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Plant function and evolutionary biology
RESEARCH ARTICLE

Carbon and nitrogen balance in beech roots under competitive pressure of soil-borne microorganisms induced by girdling, drought and glucose application

Jana B. Winkler A , Michael Dannenmann B , Judy Simon C , Rodica Pena D , Christine Offermann C , Wolfgang Sternad C , Christian Clemenz A , Pascale S. Naumann E , Rainer Gasche B , Ingrid Kögel-Knabner E , Arthur Gessler C , Heinz Rennenberg C and Andrea Polle D F
+ Author Affiliations
- Author Affiliations

A Helmholtz Zentrum München, Institute of Soil Ecology, Department of Environmental Engineering, Ingolstädter Landstraße 1, 85764 Neuherberg, Germany.

B Karlsruhe Institute of Technology, Forschungszentrum Karlsruhe GmbH, Institute for Meteorology and Climate Research, Atmospheric Environmental Research Division, Kreuzeckbahnstraße 19, 82467 Garmisch-Partenkirchen, Germany.

C Institute of Forest Botany and Tree Physiology, Chair of Tree Physiology, University of Freiburg, Georges-Koehler-Allee 53/54, 79110 Freiburg, Germany.

D Abteilung: Forstbotanik und Baumphysiologie, Büsgen-Institut, Georg-August Universität Göttingen, Büsgenweg 2, 37077 Göttingen, Germany.

E Lehrstuhl für Bodenkunde, Department für Ökologie und Ökosystemmanagement, Wissenschaftszentrum Weihenstephan, Technische Universität München, 85350 Freising-Weihenstephan, Germany.

F Corresponding author. Email: apolle@gwdg.de

Functional Plant Biology 37(9) 879-889 https://doi.org/10.1071/FP09309
Submitted: 29 December 2009  Accepted: 3 June 2010   Published: 24 August 2010

Abstract

The goal of this work was to increase the understanding of factors regulating nitrogen (N) competition between roots and soil microbes. For this purpose, root assimilate supply was diminished or abolished in beech (Fagus sylvatica L.) seedlings by girdling, drought stress or a combination of both factors. This was revealed by 13C tracer abundance in root tips after 13CO2 pulse labelling of the shoots. Analysis of different root tip fractions revealed that only 6% were ectomycorrhizal. Carbon (C) allocation to ectomycorrhizal and vital non-mycorrhizal root tips was ~26% higher than to distorted root tips. Drought resulted in ~30% increased ammonium (NH4+) and amino acid concentrations in roots and ~65% increased soil NH4+ concentrations, probably because of lower consumption of NH4+ by free-living microorganisms. Root uptake of glutamine of 13 nmol g–1 fresh mass h–1 decreased 2-fold with drought, although the number of vital root tips did not decrease. Carbon content in biomass of free-living microbes increased with glucose application regardless of drought, resulting in significant depletion in soil nitrate (NO3), root NH4+ and amino acid concentrations. Our results suggest that the root–soil system of young beech trees was C-limited, and this prevented amino acid metabolism in roots and microbial NO3 consumption in the soil, thereby exerting feedback inhibition on uptake of inorganic N by roots. We suggest that rhizodeposition is a key link in regulating the plant–microbial N balance.

Additional keywords: competition, ectomycorrhiza, Fagus sylvatica, microorganisms, root demography, stable isotopes.


Acknowledgements

We are grateful to the DFG (German Science Foundation) for financial support to the Beech Research Group (FOR 788) and acknowledge help with plant harvest, sample preparation or sample analyses by Dominik Dannenbauer, Jens Dyckmans, Merle Fastenrath, Peter Kary, Christine Kettner, Wolfgang Kornberger, Ursel Scheerer, Oliver Itzel, Michael Reichel and Sebastian Sippel.


References


Agerer R (1987–2006) ‘Colour atlas of ectomycorrhizae.’ (Einhorn Verlag + Druck GmbH: Schwäbisch Gmünd, Germany)

Allen EB, Allen MF, Helm DJ, Trappe JM, Molina R, Rincon E (1995) Patterns and regulation of mycorrhizal plant and fungal diversity. Plant and Soil 170, 47–62.
Crossref | GoogleScholarGoogle Scholar | open url image1

Andersen C, Nikolov I, Nikolova P, Matyssek R, Häberle KH (2005) Estimating ‘autotrophic’ below ground respiration in spruce and beech forests: decreases following girdling. European Journal of Forest Research 124, 155–163.
Crossref | GoogleScholarGoogle Scholar | open url image1

Bolte A, Czajkowski T, Kompa T (2007) The north-eastern distribution range of European beech – a review. Forestry 80, 413–429.
Crossref | GoogleScholarGoogle Scholar | open url image1

Booth MS, Stark JM, Rastetter E (2005) Controls on nitrogen cycling in terrestrial ecosystems: a synthetic analysis of literature data. Ecological Monographs 75, 139–157.
Crossref | GoogleScholarGoogle Scholar | open url image1

Borken W, Matzner E (2008) A reappraisal of drying and wetting effects on C and N mineralisation and fluxes in soils. Global Change Biology 14, 1–17. open url image1

Buée M, Vairelles D, Garbaye J (2005) Year-round monitoring of diversity and potential metabolic activity of the ectomycorrhizal community in a beech (Fagus silvatica) forest subjected to two thinning regimes. Mycorrhiza 15, 235–245.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Chang SC, Matzner E (2000) Soil nitrogen turn over in proximal and distal stem areas of European beech trees. Plant and Soil 218, 117–125.
Crossref | GoogleScholarGoogle Scholar | open url image1

Cochard H, Lemoine D, Dreyer E (1999) The effects of acclimation to sunlight on the xylem vulnerability to embolism in Fagus sylvatica L. Plant, Cell & Environment 22, 101–108.
Crossref | GoogleScholarGoogle Scholar | open url image1

Dannenmann M, Gasche R, Ledebuhr J, Papen H (2006) Effects of forest management on soil N cycling in beech forests stocking on calcareous soils. Plant and Soil 287, 279–300.
Crossref | GoogleScholarGoogle Scholar | open url image1

Dannenmann M, Simon J, Gasche R, Holst J, Naumann PS , et al. (2009) Tree girdling provides insight on the role of labile carbon in nitrogen partitioning between soil microorganisms and adult European beech. Soil Biology & Biochemistry 41, 1622–1631.
Crossref | GoogleScholarGoogle Scholar | open url image1

Druebert C, Lang C, Valtanen K, Polle A (2009) Beech carbon productivity as driver of ectomycorrhizal abundance and diversity. Plant, Cell & Environment 32, 992–1003.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Dučić T, Berthold D, Langenfeld-Heyser R, Beese F, Polle A (2009) Mycorrhizal communities in relation to biomass production and nutrient use efficiency in two varieties of Douglas fir (Pseudotsuga menziesii var. menziesii and var. glauca) in different forest soils. Soil Biology & Biochemistry 41, 742–753.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ford CR, Wurzburger N, Hendrick RL, Teskey RO (2007) Soil DIC uptake and fixation in Pinus taeda seedlings and its C contribution to plant tissues and ectomycorrhizal fungi. Tree Physiology 27, 375–383.
PubMed |
open url image1

Fotelli NM, Nahm M, Heidenfelder A, Papen H, Rennenberg H, Gessler A (2002) Soluble nonprotein nitrogen compounds indicate changes in the nitrogen status of beech seedlings due to climate and thinning. New Phytologist 154, 85–97.
Crossref | GoogleScholarGoogle Scholar | open url image1

Gessler A, Schneider S, von Sengbusch D, Weber P, Hanemann U, Huber C, Rothe A, Kreutzer K, Rennenberg H (1998a) Field and laboratory experiments on net uptake of nitrate and ammonium by roots of spruce (Picea abies) and beech (Fagus sylvatica) trees. New Phytologist 138, 275–285.
Crossref | GoogleScholarGoogle Scholar | open url image1

Gessler A, Schneider S, Weber P, Hanemann U, Rennenberg H (1998b) Soluble N compounds in trees exposed to high loads of N: a comparison between the roots of Norway spruce (Picea abies) and beech (Fagus sylvatica) trees. New Phytologist 138, 385–399.
Crossref | GoogleScholarGoogle Scholar | open url image1

Gessler A, Jung K, Gasche R, Papen H, Heidenfelder A, Metzler B, Börner E, Augustin S, Hildebrand E, Rennenberg H (2005) Climate and forest management influence nitrogen balance of European beech forests: Microbial N transformations and inorganic N net uptake capacity of mycorrhizal roots. European Journal of Forest Research 124, 95–111.
Crossref | GoogleScholarGoogle Scholar | open url image1

Giesler R, Högberg M, Strobel BW, Richter A, Nordgren A, Högberg P (2007) Production of dissolved organic carbon and low-molecular weight organic acids in soil solution driven by recent tree photosynthate. Biogeochemistry 84, 1–12.
Crossref | GoogleScholarGoogle Scholar | open url image1

Godbold DL, Hoosbeek MR, Lukac M, Cotrufo MF, Janssens IA , et al. (2006) Mycorrhizal hyphal turnover as a dominant process for carbon input into soil organic matter. Plant and Soil 281, 15–24.
Crossref | GoogleScholarGoogle Scholar | open url image1

Good AG, Zaplachinski ST (1994) The effects of drought stress on free amino acid accumulation and protein synthesis in Brassica napus. Physiologia Plantarum 90, 9–14.
Crossref | GoogleScholarGoogle Scholar | open url image1

Göttlicher SG, Steinmann K, Betson NR, Högberg P (2006) The dependence of soil microbial activity on rescent photosynthate from trees. Plant and Soil 287, 85–94.
Crossref | GoogleScholarGoogle Scholar | open url image1

Heinemeyer A, Hartley IP, Evans SP, Carreira de la Fuente JA, Ineson P (2007) Forest soil CO2 flux: uncovering the contribution and environmental responses of ectomycorrhizas. Global Change Biology 13, 1786–1797.
Crossref | GoogleScholarGoogle Scholar | open url image1

Högberg P, Read DJ (2006) Towards a more plant physiological perspective on soil ecology. Trends in Ecology & Evolution 21, 548–554.
Crossref | GoogleScholarGoogle Scholar | open url image1

Högberg P, Nordgren A, Buchmann N, Taylor AFS, Ekblad A, Högberg M, Nyberg G, Ottoson-Lövfnius M, Read DJ (2001) Large-scale forest girdling shows that current photosynthesis drives soil respiration. Nature 411, 789–792.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Jackson L, Burger M, Cavagnaro TR (2008) Roots, nitrogen tranformations and ecosystem services. Annual Review of Plant Biology 59, 341–363.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Langley JA, Chapman SK, Hungate BA (2006) Ectomycorrhizal colonization slows root decomposition: the post-mortem fungal legacy. Ecology Letters 9, 955–959.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lemoine D, Cochard H, Granier A (2002) Within crown variation in hydraulic architecture in beech (Fagus sylvatica L.): evidence for a stomatal control of xylem embolism. Annals of Forest Science 59, 19–27.
Crossref | GoogleScholarGoogle Scholar | open url image1

Lindahl BD, Ihrmark K, Boberg J, Trumbore SE, Högberg P, Stenlid J, Finlay RD (2007) Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest. New Phytologist 173, 611–620.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lipson DA, Raab TK, Schmidt SK, Monson RK (1999) Variation in competitive abilities of plants and microbes for specific amino acids. Biology and Fertility of Soils 29, 257–261.
Crossref | GoogleScholarGoogle Scholar | open url image1

Liu X-P, Grams TEE, Matyssek R, Rennenberg H (2005) Effects of elevated pCO2 and/or pO3 on C-, N-, and S-metabolites in the leaves of juvenile beech and spruce differ between trees grown in monoculture and mixed culture. Plant Physiology and Biochemistry 43, 147–154.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Löf M, Bolte A, Welander T (2005) Interacting effects of irradiance and water stress on dry weight and biomass partitioning in Fagus sylvatica seedlings. Scandinavian Journal of Forest Research 20, 322–328.
Crossref | GoogleScholarGoogle Scholar | open url image1

Matamala R, Gonzales-Meler MA, Jastrow J, Norby RJ, Schlesinger WH (2003) Impacts of fine root turnover on forest NPP and soil C sequestration potential. Science 302, 1385–1387.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Meier I, Leuschner C (2008) Belowground drought response of European beech: fine root biomass and carbon partitioning in 14 mature stands across a precipitation gradient. Global Change Biology 14, 2081–2095.
Crossref | GoogleScholarGoogle Scholar | open url image1

Näsholm T, Kielland K, Ganeteg U (2009) Uptake of organic nitrogen by plants. New Phytologist 182, 31–48.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Pena R, Offermann C, Simon J, Naumann PS, Geßler A , et al. (2010) Carbon limitations after girdling affect ectomycorrhizal diversity and reveal functional differences of EM community composition in a mature beech forest (Fagus sylvatica). Applied and Environmental Microbiology 76, 1831–1841.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Rennenberg H, Loreto L, Polle A, Brilli F, Fares S, Beniwal RS, Gessler A (2006) Physiological responses of forest trees to heat and drought. Plant Biology 8, 556–571.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ruehr NK, Offermann CA, Gessler A, Winkler JB, Ferrio JP, Buchmann N, Barnard RL (2009) Drought effects on allocation of recent carbon: from beech leaves to soil CO2 efflux. New Phytologist 184, 950–961.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Rumberger MD, Münzenberger B, Bens O, Ehrig F, Lentzsch P, Hüttl RF (2004) Changes in diversity and storage function of ectomycorrhiza and soil organoprofile dynamics after introduction of beech into Scots pine forests. Plant and Soil 264, 111–126.
Crossref | GoogleScholarGoogle Scholar | open url image1

Shi L, Guttenberger M, Kottke I, Hampp R (2002) The effect of drought on mycorrhiza of beech (Fagus sylvatica L.): change in community structure, and the content of carbohydrates and nitrogen storage bodies of the fungi. Mycorrhiza 12, 303–311.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Templer PH, Dawson TE (2004) Nitrogen uptake by four tree species of the Catskill Mountains, New York: implications for forest N dynamics. Plant and Soil 262, 251–261.
Crossref | GoogleScholarGoogle Scholar | open url image1

van der Heijden MGA, Bardgett RD, van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecology Letters 11, 296–310.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Vitousek P, Gosz JR, Grier CC, Melillo JM, Reiners WA, Todd RL (1979) Nitrate losses from disturbed ecosystems. Science 204, 469–474.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Wallander H, Arnebrant K, Ostrand F, Karén O (1997) Uptake of 15N-labelled alanine, ammonium and nitrate in Pinus sylvestris L. ectomycorrhiza growing in forest soil treated with nitrogen, sulphur or lime. Plant and Soil 195, 329–338.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wallenda T, Kottke I (1998) Nitrogen deposition and ectomycorrhizas. New Phytologist 139, 169–187.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wallenda T, Read DJ (1999) Kinetics of amino acid uptake by ectomycorrhizal roots. Plant, Cell & Environment 22, 179–187.
Crossref | GoogleScholarGoogle Scholar | open url image1

Winter H, Lohaus G, Heldt W (1992) Phloem transport of amino acids in relation to their cytosolic levels in barley leaves. Plant Physiology 99, 996–1004.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Zeleznik P, Hrenko M, Then C, Koch N, Grebenc T, Levanic T, Kraigher H (2007) CASIROZ: root parameters and types of ectomycorrhiza of young beeech plants exposed to different ozone and light regimes. Plant Biology 9, 298–308.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Zeller B, Liu J, Buchmann N, Richter A (2008) Tree girdling increases N mineralization in two spruce stands. Soil Biology & Biochemistry 40, 1155–1166.
Crossref | GoogleScholarGoogle Scholar | open url image1