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Arbuscular mycorrhizal fungus colonization in Nicotiana tabacum decreases the rate of both carboxylate exudation and root respiration and increases plant growth under phosphorus limitation

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Abstract

Background and aims

Under phosphorus (P) limitation, plants tend to maximize their efficiency of P acquisition by increasing the exudation of root carboxylates, such as citrate, whose synthesis is mediated by respiration via the alternative oxidase (AOX) in cluster roots. However, high respiratory costs related to nutrient uptake are associated with slower plant growth, whereas arbuscular mycorrhizal (AM) fungus colonization increases plant growth and decreases the exudation of citrate and malate. Thus, the present research is based on the hypothesis that AM fungus colonization will decrease root respiration via the alternative pathway and the amount of carboxylates in the rhizosphere, and increase plant growth.

Methods

We used the oxygen-isotope-fractionation technique to study the in vivo respiratory activities of the cytochrome and the alternative oxidase pathways (COP and AOP) in AM and nonmycorrhizal (NM) tobacco plants grown under P-sufficient (0.25 mM) and P-limiting (0.025 mM) conditions in sand. The amount of root exudates in the rhizosphere, total biomass and root P content were determined.

Results

Under sufficient P, the amount of citrate and malate was higher in NM plants, while no differences were found in respiration between NM and AM plants. On the other hand, low P increases the exudation of citrate and respiration via AOP in NM plants, while it does not affect the amount of carboxylates, nor the respiratory rate in AM plants. Biomass production was reduced only in NM plants under low P.

Conclusions

Our results highlight that AM fungus colonization decreases the rate of root respiration and the exudation of citrate and malate, whilst increasing plant growth. Conversely, respiration, via AOX, is associated with the exudation of citrate and less biomass production in NM roots.

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Abbreviations

ATP:

Adenosine triphosphate

AOX:

Alternative oxidase

AOP:

Alternative oxidase pathway

v alt :

Alternative pathway activity

AM:

Arbuscular mycorrhiza

AMF:

Arbuscular mycorrhizal fungi

Valt :

Capacity of the alternative pathway

COX:

Cytochrome oxidase

COP:

Cytochrome oxidase pathway

v cyt :

Cytochrome pathway activity

NM:

Non- Arbuscular mycorrhiza

Vt :

Total respiration

TCA:

Tricarboxylic acid cycle

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Acknowledgements

This work was financed by the MICINN - projects BFU2011-23294 and CTM2014-53902-C2-1-P. We would like to thank Juan Camilo Moreno for providing Nicotiana tabacum L. cv Petit Havanna seeds, Biel Martorell for his technical help on the IRMS, Amparo Salido Ruiz for her technical help on the ICP-OES, and Miquel Truyols and collaborators of the UIB Experimental Field and Greenhouses which are supported by the UIBGrant 15/2015.

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Authors and Affiliations

  1. Grup de Recerca en Biologia de les Plantes en Condicions Mediterranies, Departament de Biologia, Universitat de les Illes Balears, Carretera de Valldemossa Km 7.5, 07122, Palma de Mallorca, Spain

    Néstor Fernández Del-Saz, Antonia Romero-Munar, Elena Baraza, Jaume Flexas & Miquel Ribas-Carbó

  2. School of Plant Biology and Institute of Agriculture, University of Western Australia, 35 Stirling Highway, Crawley (Perth), WA, 6009, Australia

    Gregory R. Cawthray & Hans Lambers

  3. Department of Soil Microbiology and Symbiotic Systems, Estación Experimental del Zaidín-Consejo Superior de Investigaciones Científicas (EEZ-CSIC), Profesor Albareda 1, 18008, Granada, Spain

    Ricardo Aroca

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  1. Néstor Fernández Del-Saz
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  2. Antonia Romero-Munar
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  3. Gregory R. Cawthray
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  4. Ricardo Aroca
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  5. Elena Baraza
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  6. Jaume Flexas
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  7. Hans Lambers
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  8. Miquel Ribas-Carbó
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Correspondence to Miquel Ribas-Carbó.

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Del-Saz, N.F., Romero-Munar, A., Cawthray, G.R. et al. Arbuscular mycorrhizal fungus colonization in Nicotiana tabacum decreases the rate of both carboxylate exudation and root respiration and increases plant growth under phosphorus limitation. Plant Soil 416, 97–106 (2017). https://doi.org/10.1007/s11104-017-3188-y

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