seedlings: Developmental, light-dark regulation and spatial distribution of specific transcripts Plant Mol Biol 40 623–634 Occurrence Handle10.1023/A:1006219205062 Occurrence Handle10480386

    Article  PubMed  Google Scholar 

  • L Cardemil A Reinero (1982) ArticleTitleChanges of Araucaria araucana seed reserves during germination and early seedling growth Can J Bot 60 1629–1638

    Google Scholar 

  • GD Coleman THH Chen (1993) ArticleTitleSequence of a poplar bark storage protein gen Plant Physiol 102 1347–1348 Occurrence Handle10.1104/pp.102.4.1347 Occurrence Handle8278552

    Article  PubMed  Google Scholar 

  • G Coleman MP Bañados THH Chen (1994) ArticleTitlePoplar bark storage protein and a related wound induced gene are differentially induced by nitrogen Plant Physiol 106 211–215 Occurrence Handle12232321

    PubMed  Google Scholar 

  • KT Coschigano R Melo-Oliveira J Lim GM Coruzzi (1998) ArticleTitleArabidopsis gls mutants and distinct Fd-GOGAT genes Implications for photorespiration and primary nitrogen assimilation. Plant Cell 10 741–52 Occurrence Handle10.1105/tpc.10.5.741 Occurrence Handle9596633

    Article  PubMed  Google Scholar 

  • M Cren B Hirel (1999) ArticleTitleGlutamine synthetase in higher plants Regulation of gene and protein expression from the organ to the cell. Plant Cell Physiol 40 1187–1193

    Google Scholar 

  • R Douce M Neuburger (1999) ArticleTitleBiochemical dissection of photorespiration Curr Opin Plant Biol 2 214–222 Occurrence Handle10.1016/S1369-5266(99)80038-7 Occurrence Handle10375564

    Article  PubMed  Google Scholar 

  • F Dubois N Brugière RS Sangwan B Hirel (1996) ArticleTitleLocalization of tobacco cytosolic glutamine synthetase enzymes and the corresponding transcripts shows organ- and cell-specific patterns of protein synthesis and gene expression Plant Mol Biol 31 803–817 Occurrence Handle10.1007/BF00019468 Occurrence Handle8806411

    Article  PubMed  Google Scholar 

  • F Dubois T Tercé-laforgue MB González Moro JM Estavillo R Sangwan A Gallais B Hirel (2003) ArticleTitleGlutamate dehydrogenase in plants: is there a new story for an old enzyme Plant Physiol Biochem 41 565–576 Occurrence Handle10.1016/S0981-9428(03)00075-5

    Article  Google Scholar 

  • JW Edwards GM Coruzzi (1989) ArticleTitlePhotorespiration and light act in concert to regulate the expression of the nuclear gene for chloroplast glutamine synthetase Plant Cell 1 241–248 Occurrence Handle10.1105/tpc.1.2.241 Occurrence Handle2577725

    Article  PubMed  Google Scholar 

  • RP Feirer (1995) The biochemistry of conifer embryo development: amino acids, polyamines and storage proteins S Jain P Gupta R Newton (Eds) Somatic Embryogenesis in Woody Plants Kluwer Academic Publishers Dordrecht, The Netherlands 317–336

    Google Scholar 

  • J Fu R Sampalo F Gallardo FM Cánovas EG Kirby (2003) ArticleTitleAssembly of a cytosolic pine glutamine synthetase holoenzyme in the leaf of transgenic poplar leads to enhanced vegetative growth in young plants Plant Cell Environ 26 411–418 Occurrence Handle10.1046/j.1365-3040.2003.00972.x

    Article  Google Scholar 

  • SI Fuentes DJ Allen A Ortiz-López G Hernández (2001) ArticleTitleOver-expression of cytosolic glutamine synthetase increases photosynthesis and growth at low nitrogen concentrations J Exp Bot 52 1071–1081 Occurrence Handle10.1093/jexbot/52.358.1071 Occurrence Handle11432923

    Article  PubMed  Google Scholar 

  • F Gallardo J Fu FR Cantón A García-Gutiérrez FM Cánovas EG Kirby (1999) ArticleTitleExpression of a conifer glutamine synthetase gene in transgenic poplar Planta 210 19–26 Occurrence Handle10.1007/s004250050649 Occurrence Handle10592028

    Article  PubMed  Google Scholar 

  • F Gallardo J Fu ZP Jing EG Kirby FM Cánovas (2003) ArticleTitleGenetic manipulation of amino acid metabolism in woody plants Plant Physiol Biochem 41 587–594 Occurrence Handle10.1016/S0981-9428(03)00081-0

    Article  Google Scholar 

  • A García-Gutiérrez FR Cantón F Gallardo F Sánchez-Jiménez FM Cánovas (1995) ArticleTitleExpression of ferredoxin-dependent glutamate synthase in dark-grown pine seedlings Plant Mol Biol 27 115–128 Occurrence Handle10.1007/BF00019183 Occurrence Handle7865781

    Article  PubMed  Google Scholar 

  • A García-Gutiérrez F Dubois FR Cantón F Gallardo RS Sangwan FM Cánovas (1998) ArticleTitleTwo different modes of early development and nitrogen assimilation in gymnosperm seedlings Plant J 13 187–199 Occurrence Handle10.1046/j.1365-313X.1998.00018.x

    Article  Google Scholar 

  • DJ Gifford MC Tolley (1989) ArticleTitleThe seed proteins of white spruce and their mobilization following germination Physiol Plant 77 254–261

    Google Scholar 

  • DJ Gifford KA Wenzel DL Lammer (1989) ArticleTitleLodgepole pine seed-germination 1. Changes in peptidase activity in the megagametophyte and embryonic axis. Can J Bot 67 2539–2543

    Google Scholar 

  • V Glavac H Jockheim (1993) ArticleTitleA contribution to understanding the internal nitrogen budget of beech (Fagus sylvatica L.) Trees 7 237–241 Occurrence Handle10.1007/BF00202080

    Article  Google Scholar 

  • L Gomez M Faurobert (2002) ArticleTitleContribution of vegetative storage proteins to seasonal nitrogen variations in the young shoots of peach trees (Prunus persica L Batsch). J Exp Bot 53 2431–2439 Occurrence Handle10.1093/jxb/erf098 Occurrence Handle12432035

    Article  PubMed  Google Scholar 

  • J Gómez-Maldonado FM Cánovas C Avila (2004) ArticleTitleMolecular analysis of the 5′ upstream region of a gibberellin-inducible cytosolic glutamine synthetase gene (GS1b) expressed in the pine vascular tissue Planta 218 1036–1045 Occurrence Handle10.1007/s00425-003-1185-2 Occurrence Handle14735362

    Article  PubMed  Google Scholar 

  • M Gray-Mitsumune EK Molitor D Cukovic JE Carlson CJ Douglas (1999) ArticleTitleDevelopmentally regulated patterns of expression directed by poplar PAL promoters in transgenic tobacco and poplar Plant Mol Biol 39 657–669 Occurrence Handle10.1023/A:1006148715050 Occurrence Handle10350081

    Article  PubMed  Google Scholar 

  • M Groome S Axler (1991) ArticleTitleHydrolysis of lipid and protein reserves in loblolly pine seeds in relation to protein electrophoretic patterns following imbibition Physiol Plant 83 99–106 Occurrence Handle10.1034/j.1399-3054.1991.830115.x

    Article  Google Scholar 

  • AD Hanson S Roje (2001) ArticleTitleOne-carbon metabolism in higher plants Annu Rev Plant Physiol Plant Mol Biol 52 119–137 Occurrence Handle10.1146/annurev.arplant.52.1.119 Occurrence Handle11337394

    Article  PubMed  Google Scholar 

  • Harms U and Sauter JJ (1992) Localization of a storage protein in the wood ray parenchyma cells of Taxodium distichum (L.), L.C. Rich, by immunogold labeling. Trees 6: 37–40

    Google Scholar 

  • B Hirel P Bertin I Quilleré W Bourdoncle C Attagnant C Dellay A Gouy S Cadiou C Retailliau M Falque A Gallais (2001) ArticleTitleTowards a better understanding of the genetic and physiological basis for nitrogen use efficiency in maize Plant Physiol 125 1258–1270 Occurrence Handle10.1104/pp.125.3.1258 Occurrence Handle11244107

    Article  PubMed  Google Scholar 

  • C-L Ho K Saito (2001) ArticleTitleMolecular biology of the plastidic phosphorylated serine biosynthetic pathway in Arabidopsis thaliana Amino Acids 20 243–259 Occurrence Handle10.1007/s007260170042 Occurrence Handle11354602

    Article  PubMed  Google Scholar 

  • M Hodges (2002) ArticleTitleEnzyme redundancy and the importance of 2-oxoglutarate in plant ammonium assimilation J Exp Bot 53 905–916 Occurrence Handle10.1093/jexbot/53.370.905 Occurrence Handle11912233

    Article  PubMed  Google Scholar 

  • MH Hsieh HM Lam FJ Loo Particlevande G Coruzzi (1998) ArticleTitleA PII-like protein in Arabidopsis: Putative role in nitrogen sensing Proc Natl Acad Sci USA 95 13965–13970 Occurrence Handle10.1073/pnas.95.23.13965 Occurrence Handle9811909

    Article  PubMed  Google Scholar 

  • RJ Ireland PJ Lea (1999) The enzymes of glutamine, glutamate, asparagine, and aspartate metabolism BK Singh (Eds) Plant Amino Acids Biochemistry and Biotechnology Marcel Dekker, New York 49–109

    Google Scholar 

  • AJ Keys IF Bird MJ Cornelius PJ Lea RM Wallsgrove BJ Miflin (1978) ArticleTitlePhotorespiratory nitrogen cycle Nature 275 741–743 Occurrence Handle10.1038/275741a0 Occurrence Handle16069754

    Article  PubMed  Google Scholar 

  • JE King DJ Gifford (1997) ArticleTitleAmino acid utilization in seeds of loblolly pine during germination and early seedling growth I. Arginine and arginase activity. Plant Physiol 113 1125–1135 Occurrence Handle12223664

    PubMed  Google Scholar 

  • DL Lammer DJ Gifford (1989) ArticleTitleLodgepole Pine Seed-Germination 2 The seed proteins and their mobilization In the megagametophyte and embryonic axis. Can J Bot 67 2544–2551

    Google Scholar 

  • SD Lawrence JS Greenwood TE Korhnak JM Davis (1997) ArticleTitleA vegetative storage protein homolog is expressed in the growing shoot apex of hybrid poplar Planta 203 237–244 Occurrence Handle10.1007/s004250050187 Occurrence Handle9362569

    Article  PubMed  Google Scholar 

  • PJ Lea BG Forde (1994) ArticleTitleThe use of mutants and transgenic plants to study amino acid metabolism Plant Cell Environ 17 541–556

    Google Scholar 

  • PJ Lea BJ Miflin (2003) ArticleTitleGlutamate synthase and the synthesis of glutamate in plants Plant Physiol Biochem 41 555–564 Occurrence Handle10.1016/S0981-9428(03)00060-3

    Article  Google Scholar 

  • AM Limami C Rouillon G Glevarec A Gallais B Hirel (2002) ArticleTitleGenetic and physiological analysis of germination efficiency in maize in relation to nitrogen metabolism reveals the importance of cytosolic glutamine synthetase Plant Physiol 130 1860–1870 Occurrence Handle10.1104/pp.009647 Occurrence Handle12481069

    Article  PubMed  Google Scholar 

  • D Malaguti P Millard R Wendler A Hepburn M Tagliavini (2001) ArticleTitleTranslocation of amino acids in the xylem of apple (Malus domestica Borkh.) trees in spring as a consequence of both N remobilization and root uptake J Exp Bot 52 1665–1671 Occurrence Handle10.1093/jexbot/52.361.1665 Occurrence Handle11479331

    Article  PubMed  Google Scholar 

  • HS Mason JE Mullet (1990) ArticleTitleExpression of two soybean vegetative storage protein genes during development and in response to water deficit, wounding, and jasmonic acid. Plant Cell 2 569–579 Occurrence Handle10.1105/tpc.2.6.569 Occurrence Handle2152178

    Article  PubMed  Google Scholar 

  • R Melo-Oliveira IC Oliveira M-G Coruzzi (1996) ArticleTitleArabidopsis thaliana mutant analysis and gene regulation defines a non-redundant role for glutamate dehydrogenase in nitrogen assimilation Proc Natl Acad Sci USA 93 4718–4723 Occurrence Handle10.1073/pnas.93.10.4718 Occurrence Handle8643469

    Article  PubMed  Google Scholar 

  • EJ Mellerowicz M Baucher B Sundberg W Boerjan (2001) ArticleTitleUnravelling cell wall formation in the woody dicot stem Plant Mol Biol 47 239–274 Occurrence Handle10.1023/A:1010699919325 Occurrence Handle11554475

    Article  PubMed  Google Scholar 

  • BJ Miflin PJ Lea (1980) Ammonia assimilation BJ Miflin (Eds) The biochemistry of Plants Amino Acids and Their Derivatives Academic Press, New York 169–202

    Google Scholar 

  • P Millard R Wendler A Hepburn A Smith (1998) ArticleTitleVariations in the amino acid composition of xylem sap of Betula pendula Roth Trees due to remobilization of stored N in the spring. Plant Cell Environ 21 715–722 Occurrence Handle10.1046/j.1365-3040.1998.00313.x

    Article  Google Scholar 

  • KV Mijnsbrugge H Meyermans M Montagu Particlevan G Bauw W Boerjan (2000) ArticleTitleWood formation in poplar: identification, characterization, and seasonal variation of xylem proteins Planta 210 589–598 Occurrence Handle10.1007/s004250050048 Occurrence Handle10787052

    Article  PubMed  Google Scholar 

  • GBG Moorhead CS Smith (2003) ArticleTitleInterpreting the plastid carbon, nitrogen, and energy status A role for PII? Plant Physiol 133 492–498 Occurrence Handle10.1104/pp.103.025627 Occurrence Handle14555778

    Article  PubMed  Google Scholar 

  • J-M Mouillon S Aubert J Bourguignon E Gout R Douce F Rébeillé (1999) ArticleTitleGlycine and serine catabolism in non-photosynthetic higher plant cells: their role in C1 metabolism Plant J 20 197–205 Occurrence Handle10.1046/j.1365-313x.1999.00591.x Occurrence Handle10571879

    Article  PubMed  Google Scholar 

  • RT Mullen JE King DJ Gifford (1996) ArticleTitleChanges in mRNA populations during loblolly pine (Pinus taeda L.) seed stratification, germination, and post-germinative growth Physiol Plant 9 545–553 Occurrence Handle10.1034/j.1399-3054.1996.970318.x

    Article  Google Scholar 

  • A Ninfa M Atkinson (2000) ArticleTitlePII signal transduction proteins Trends Microbiol 8 172–179 Occurrence Handle10.1016/S0966-842X(00)01709-1 Occurrence Handle10754576

    Article  PubMed  Google Scholar 

  • M Obara T Sato T Yamaya (2001) ArticleTitleMapping of QTLs associated with cytosolic glutamine synthetase and NADH-glutamate synthase in rice (Oryza sativa L.) J Exp Bot 52 1209–1217 Occurrence Handle10.1093/jexbot/52.359.1209 Occurrence Handle11432939

    Article  PubMed  Google Scholar 

  • J Palomo F Gallardo MF Suárez FM Cánovas (1998) ArticleTitlePurification and characterization of NADP+-linked isocitrate dehydrogenase from Scots pine Evidence for different physiologigal roles of the enzyme in primary development. Plant Physiol 118 617–626 Occurrence Handle10.1104/pp.118.2.617 Occurrence Handle9765548

    Article  PubMed  Google Scholar 

  • A Pérez-García S Pereira J Pisarra A García-Gutiérrez F Cazorla R Salema A Vicente Particlede FM Cánovas (1998) ArticleTitleCytosolic localization in tomato mesophyll cells of a novel glutamine synthetase induced in response to bacterial infection or phosphinothricin treatment Planta 206 426–434 Occurrence Handle10.1007/s004250050418

    Article  Google Scholar 

  • J Pitel W Cheliak (1986) ArticleTitleEnzyme activities during imbibition and germination of seeds of tamarack (Larix laricina) Physiol Plant 67 562–569

    Google Scholar 

  • RA Razal S Ellis S Singh NG Lewis GHN Towers (1996) ArticleTitleNitrogen recycling in phenylpropanoid metabolism Phytochemistry 41 31–35 Occurrence Handle10.1016/0031-9422(95)00628-1

    Article  Google Scholar 

  • LS Roberts P Toivonen SM McInnis (1991) ArticleTitleDiscrete proteins associated with overwintering of interior spruce and douglas-fir seedlings Can J Bot 69 437–441

    Google Scholar 

  • S Roje H Wang SD McNeil RK Raymond DR Appling Y Shachar-Hilli HJ Bohnert AD Hanson (1999) ArticleTitleIsolation, characterization, and functional expression of cDNAs encoding NADH-dependent methylenetetrahydrofolate reductase from higher plants J Biol Chem 274 36089–36096 Occurrence Handle10.1074/jbc.274.51.36089 Occurrence Handle10593891

    Article  PubMed  Google Scholar 

  • S Schmidt G Stewart (1998) ArticleTitleTransport, storage and mobilization of nitrogen by trees and shrubs in the wet/dry topics of northern Australia Tree Physiol 18 403–410 Occurrence Handle12651365

    PubMed  Google Scholar 

  • A Schneider J Kreazwieser R Schums JJ Sauter H Rennenberg (1994) ArticleTitleThiol and amino acid composition of the xylem sap of poplar trees Can J Bot 72 347–351

    Google Scholar 

  • WL Schneider DJ Gifford (1994) ArticleTitleLoblolly pine seed dormancy I. The relationship between protein synthesis and the loss of dormancy. Physiol Plant 90 246–252 Occurrence Handle10.1034/j.1399-3054.1994.900202.x

    Article  Google Scholar 

  • CR Somerville WL Ogren (1980) ArticleTitleInhibition of photosynthesis in Arabidopsis mutants lacking leaf glutamate synthase activity Nature 286 257–259 Occurrence Handle10.1038/286257a0

    Article  Google Scholar 

  • V Stepien JJ Sauter F Martin (1994) ArticleTitleVegetative storage proteins in woody plants Plant Physiol Biochem 32 185–192

    Google Scholar 

  • F Sterky S Regan J Karlsson M Hertzberg A Rohde A Holmberg B Amini R Bhalerao M Larsson R Villarroel M Montagu Particlevan G Sandberg O Olsson TT Teeri W Boerjan P Gustafsson M Uhlén B Sundberg J Lundeberg (1998) ArticleTitleGene discovery in the wood-forming tissues of poplar: analysis of 5,692 expressed sequence tags Proc Natl Acad Sci USA 95 13330–13335 Occurrence Handle10.1073/pnas.95.22.13330 Occurrence Handle9789088

    Article  PubMed  Google Scholar 

  • H Stoerner B Seith U Hanemann E George H Rennenberg (1997) ArticleTitleNitrogen distribution in young Norway spruce (Picea abies) trees as affected by pedospheric nitrogen supply Physiol Plant 101 764–769 Occurrence Handle10.1034/j.1399-3054.1997.1010412.x

    Article  Google Scholar 

  • SL Stone DJ Gifford (1997) ArticleTitleStructural and biochemical changes in loblolly pine (Pinus taeda L.) seeds during germination and early seedling growth I. Storage protein reserves. Int J Plant Sci 158 727–737 Occurrence Handle10.1086/297484

    Article  Google Scholar 

  • MF Suárez C Avila F Gallardo FR Cantón A García-Gutiérrez MG Claros FM Cánovas (2002) ArticleTitleMolecular and enzymatic analysis of ammonium assimilation in woody plants J Exp Bot 53 891–904 Occurrence Handle10.1093/jexbot/53.370.891 Occurrence Handle11912232

    Article  PubMed  Google Scholar 

  • JS Titus S-M Kang (1982) ArticleTitleNitrogen metabolism, translocation and recycling in apple trees Hort Rev 4 204–246

    Google Scholar 

  • CD Todd DJ Gifford (2002) ArticleTitleThe role of the megagametophyte in maintaining loblolly pine (Pinus taeda L.) seedling arginase gene expression in vitro Planta 215 110–1181 Occurrence Handle10.1007/s00425-001-0720-2 Occurrence Handle12012247

    Article  PubMed  Google Scholar 

  • CD Todd DJ Gifford (2003) ArticleTitleLoblolly pine arginase responds to arginine in vitro Planta 217 610–615 Occurrence Handle10.1007/s00425-003-1022-7 Occurrence Handle12684785

    Article  PubMed  Google Scholar 

  • CD Todd JEK Cooke RT Mullen DJ Gifford (2001) ArticleTitleRegulation of loblolly pine (Pinus taeda L.) arginase in developing seedling tissue during germination and post-germinative growth Plant Mol Biol 45 555–565 Occurrence Handle10.1023/A:1010645616920 Occurrence Handle11414614

    Article  PubMed  Google Scholar 

  • K Mijnsbrugge ParticleVander M Montagu ParticleVan D Inze W Boerjan (1996) ArticleTitleTissue-specific expression conferred by the S-adenosyl-L-methionine synthetase promoter of Arabidopsis thaliana in transgenic poplar Plant Cell Physiol 37 1108–1115 Occurrence Handle9032966

    PubMed  Google Scholar 

  • K Mijnsbrugge ParticleVander H Meyermans M Montagu ParticleVan G Bauw W Boerjan (2000) ArticleTitleWood formation in poplar: identification, characterization, and seasonal variation of xylem proteins Planta 210 589–598 Occurrence Handle10.1007/s004250050048 Occurrence Handle10787052

    Article  PubMed  Google Scholar 

  • PS Heerden Particlevan GH Towers NG Lewis (1996) ArticleTitleNitrogen metabolism in lignifying Pinus taeda cell cultures J Biol Chem 271 12350–12355 Occurrence Handle10.1074/jbc.271.21.12350 Occurrence Handle8647837

    Article  PubMed  Google Scholar 

  • RM Wallsgrove JC Turner NP Hall AC Kendall SJW Bright (1987) ArticleTitleBarley mutants lacking chloroplast glutamine synthetase-biochemical and genetic analysis Plant Physiol 83 155–158

    Google Scholar 

  • A Weber U-I Flügge (2002) ArticleTitleInteraction of cytosolic and plastidic nitrogen metabolism in plants J Exp Bot 53 865–874 Occurrence Handle10.1093/jexbot/53.370.865 Occurrence Handle11912229

    Article  PubMed  Google Scholar 

  • R Whetten Y-H Sun R Sederoff (2001) ArticleTitleFunctional genomics and cell wall biosynthesis in loblolly pine Plant Mol Biol 47 275–291 Occurrence Handle10.1023/A:1010652003395 Occurrence Handle11554476

    Article  PubMed  Google Scholar 

  • T Yamaya M Obara H Nakajima S Sasaki T Hayakawa T Sato (2001) ArticleTitleGenetic manipulation and quantitative-trait loci mapping for nitrogen recycling in rice J Exp Bot 53 917–925 Occurrence Handle10.1093/jexbot/53.370.917

    Article  Google Scholar 

  • F Youssefi PH Brown SA Weinbaum (2000) ArticleTitleRelationship between tree nitrogen status, xylem and phloem sap amino acid concentrations, and apparent soil nitrogen uptake by almond trees (Prunus dulcis) J Hortic Sci Biotech 75 62–68

    Google Scholar 

  • R Zhong WH Morrison SuffixIII J Negrel Z-H Ye (1998) ArticleTitleDual methylation pathways in lignin biosynthesis Plant Cell 10 2033–2045 Occurrence Handle10.1105/tpc.10.12.2033 Occurrence Handle9836743

    Article  PubMed  Google Scholar 

Download references

Author information

Author notes

  1. María Fernanda Suárez

    Present address: Department of Plant Biology and Forest Genetics, Swedish University of Agricultural Sciences, Genetic Centre, Uppsala, Sweden, P.O. Box 7080, 75007

Authors and Affiliations

  1. Departamento de Biología Molecular y Bioquímica, Instituto Andaluz de Biotecnología, Unidad Asociada UMA-CSIC, Universidad de Málaga, Málaga, Spain, 29071

    Francisco R. Cantón & Francisco M. Cánovas

Authors
  1. Francisco R. Cantón
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. María Fernanda Suárez
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Francisco M. Cánovas
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Francisco M. Cánovas.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cantón, F.R., Suárez, M.F. & Cánovas, F.M. Molecular aspects of nitrogen mobilization and recycling in trees. Photosynth Res 83, 265–278 (2005). https://doi.org/10.1007/s11120-004-9366-9

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-004-9366-9

Keywords

Search

Navigation