Abstract

Most plants living in tropical acid soils depend on the arbuscular mycorrhizal (AM) symbiosis for mobilizing low-accessible phosphorus (P), due to its strong bonding by iron (Fe) oxides. The roots release low-molecular-weight organic acids (LMWOAs) as a mechanism to increase soil P availability by ligand exchange or dissolution. However, little is known on the LMWOA production by AM fungi (AMF), since most studies conducted on AM plants do not discriminate on the LMWOA origin. This study aimed to determine whether AMF release significant amounts of LMWOAs to liberate P bound to Fe oxides, which is otherwise unavailable for the plant. Solanum lycopersicum L. plants mycorrhized with Rhizophagus irregularis were placed in a bicompartmental mesocosm, with P sources only accessible by AMF. Fingerprinting of LMWOAs in compartments containing free and goethite-bound orthophosphate (OP or GOE-OP) and phytic acid (PA or GOE-PA) was done. To assess P mobilization via AM symbiosis, P content, photosynthesis, and the degree of mycorrhization were determined in the plant; whereas, AM hyphae abundance was determined using lipid biomarkers. The results showing a higher shoot P content, along with a lower N:P ratio and a higher photosynthetic capacity, may be indicative of a higher photosynthetic P-use efficiency, when AM plants mobilized P from less-accessible sources. The presence of mono-, di-, and tricarboxylic LMWOAs in compartments containing OP or GOE-OP and phytic acid (PA or GOE-PA) points toward the occurrence of reductive dissolution and ligand exchange/dissolution reactions. Furthermore, hyphae grown in goethite loaded with OP and PA exhibited an increased content of unsaturated lipids, pointing to an increased membrane fluidity in order to maintain optimal hyphal functionality and facilitate the incorporation of P. Our results underpin the centrality of AM symbiosis in soil biogeochemical processes, by highlighting the ability of the AMF and accompanying microbiota in releasing significant amounts of LMWOAs to mobilize P bound to Fe oxides.

Highlights

  • Phosphorus (P) is an essential plant macronutrient (Schachtman et al, 1998), and its deficiency limits the plant growth in both natural and agricultural systems (Oberson et al, 2001)

  • All arbuscular mycorrhizal (AM) plants with access to a P source in the fungal compartment (FC) showed significantly larger P contents in the shoots compared to the roots (Figure 2)

  • We investigated the role of lowmolecular-weight organic acids (LMWOAs) secreted by AM fungi (AMF) and their accompanying microbiota in the mobilization of GOE-bound P sources

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Summary

Introduction

Phosphorus (P) is an essential plant macronutrient (Schachtman et al, 1998), and its deficiency limits the plant growth in both natural and agricultural systems (Oberson et al, 2001). The adsorption of LMWOAs is driven by positively charged oxide surfaces and the negative charge of the carboxylate group and is influenced by the formation of metal complexes in solution, with adsorption generally increasing with their concentration in solution and the number of carboxylic groups (Oburger et al, 2011; Adeleke et al, 2017). Tricarboxylic acids such as citrate have a higher efficiency to desorb P from Fe oxides than dicarboxylic or monocarboxylic ones (Geelhoed et al, 1999; Richardson, 2001)

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