Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Supplying nitrate before bud break induces pronounced changes in nitrogen nutrition and growth of young poplars

Suraphon Thitithanakul A B C , Gilles Pétel A B , Michel Chalot D E and François Beaujard A B F
+ Author Affiliations
- Author Affiliations

A INRA, UMR547 PIAF, F-63039 Clermont-Ferrand, France.

B Université de Clermont-Ferrand, Université Blaise Pascal, UMR547 PIAF, BP 10448, F-63000 Clermont-Ferrand, France.

C Faculty of Science and Industrial Technology, Prince of Songkla University, Surat Thani Campus, Muang Surat Thani 84100, Thailand.

D UMR CNRS 6249 Université de Franche-Comté, Place Leclerc, 25030 Besançon, France.

E Université de Lorraine, Faculté des Sciences and Technologies, 54506 Vandoeuvre-les-Nancy cedex, France.

F Corresponding author. Email: francois.beaujard@clermont.inra.fr

Functional Plant Biology 39(9) 795-803 https://doi.org/10.1071/FP12129
Submitted: 25 April 2012  Accepted: 12 July 2012   Published: 15 August 2012

Abstract

Tree nutrient research concentrated on endogenous C and N remobilisation in spring has neglected to acknowledge the possibilities of significant effects of N uptake before bud break, especially on the quality of regrowth and N reserve remobilisation. To investigate this subject, experimental studies were performed on young poplars (Populus tremula × Populus alba, clone INRA 717–1B4) grown with a controlled nutrient supply: (i) without N, ‘control’; (ii) N supplied throughout the course of the experiment, ‘N-supply’; and (iii) N supplied only before bud break, ‘N-pulse’. Results confirm the hypothesis that poplar scions can significantly take up nitrate before bud break, amounting to ~34% of the total N stored the previous year. After bud break, emerging leaves restart the sap flow, which increased nitrate uptake to support the regrowth. N-pulse and N-supply treatments were found to have significant effects shortly after a growth period, i.e. by increasing N content of all tissues (e.g. 37 and 81% in new shoots respectively), leaf area (18 and 29%) and specific leaf area (20 and 35%). Therefore, results confirm the hypothesis that early N supply plays a significant role in the N status and N remobilisation involved in the spring regrowth of young trees.

Additional keywords: absorption, nitrogen, Poplar, regrowth, remobilisation, spring.


References

Ameglio T, Bodet C, Lacointe A, Cochard H (2002) Winter embolism, mechanisms of xylem hydraulic conductivity recovery and springtime growth patterns in walnut and peach trees. Tree Physiology 22, 1211–1220.
Winter embolism, mechanisms of xylem hydraulic conductivity recovery and springtime growth patterns in walnut and peach trees.Crossref | GoogleScholarGoogle Scholar |

Baker JM, Van Bavel CHM (1987) Measurement of mass flow of water in the stems of herbaceous plants. Plant, Cell & Environment 10, 777–782.

Bausenwein U, Millard P, Thornton B, Raven JA (2001) Seasonal nitrogen storage and remobilization in the forb Rumex acetosa. Functional Ecology 15, 370–377.
Seasonal nitrogen storage and remobilization in the forb Rumex acetosa.Crossref | GoogleScholarGoogle Scholar |

Beaujard F, Hunault G (1996) An original approach to study the kinetics of mineral element uptake for some woody species. Acta Horticulturae 435, 243–253.

Cheng LL, Fuchigami LH (2002) Growth of young apple trees in relation to reserve nitrogen and carbohydrates. Tree Physiology 22, 1297–1303.
Growth of young apple trees in relation to reserve nitrogen and carbohydrates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXit1Shsw%3D%3D&md5=b455a298afe58d3836d09bb33002787aCAS |

Cooke JEK, Martin TA, Davis JM (2005) Short-term physiological and developmental responses to nitrogen availability in hybrid poplar. New Phytologist 167, 41–52.
Short-term physiological and developmental responses to nitrogen availability in hybrid poplar.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmtl2nsbo%3D&md5=335affcc7028acfe8382f0c3a18c16f0CAS |

Couturier J, Doidy J, Guinet F, Wipf D, Blaudez D, Chalot M (2010) Glutamine, arginine and the amino acid transporter Pt-CAT11 play important roles during senescence in poplar. Annals of Botany 105, 1159–1169.
Glutamine, arginine and the amino acid transporter Pt-CAT11 play important roles during senescence in poplar.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnvVOqt7Y%3D&md5=19c17307ca7da488069167d95ffa5330CAS |

Delaire M (2005) Variations de la capacité d’absorption minérale par les racines du jeune Acer pseudoplatanus, L. (Acéracées) consécutives à l’histoire nutritionnelle récente et ancienne de la plante. PhD, Université d’Angers, Thesis no. 676.

Dickson RE (1989) Carbon and nitrogen allocation in trees. Annals of Forest Science 46, 631s–647s.
Carbon and nitrogen allocation in trees.Crossref | GoogleScholarGoogle Scholar |

Dluzniewska P, Gessler A, Kopriva S, Strnad M, Novak O, Dietrich H, Rennenberg H (2006) Exogenous supply of glutamine and active cytokinin to the roots reduces NO3 – uptake rates in poplar. Plant, Cell & Environment 29, 1284–1297.
Exogenous supply of glutamine and active cytokinin to the roots reduces NO3 uptake rates in poplar.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XnsVGjsrw%3D&md5=7a1152ddc2c4416cc70f8cfbe96e2551CAS |

Dong SF, Scagel CF, Cheng LL, Fuchigami LH, Rygiewicz PT (2001) Soil temperature and plant growth stage influence nitrogen uptake and amino acid concentration of apple during early spring growth. Tree Physiology 21, 541–547.
Soil temperature and plant growth stage influence nitrogen uptake and amino acid concentration of apple during early spring growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXksFams7k%3D&md5=1d6469271947c873299004b01dc21b9cCAS |

Dong SF, Cheng LL, Scagel CF, Fuchigami LH (2004) Nitrogen mobilization, nitrogen uptake and growth of cuttings obtained from poplar stock plants grown in different N regimes and sprayed with urea in autumn. Tree Physiology 24, 355–359.
Nitrogen mobilization, nitrogen uptake and growth of cuttings obtained from poplar stock plants grown in different N regimes and sprayed with urea in autumn.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXislyiu7g%3D&md5=9d9e0d8b5a992e2db73c003a03ae7682CAS |

Dyckmans J, Flessa H (2001) Influence of tree internal N status on uptake and translocation of C and N in beech: a dual 13C and 15N labeling approach. Tree Physiology 21, 395–401.
Influence of tree internal N status on uptake and translocation of C and N in beech: a dual 13C and 15N labeling approach.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38%2FgslygsA%3D%3D&md5=34432ac7fbf30aba6a2362093e40c5aeCAS |

El Zein R, Bréda N, Gérant D, Zeller B, Maillard P (2011a) Nitrogen sources for current-year shoot growth in 50-year-old sessile oak trees: an in situ 15N labeling approach. Tree Physiology 31, 1390–1400.
Nitrogen sources for current-year shoot growth in 50-year-old sessile oak trees: an in situ 15N labeling approach.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xit1ykt7o%3D&md5=f1065f760c64ed3d0356e426804d476aCAS |

El Zein R, Maillard P, Bréda N, Marchand J, Montpied P, Gérant D (2011b) Seasonal changes of C and N non-structural compounds in the stem sapwood of adult sessile oak and beech trees. Tree Physiology 31, 843–854.
Seasonal changes of C and N non-structural compounds in the stem sapwood of adult sessile oak and beech trees.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlansL7E&md5=a878bd7bbe0c080bf976e0c1d8f4177aCAS |

Ewers FW, Ameglio T, Cochard H, Beaujard F, Martignac M, Vandame M, Bodet C, Cruiziat P (2001) Seasonal variation in xylem pressure of walnut trees: root and stem pressures. Tree Physiology 21, 1123–1132.
Seasonal variation in xylem pressure of walnut trees: root and stem pressures.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MrjsV2rtw%3D%3D&md5=5d8abd32ae49efe04ac05393102ac2dbCAS |

Frak E, Millard P, Le Roux X, Guillaumie S, Wendler R (2002) Coupling sap flow velocity and amino acid concentrations as an alternative method to 15N labeling for quantifying nitrogen remobilization by walnut trees. Plant Physiology 130, 1043–1053.
Coupling sap flow velocity and amino acid concentrations as an alternative method to 15N labeling for quantifying nitrogen remobilization by walnut trees.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XotVKnurw%3D&md5=8bce38b9db9c2dbb5087ae786448f708CAS |

Galopin G, Beaujard F, Gendraud M (1996) Intensive production of juvenile cuttings by mother microplant culture in hydrangea macrophylla ‘Leuchtfeuer’. Canadian Journal of Botany 74, 561–567.
Intensive production of juvenile cuttings by mother microplant culture in hydrangea macrophylla ‘Leuchtfeuer’.Crossref | GoogleScholarGoogle Scholar |

Gessler A, Kopriva S, Rennenberg H (2004) Regulation of nitrate uptake at the whole-tree level: interaction between nitrogen compounds, cytokinins and carbon metabolism. Tree Physiology 24, 1313–1321.

Grassi G, Millard P, Wendler R, Minotta G, Tagliavini M (2002) Measurement of xylem sap amino acid concentrations in conjunction with whole-tree transpiration estimates spring N remobilization by cherry (Prunus avium L.) trees. Plant, Cell & Environment 25, 1689–1699.
Measurement of xylem sap amino acid concentrations in conjunction with whole-tree transpiration estimates spring N remobilization by cherry (Prunus avium L.) trees.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXislCjtA%3D%3D&md5=0e48dc09801c7cd0619023398c0f0de3CAS |

Grassi G, Millard P, Gioacchini P, Tagliavini M (2003) Recycling of nitrogen in the xylem of Prunus avium trees starts when spring remobilization of internal reserves declines. Tree Physiology 23, 1061–1068.
Recycling of nitrogen in the xylem of Prunus avium trees starts when spring remobilization of internal reserves declines.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXptVCitbs%3D&md5=214e2205519c1d6891edbef76cbeaac0CAS |

Guak S, Neilsen D, Millard P, Wendler R, Neilsen GH (2003) Determining the role of N remobilization for growth of apple (Malus domestica Borkh.) trees by measuring xylem-sap N flux. Journal of Experimental Botany 54, 2121–2131.
Determining the role of N remobilization for growth of apple (Malus domestica Borkh.) trees by measuring xylem-sap N flux.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXns1Slu7g%3D&md5=dc34f1e07b94578f4e655d24163cc348CAS |

Guérin V, Huche-Thelier L, Charpentier S (2007) Mobilisation of nutrients and transport via the xylem sap in a shrub (Ligustrum ovalifolium) during spring growth: N and C compounds and interactions. Journal of Plant Physiology 164, 562–573.
Mobilisation of nutrients and transport via the xylem sap in a shrub (Ligustrum ovalifolium) during spring growth: N and C compounds and interactions.Crossref | GoogleScholarGoogle Scholar |

Imsande J, Touraine B (1994) N demand and the regulation of nitrate uptake. Plant Physiology 105, 3–7.

Landhäusser SM, Lieffers VJ (2003) Seasonal changes in carbohydrate reserves in mature northern Populus tremuloides clones. Trees – Structure and Function 17, 471–476.
Seasonal changes in carbohydrate reserves in mature northern Populus tremuloides clones.Crossref | GoogleScholarGoogle Scholar |

Malaguti D, Millard P, Wendler R, Hepburn A, Tagliavini M (2001) Translocation of amino acids in the xylem of apple (Malus domestica Borkh.) trees in spring as a consequence of both N remobilization and root uptake. Journal of Experimental Botany 52, 1665–1671.
Translocation of amino acids in the xylem of apple (Malus domestica Borkh.) trees in spring as a consequence of both N remobilization and root uptake.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlvVClsrk%3D&md5=2497a51647ee98187f54020ff8bfdc78CAS |

Marmann P, Wendler R, Millard P, Heilmeier H (1997) Nitrogen storage and remobilization in ash (Fraxinus excelsior) under field and laboratory conditions. Trees – Structure and Function 11, 298–305.
Nitrogen storage and remobilization in ash (Fraxinus excelsior) under field and laboratory conditions.Crossref | GoogleScholarGoogle Scholar |

Millard P, Grelet GA (2010) Nitrogen storage and remobilization by trees: ecophysiological relevance in a changing world. Tree Physiology 30, 1083–1095.
Nitrogen storage and remobilization by trees: ecophysiological relevance in a changing world.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFKhtLbL&md5=e9acc49de64322bad9236e0683b8e88fCAS |

Millard P, Wendler R, Grassi G, Grelet GA, Tagliavini M (2006) Translocation of nitrogen in the xylem of field-grown cherry and poplar trees during remobilization. Tree Physiology 26, 527–536.
Translocation of nitrogen in the xylem of field-grown cherry and poplar trees during remobilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjslOltLw%3D&md5=e47aa10d140dffc09d6a199dc43d1cb9CAS |

Miller AJ, Fan XR, Shen QR, Smith SJ (2008) Amino acids and nitrate as signals for the regulation of nitrogen acquisition. Journal of Experimental Botany 59, 111–119.
Amino acids and nitrate as signals for the regulation of nitrogen acquisition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1Sitbc%3D&md5=ac0b6ceef2ca51148332fe3bcf95a9d1CAS |

Reich PB, Ellsworth DS, Walters MB (1998) Leaf structure (specific leaf area) modulates photosynthesis–nitrogen relations: evidence from within and across species and functional groups. Functional Ecology 12, 948–958.
Leaf structure (specific leaf area) modulates photosynthesis–nitrogen relations: evidence from within and across species and functional groups.Crossref | GoogleScholarGoogle Scholar |

Ripullone F, Grassi G, Lauteri M, Borghetti M (2003) Photosynthesis-nitrogen relationships: interpretation of different patterns between Pseudotsuga menziesii and Populus × euroamericana in a mini-stand experiment. Tree Physiology 23, 137–144.
Photosynthesis-nitrogen relationships: interpretation of different patterns between Pseudotsuga menziesii and Populus × euroamericana in a mini-stand experiment.Crossref | GoogleScholarGoogle Scholar |

Sakuratani T (1984) Improvement of the probe for measuring water flow rate in intact plants with the stem heat balance method. Journal of Agricultural Meteorology 40, 273–277.
Improvement of the probe for measuring water flow rate in intact plants with the stem heat balance method.Crossref | GoogleScholarGoogle Scholar |

Salaün M, Guérin V, Huché-Thélier L, Charpentier S, Dily FL (2005) Nitrogen storage and mobilisation for spring growth in Ligustrum cultivated in container. Scientia Horticulturae 103, 461–471.
Nitrogen storage and mobilisation for spring growth in Ligustrum cultivated in container.Crossref | GoogleScholarGoogle Scholar |

Sauter JJ, Vancleve B (1994) Storage, mobilization and Interrelations of starch, sugars, protein and fat in the ray storage tissue of poplar trees. Trees – Structure and Function 8, 297–304.
Storage, mobilization and Interrelations of starch, sugars, protein and fat in the ray storage tissue of poplar trees.Crossref | GoogleScholarGoogle Scholar |

Tagliavini M, Quartieri M, Millard P (1997) Remobilised nitrogen and root uptake of nitrate for spring leaf growth, flowers and developing fruits of pear (Pyrus communis L.) trees. Plant and Soil 195, 137–142.
Remobilised nitrogen and root uptake of nitrate for spring leaf growth, flowers and developing fruits of pear (Pyrus communis L.) trees.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXnt1Oqt7Y%3D&md5=af6beb2f38a8f067c906728cac430609CAS |

Ter Steege MW, Stulen I, Wiersema PK, Posthumus F, Vaalburg W (1999) Efficiency of nitrate uptake in spinach: impact of external nitrate concentration and relative growth rate on nitrate influx and efflux. Plant and Soil 208, 125–134.
Efficiency of nitrate uptake in spinach: impact of external nitrate concentration and relative growth rate on nitrate influx and efflux.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXltFGisb4%3D&md5=65643c35017e591ebb3b3ac42e8eebdcCAS |

Valancogne C, Nasr Z (1989) Measuring sap flow in the stem of small trees by a heat balance method. HortScience 24, 383–385.

van den Driessche R, Thomas BR, Kamelchuk DP (2008) Effects of N, NP, and NPKS fertilizers applied to four-year-old hybrid poplar plantations. New Forests 35, 221–233.
Effects of N, NP, and NPKS fertilizers applied to four-year-old hybrid poplar plantations.Crossref | GoogleScholarGoogle Scholar |

Vizoso S, Gerant D, Guehl JM, Joffre R, Chalot M, Gross P, Maillard P (2008) Do elevation of CO2 concentration and nitrogen fertilization alter storage and remobilization of carbon and nitrogen in pedunculate oak saplings? Tree Physiology 28, 1729–1739.
Do elevation of CO2 concentration and nitrogen fertilization alter storage and remobilization of carbon and nitrogen in pedunculate oak saplings?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVOqsrvI&md5=5dd0d669eed5158ac82b3925fd267062CAS |

Wong BL, Baggett KL, Rye AH (2003) Seasonal patterns of reserve and soluble carbohydrates in mature sugar maple (Acer saccharum). Canadian Journal of Botany 81, 780–788.
Seasonal patterns of reserve and soluble carbohydrates in mature sugar maple (Acer saccharum).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXptFKitrk%3D&md5=727edf3ff43562ec4fd57b7aaa4ed905CAS |

Yin CY, Pang XY, Chen K (2009) The effects of water, nutrient availability and their interaction on the growth, morphology and physiology of two poplar species. Environmental and Experimental Botany 67, 196–203.
The effects of water, nutrient availability and their interaction on the growth, morphology and physiology of two poplar species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtV2qs7vN&md5=e221a33dab67526c6acab37e274f4f84CAS |