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Nitrogen fertilisation reduces sink strength of poplar ectomycorrhizae during recovery after drought more than phosphorus fertilisation

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Abstract

Background and aims

Drought reduces the carbon (C) flux from leaves (source) to mycorrhizal roots (sink); however, during recovery from drought, C flux exceeds the levels observed in irrigated controls. This process could be source- or sink-controlled. We studied this source–sink relationship in an agronomically used poplar clone grown at different levels of nitrogen (N) and phosphorus (P) fertilisation as used in silvoarable agroforestry systems.

Methods

We conducted a fully factorial pot experiment combining four fertiliser and two drought regimes. Gas exchange and chlorophyll and flavonol indices were regularly monitored. One week after rewatering, we performed 13CO2 pulse labelling. At harvest, enzyme activities of ectomycorrhizal root tips were determined.

Results

After one week of recovery, we observed an excess in C allocation to ectomycorrhizae (ECM) in non-N-fertilised treatments. However, net photosynthesis only recovered to the level of continuously irrigated controls. Drought increased chitinase, cellulase, phosphatase and peptidase activities, but the latter only in N-fertilised treatments.

Conclusions

We add evidence that the allocation of recently assimilated C is most likely sink-controlled. Less C allocation to recovering ECM supplied with fertiliser may be either due to better nutritional status and hence higher stress tolerance, or due to partitioning between above and below-ground sinks.

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References

  • Abuzinadah R, Read D (1988) Amino acids as nitrogen sources for ectomycorrhizal fungi: utilization of individual amino acids. Trans Br Mycol Soc 91:473–479

    Article  CAS  Google Scholar 

  • Agerer R (1991) 2 Characterization of Ectomycorrhiza. In: Norris DJRJR, Varma AK (eds) Methods in microbiology. Academic Press

  • Arnold TM, Schultz JC (2002) Induced sink strength as a prerequisite for induced tannin biosynthesis in developing leaves of Populus. Oecologia 130:585–593

    Article  PubMed  Google Scholar 

  • Bidartondo MI, Ek H, Wallander H, Söderström B (2001) Do nutrient additions alter carbon sink strength of ectomycorrhizal fungi? New Phytol 151:543–550

    Article  CAS  Google Scholar 

  • Brix H, Arias CA, del Bubba M (2001) Media selection for sustainable phosphorus removal in subsurface flow constructed wetlands. Water Sci Technol 44:47–54

    CAS  PubMed  Google Scholar 

  • Brodribb TJ, McAdam SA (2011) Passive origins of stomatal control in vascular plants. Science 331:582–585

    Article  CAS  PubMed  Google Scholar 

  • Browne P, Rice O, Miller SH, Burke J, Dowling DN, Morrissey JP, O’Gara F (2009) Superior inorganic phosphate solubilization is linked to phylogeny within the Pseudomonas fluorescens complex. Appl Soil Ecol 43:131–138

    Article  Google Scholar 

  • van den Burg J (1985) Foliar analysis for determination of tree nutrient status - a compilation of literature data. Rapport Rijksinstituut voor Onderzoek in de Bos-en Landschapsbouw De Dorschkamp, Netherlands

    Google Scholar 

  • Cartelat A, Cerovic ZG, Goulas Y, Meyer S, Lelarge C, Prioul JL, Barbottin A, Jeuffroy MH, Gate P, Agati G, Moya I (2005) Optically assessed contents of leaf polyphenolics and chlorophyll as indicators of nitrogen deficiency in wheat (Triticum aestivum L.) Field Crop Res 91:35–49

    Article  Google Scholar 

  • Cerovic ZG, Masdoumier G, Ghozlen NB, Latouche G (2012) A new optical leaf-clip meter for simultaneous non-destructive assessment of leaf chlorophyll and epidermal flavonoids. Physiol Plant 146:251–260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chalot M, Brun A (1998) Physiology of organic nitrogen acquisition by ectomycorrhizal fungi and ectomycorrhizas. FEMS Microbiol Rev 22:21–44

    Article  CAS  PubMed  Google Scholar 

  • Chalot M, Brun A, Finlay RD, Söderström B (1994) Metabolism of [14C] glutamate and [14C] glutamine by the ectomycorrhizal fungus Paxillus involutus. Microbiology 140:1641–1649

    Article  CAS  Google Scholar 

  • Conry M, Hogan J (2001) Comparison of cereals grown under high (conventional) and low (reduced) inputs systems. Teagasc, Crops Research Centre, Carlow

  • Costa L, Faustino LI, Graciano C (2016) The spatial distribution of phosphate in the root system modulates N metabolism and growth in Eucalyptus grandis young plants. Trees:1–11

  • Danielson RM (1984) Ectomycorrhiza formation by the Operculate Discomycete Sphaerosporella brunnea (Pezizales). Mycologia 76:454–461

    Article  Google Scholar 

  • Diedhiou AG, Dupouey J-L, Buée M, Dambrine E, Laüt L, Garbaye J (2010) The functional structure of ectomycorrhizal communities in an oak forest in central France witnesses ancient Gallo-Roman farming practices. Soil Biol Biochem 42:860–862

    Article  CAS  Google Scholar 

  • Dunham RJ, Nye PH (1976) The influence of soil water content on the uptake of ions by roots. III. Phosphate, potassium, calcium and magnesium uptake and concentration gradients in soil. J Appl Ecol 13:967–984

    Article  CAS  Google Scholar 

  • Field CB (2012) Managing the risks of extreme events and disasters to advance climate change adaptation: special report of the intergovernmental panel on climate change. Cambridge University Press

  • Finlay RD (2008) Ecological aspects of mycorrhizal symbiosis: with special emphasis on the functional diversity of interactions involving the extraradical mycelium. J Exp Bot 59:1115–1126

    Article  CAS  PubMed  Google Scholar 

  • Frossard E, Condron LM, Oberson A, Sinaj S, Fardeau JC (2000) Processes governing phosphorus availability in temperate soils. J Environ Qual 29:15–23

    Article  CAS  Google Scholar 

  • Garnier E, Laurent G, Bellmann A, Debain S, Berthelier P, Ducout B, Roumet C, Navas ML (2001) Consistency of species ranking based on functional leaf traits. New Phytol 152:69–83

    Article  Google Scholar 

  • Gessler A, Schaub M, McDowell NG (2016) The role of nutrients in drought-induced tree mortality and recovery. New Phytol 214:513–520

    Article  PubMed  Google Scholar 

  • Graciano C, Tambussi EA, Castán E, Guiamet JJ (2009) Dry mass partitioning and nitrogen uptake by Eucalyptus grandis plants in response to localized or mixed application of phosphorus. Plant Soil 319:175–184

    Article  CAS  Google Scholar 

  • Greenway H, Hughes PG, Klepper B (1969) Effects of water deficit on phosphorus nutrition of tomato plants. Physiol Plant 22:199–207

    Article  CAS  Google Scholar 

  • Guillemot J, Martin-StPaul N, Dufrêne E, François C, Soudani K, Ourcival J, Delpierre N (2015) The dynamic of the annual carbon allocation to wood in European tree species is consistent with a combined source–sink limitation of growth: implications for modelling. Biogeosciences 12:2773–2790

    Article  Google Scholar 

  • Hagedorn F, Joseph J, Peter M, Luster J, Pritsch K, Geppert U, Kerner R, Molinier V, Egli S, Schaub M, Liu J-F, Li M, Sever K, Weiler M, Siegwolf RTW, Gessler A, Arend M (2016) Recovery of trees from drought depends on belowground sink control. Nat Plants 2:16111

    Article  PubMed  Google Scholar 

  • Handa S, Handa AK, Hasegawa PM, Bressan RA (1986) Proline accumulation and the adaptation of cultured plant cells to water stress. Plant Physiol 80:938–945

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hartmann H, Trumbore S (2016) Understanding the roles of nonstructural carbohydrates in forest trees–from what we can measure to what we want to know. New Phytol 211:386–403

    Article  CAS  PubMed  Google Scholar 

  • Hayes JE, Simpson RJ, Richardson AE (2000) The growth and phosphorus utilisation of plants in sterile media when supplied with inositol hexaphosphate, glucose 1-phosphate or inorganic phosphate. Plant Soil 220:165–174

    Article  CAS  Google Scholar 

  • Herzog C, Peter M, Pritsch K, Gunthardt-Goerg MS, Egli S (2013) Drought and air warming affects abundance and exoenzyme profiles of Cenococcum geophilum associated with Quercus robur, Q. petraea and Q. pubescens. Plant Biol 15:230–237

    Article  CAS  PubMed  Google Scholar 

  • Ibrahim L, Proe MF, Cameron AD (1997) Main effects of nitrogen supply and drought stress upon whole-plant carbon allocation in poplar. Can J For Res 27:1413–1419

    Article  Google Scholar 

  • Jones MD, Twieg BD, Ward V, Barker J, Durall DM, Simard SW (2010) Functional complementarity of Douglas-fir ectomycorrhizas for extracellular enzyme activity after wildfire or clearcut logging. Funct Ecol 24:1139–1151

    Article  Google Scholar 

  • Jug A, Hofmann-Schielle C, Makeschin F, Rehfuess KE (1999) Short-rotation plantations of balsam poplars, aspen and willows on former arable land in the Federal Republic of Germany. II. Nutritional status and bioelement export by harvested shoot axes. For Ecol Manag 121:67–83

    Article  Google Scholar 

  • Jung V, Violle C, Mondy C, Hoffmann L, Muller S (2010) Intraspecific variability and trait-based community assembly. J Ecol 98:1134–1140

    Article  Google Scholar 

  • Kelly JM, Ericsson T (2003) Assessing the nutrition of juvenile hybrid poplar using a steady state technique and a mechanistic model. Forest Ecol Manag 180:249–260

    Article  Google Scholar 

  • Kjøller A H and Struwe S 2002 Fungal communities, succession, enzymes, and decomposition. Enezymes in the environment: activity, ecology, and applications. CRC Press

  • Körner C (2003) Carbon limitation in trees. J Ecol 91:4–17

    Article  Google Scholar 

  • Körner C (2015) Paradigm shift in plant growth control. Curr Opin Plant Biol 25:107–114

    Article  PubMed  Google Scholar 

  • Kumar V, Bolland MDA, Gilkes RJ (1994) Comparison of the Pi, Colwell, Bray 1, calcium acetate lactate (CAL) and Truog soil phosphorus test for predicting growth of oats, barley, triticale and clover in the field in lateritic soils fertilised with superphosphate and rock phosphate. Fertilizer Res 37:115–124

    Article  CAS  Google Scholar 

  • LeBauer DS, Treseder KK (2008) Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89:371–379

    Article  PubMed  Google Scholar 

  • Liu F, Andersen MN, Jacobsen S-E, Jensen CR (2005) Stomatal control and water use efficiency of soybean (Glycine max L. Merr.) during progressive soil drying. Environ Exp Bot 54:33–40

    Article  CAS  Google Scholar 

  • Maracchi G, Sirotenko O, Bindi M (2005) Impacts of present and future climate variability on agriculture and forestry in the temperate regions: Europe. Clim Chang 70:117–135

    Article  CAS  Google Scholar 

  • Martin F, Canet D (1986) Biosynthesis of amino acids during [13C] glucose utilization by the ectomycorrhizal ascomycete Cenococcum geophilum monitored by 13C nuclear magnetic resonance. Physiol Vég 24:209–218

    CAS  Google Scholar 

  • Martin F, Ramstedt M, Söderhäll K, Canet D (1988) Carbohydrate and amino acid metabolism in the ectomycorrhizal ascomycete Sphaerosporella brunnea during glucose utilization: a 13C NMR study. Plant Physiol 86:935–940

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McDowell N, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T, Plaut J, Sperry J, West A, Williams DG (2008) Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytol 178:719–739

    Article  PubMed  Google Scholar 

  • McNeil SD, Nuccio ML, Hanson AD (1999) Betaines and related osmoprotectans. Targets for metabolic engineering of stress resistance. Plant Physiol 120:945–949

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muller B, Pantin F, Génard M, Turc O, Freixes S, Piques M, Gibon Y (2011) Water deficits uncouple growth from photosynthesis, increase C content, and modify the relationships between C and growth in sink organs. J Exp Bot 62:1715–1729

    Article  CAS  PubMed  Google Scholar 

  • Nelsen CE, Safir GR (1982) Increased drought tolerance of mycorrhizal onion plants caused by improved phosphorus nutrition. Planta 154:407–413

    Article  CAS  PubMed  Google Scholar 

  • Neville J, Tessier JL, Morrison I, Scarratt J, Canning B, Klironomos JN (2002) Soil depth distribution of ecto- and arbuscular mycorrhizal fungi associated with Populus tremuloides within a 3-year-old boreal forest clear-cut. Appl Soil Ecol 19:209–216

    Article  Google Scholar 

  • Perez-Moreno J, Read D (2000) Mobilization and transfer of nutrients from litter to tree seedlings via the vegetative mycelium of ectomycorrhizal plants. New Phytol 145:301–309

    Article  CAS  Google Scholar 

  • Pinheiro J, Bates D, DebRoy S and Sarkar D 2014 R Core Team (2014) nlme: linear and nonlinear mixed effects models. R package veersion 3.1-117. See http://www.CRANR-projectorg/package=nlme

  • Pitman M (1981) Ion uptake. Physiology and biochemistry of drought resistance in plants Academic Press, New York, pp 71–96

    Google Scholar 

  • Pou A, Flexas J, Alsina M d M, Bota J, Carambula C, De Herralde F, Galmés J, Lovisolo C, Jiménez M, Ribas-Carbó M (2008) Adjustments of water use efficiency by stomatal regulation during drought and recovery in the drought-adapted Vitis hybrid Richter-110 (V. berlandieri × V. rupestris). Physiol Plant 134:313–323

    Article  CAS  PubMed  Google Scholar 

  • Pritsch K, Garbaye J (2011) Enzyme secretion by ECM fungi and exploitation of mineral nutrients from soil organic matter. Ann For Sci 68:25–32

    Article  Google Scholar 

  • Pritsch K, Courty PE, Churin J-L, Cloutier-Hurteau B, Ali MA, Damon C, Duchemin M, Egli S, Ernst J, Fraissinet-Tachet L, Kuhar F, Legname E, Marmeisse R, Mueller A, Nikolova P, Peter M, Plassard C, Richard F, Schloter M, Selosse M-A, Franc A, Garbaye J (2011) Optimized assay and storage conditions for enzyme activity profiling of ectomycorrhizae. Mycorrhiza 21:589–600

    Article  CAS  PubMed  Google Scholar 

  • R Core Team 2016 R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/

  • Ramulu USS, Pratt PF, Page AL (1967) Phosphorus fixation by soils in relation to extractable iron oxides and mineralogical Composition1. Soil Sci Soc Am J 31:193–196

    Article  CAS  Google Scholar 

  • Reisner Y, de Filippi R, Herzog F, Palma J (2007) Target regions for silvoarable agroforestry in Europe. Ecol Eng 29:401–418

    Article  Google Scholar 

  • Rhodes D, Handa S, Bressan RA (1986) Metabolic changes associated with adaptation of plant cells to water stress. Plant Physiol 82:890–903

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rineau F, Garbaye J (2009) Does forest liming impact the enzymatic profiles of ectomycorrhizal communities through specialized fungal symbionts? Mycorrhiza 19:493

    Article  CAS  PubMed  Google Scholar 

  • Russell EW (1973) Soil conditions and plant growth, 10th edn. Longman, London

    Google Scholar 

  • Sala A, Woodruff DR, Meinzer FC (2012) Carbon dynamics in trees: feast or famine? Tree Physiol 32:764–775

    Article  CAS  PubMed  Google Scholar 

  • Smith SE, Read DJ (2010) Mycorrhizal symbiosis. Academic press, San Diego

    Google Scholar 

  • Tibbett M, Sanders F (2002) Ectomycorrhizal symbiosis can enhance plant nutrition through improved access to discrete organic nutrient patches of high resource quality. Ann Bot 89:783–789

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • VDLUFA (1991) The examination of soils. Book of methods no. I, chapter 6.1.4.1. VDLUFA-Press, Darmstadt

  • Vierheilig H, Coughlan AP, Wyss U, Piché Y (1998) Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Appl Environ Microbiol 64:5004–5007

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wendland M, Diepolder M and Capriel P 2014 Leitfaden für die Düngung von Acker-und Grünland: gelbes Heft. LfL

  • Wu F, Bao W, Li F, Wu N (2008) Effects of drought stress and N supply on the growth, biomass partitioning and water-use efficiency of Sophora davidii seedlings. Environ Exp Bot 63:248–255

    Article  CAS  Google Scholar 

  • Yancey PH, Clark ME, Hand SC, Bowlus RD, Somero GN (1982) Living with water stress: evolution of osmolyte systems. Science 217:1214–1222

    Article  CAS  PubMed  Google Scholar 

  • Yin C, Peng Y, Zang R, Zhu Y, Li C (2005) Adaptive responses of Populus kangdingensis to drought stress. Physiol Plant 123:445–451

    Article  CAS  Google Scholar 

  • Zhang X, Zang R, Li C (2004) Population differences in physiological and morphological adaptations of Populus davidiana seedlings in response to progressive drought stress. Plant Sci 166:791–797

    Article  CAS  Google Scholar 

  • Zhu H, Dancik BP, Higginbotham KO (1994) Regulation of extracellular proteinase production in an ectomycorrhizal fungus Hebeloma crustuliniforme. Mycologia 86:227–234

    Article  CAS  Google Scholar 

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Acknowledgements

The authors wish to thank two anonymous reviewers, the handling editor and Diethart Matthies (Philipps University of Marburg) for valuable comments to improve the manuscript, Tatjana Gartner for measurements in the greenhouse, Peter Kary for technical support, Peter Grill for analysis of leaf phosphorus content. The plant material was kindly provided by Karolina Faust from the Bavarian Office for Forestal Seed and Plant Breeding (ASP).

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Nickel, U.T., Winkler, J.B., Mühlhans, S. et al. Nitrogen fertilisation reduces sink strength of poplar ectomycorrhizae during recovery after drought more than phosphorus fertilisation. Plant Soil 419, 405–422 (2017). https://doi.org/10.1007/s11104-017-3354-2

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