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

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.