Carbon trading for phosphorus gain: the balance between rhizosphere carboxylates and arbuscular mycorrhizal symbiosis in plant phosphorus acquisition

Abstract

Two key plant adaptations for phosphorus (P) acquisition are carboxylate exudation into the rhizosphere and mycorrhizal symbioses. These target different soil P resources, presumably with different plant carbon costs. We examined the effect of inoculation with arbuscular mycorrhizal fungi (AMF) on amount of rhizosphere carboxylates and plant P uptake for 10 species of low-P adapted Kennedia grown for 23 weeks in low-P sand. Inoculation decreased carboxylates in some species (up to 50%), decreased plant dry weight (21%) and increased plant P content (23%). There was a positive logarithmic relationship between plant P content and the amount of rhizosphere citric acid for inoculated and uninoculated plants. Causality was indicated by experiments using sand where little citric acid was lost from the soil solution over 2 h and citric acid at low concentrations desorbed P into the soil solution. Senesced leaf P concentration was often low and P-resorption efficiencies reached >90%. In conclusion, we propose that mycorrhizally mediated resource partitioning occurred because inoculation reduced rhizosphere carboxylates, but increased plant P uptake. Hence, presumably, the proportion of plant P acquired from strongly sorbed sources decreased with inoculation, while the proportion from labile inorganic P increased. Implications for plant fitness under field conditions now require investigation.

Plant adaptations to severely phosphorus-impoverished soils

“…When a large fraction of total soil P is sorbed, carboxylate-releasing strategies are desirable. Some species use this strategy when non-mycorrhizal, suppressing it when inoculated by mycorrhizas [67], showing there is no sharp boundary between mycorrhizal and carboxylatereleasing species. Cluster roots are likely the very best strategy when P is very poorly available.…”

Variation in phosphorus acquisition efficiency among maize varieties as related to mycorrhizal functioning

“…In rice it was shown that the ability of varieties to acquire Zn through the mycorrhizal pathway was negatively correlated with (and hence traded off against) the ability to acquire Zn in the non-mycorrhizal condition (Gao et al 2007). The same negative correlation and trade-off was found for members of the genus Kennedia (Ryan et al 2012). It has been demonstrated that there are architectural tradeoffs between adventitious and basal roots (Walk et al 2006;Zhu and Lynch 2004).…”

“…Such a trade-off has been reported for rice, where increased Zn uptake through organic anions and through the mycorrhizal symbiosis could not be stacked (Gao et al 2012). Downregulation of organic anion production in the genus Kennedia in the mycorrhizal condition also suggests a trade-off (Ryan et al 2012). However, Lynch (2007) suggested that root hairs and the symbiosis with AMF could be combined and do not show a trade-off.…”

Citrate and malonate increase microbial activity and alter microbial community composition in uncontaminated and diesel-contaminated soil microcosms

“…Carboxylates may act as bio-stimulating agents in the degradation of PHCs through the provision of a labile carbon source that supports increased microbial growth and activity. When added to soils, carboxylates are rapidly degraded by soil microorganisms, with up to 80 % mineralized to CO 2 within 24 h, depending upon the carboxylate added and the soil type (Evans, 1998;Ström et al, 2001;Hashimoto, 2007;Oburger et al, 2009;Fujii et al, 2010;Ryan et al, 2012). In addition, carboxylates have the capacity to enhance soil phosphorus supply and, hence, microbial growth and activity through phosphate desorption either due to anion exchange or their ability to chelate to metal cations (e.g., Al 3+ , Fe 3+ and Ca 2+ ) (Jones and Darrah, 1994;Ryan et al, 2001;Shane and Lambers, 2005).…”