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Carbon allocation in ectomycorrhizal plants at limited and optimal N supply: an attempt at unraveling conflicting theories

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Abstract

With regard to mycorrhiza, conflicting theories try to explain how the balance between fungal demand for carbohydrates and the plant’s needs for nutrients varies, resulting in conflicting predictions. In order to evaluate current concepts, we investigated some metabolic parameters, which are indicative for plant carbon allocation in response to mycorrhization at limited and optimal N supply. Pinus pinaster seedlings were inoculated with living or dead (control) cultures of Pisolithus tinctorius, supplied with ammonium at 4 (limiting) or 7% d−1 (non-limiting) N relative addition rate (RARN), and followed development for 29 days. Mycorrhizal colonization of roots was quantified by the determination of ergosterol. A series of enzymes (sucrose and trehalose metabolism, anaplerosis) and metabolites (soluble carbohydrate, including trehalose; fructose 2,6 bisphosphate, free amino acids) relevant in the C/N exchange between symbionts, and in the carbon allocation and sink strength within the plant were assayed for 2-day-intervals for up to 14 days, and at 5-day-intervals for the rest of the experiment. The first 10 days reflected the establishment of mycorrhizal interaction, and the carbon allocation to the root was higher in M plants independent of N supply. Following this period, carbon allocation became N-related, higher at low, and lower at high N supply. The belowground C investment of M plants was dependent on N availability, but not on N gain. Finally, increased belowground C allocation was accompanied by a shift from plant to fungal metabolism.

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Abbreviations

ECM:

ectomycorrhizae

PEPc:

phosphoenolpyruvate carboxylase

SS:

sucrose synthase

TSC:

total soluble carbohydrates

FAA:

free amino acids

M:

mycorrhizal

NM:

non-mycorrhizal

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Acknowledgments

We are indebted to Dr. Luisa Loura for statistical advice, to Dr. Harald Stransky (University of Tübingen) for the analysis of amino acids, and the CENASEF, for the generous supply of the seeds used in this work. This work was funded by a PRAXIS XXI fellowship grant BD no. 3119 / 2000.

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Authors and Affiliations

  1. Universidade de Lisboa, Faculdade de Ciências, Centro de Biologia Aplicada, Campo Grande C2. Piso 4, 1749-016, Lisbon, Portugal

    Ana Corrêa & Maria-Amélia Martins-Loução

  2. Departamento de Microbiología del Suelo y Sistemas Simbióticos, Estación Experimental del Zaidín, CSIC, Profesor Albareda 1, 18008, Granada, Spain

    Ana Corrêa

  3. Physiological Ecology of Plants, University of Tübingen, Auf der Morgenstelle 1, 72076, Tübingen, Germany

    Rüdiger Hampp

  4. Department of Wood Science / Wood Biology, University of Hamburg, Leuschnerstr. 91, 21031, Hamburg, Germany

    Elisabeth Magel

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  1. Ana Corrêa
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  2. Rüdiger Hampp
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  3. Elisabeth Magel
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  4. Maria-Amélia Martins-Loução
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Correspondence to Ana Corrêa.

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Table S1

Root, shoot and whole plant relative dry weight of M and NM plants that were supplied with a nutrient solution with NH4 + as N source, at 7%d-1 or 4%d-1 RARN. Values are averages ± S.E. A one-way ANOVA, considering as independent variable the combination of the variables mycorrhization, N supply and time, followed by a Tukey test, was used to test for significant differences between treatments at each time (p < 0.05). Letters stand for statistically significant differences at each time (DOC 44 kb)

Table S2

Root, shoot and whole plant relative growth rate (RGR), calculated between days 0 and 29, of M and NM plants that were supplied with a nutrient solution with NH4 + as N source, at 7%d-1 or 4%d-1 RARN. Values are averages ± S.E. A two-way ANCOVA was used to test for the effects of mycorrhization (Myc) and N supply (Nut) on the different parameters measured in this study, using the age of the plant as covariate, at p < 0.05. A one-way ANOVA, considering as independent variable the combination of the variables mycorrhization, N supply and time, followed by a Tukey test, was used to test for significant differences between treatments at each time, at p < 0.05. Letters stand for statistically significant differences at each time (DOC 38 kb)

Table S3

Net photosynthesis rate (A) of M and NM plants that were supplied with a nutrient solution with NH4 + as N source, at 7%d-1 or 4%d-1 RARN. Values are averages ± S.E. A two-way ANCOVA was used to test for the effects of mycorrhization (Myc) and N supply (Nut) on the different parameters measured in this study, using the age of the plant as covariate, at p < 0.05. A one-way ANOVA, considering as independent variable the combination of the variables mycorrhization, N supply and time, followed by a Tukey test, was used to test for significant differences between treatments at each time, at p < 0.05. Letters stand for statistically significant differences at each time (DOC 34 kb)

Figure S1

Shoot starch concentration of M plants as a percentage of NM plants. The plants were fed a nutrient solution with NH4 + as N source, at 7%d-1 (closed circles) or 4%d-1 (open circles) RARN. P1: early mycorrhizal establishment phase; P2: post-establishment phase. All values are averages ± S.E. (n = 4 × 2–3). Asterisks stand for significant differences on each day, at p < 0.05 (DOC 14 kb)

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Corrêa, A., Hampp, R., Magel, E. et al. Carbon allocation in ectomycorrhizal plants at limited and optimal N supply: an attempt at unraveling conflicting theories. Mycorrhiza 21, 35–51 (2011). https://doi.org/10.1007/s00572-010-0309-3

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