Effect of variable phosphorus availability on root mechanisms involved in mobilization of the soil P in three lupine species

Abstract

Improving the soil phosphorus (P) acquisition efficiency by plants is one of the most important challenges for modern agriculture. Only 15-20% of this nutrient applied to the soil with fertilisers is used by plants, with the majority being converted to less available forms. Lupine species are a great genetic model system with significant potential to provide novel information. Here we present an investigation into the effects of variable availability in the rhizosphere on P-mobilising mechanisms and photosynthetic activity, studied in 12 varieties of three lupine species. P uptake was significantly stimulated by low molecular weight organic acid (OA) exudation and H⁺-ATPase-mediated proton transport in roots. The predominant mechanism in white lupine was the H⁺ release into the rhizosphere, OA exudation predominated in yellow lupine, while narrow-leaved lupine varieties used both strategies effectively. Three lupine species showed significant differences in the quantitative and qualitative composition of carboxylic acids in root exudates. The variable P availability in soil solution significantly affected the photosynthetic performance of the plants studied. At the same time, the activity of the photosynthetic electron transport chain and photosynthetic CO₂ assimilation was a key factor determining activity of the mechanisms involved in P mobilisation. We discuss the implications of these contrasting strategies for our understanding of tolerance to low P and in relation to breeding plants with higher P acquisition efficiency.

Keywords: H+-ATPase; Low-molecular-weight organic acids; Lupines; Phosphorus availability; Photosynthetic activity.

Fig. 1

The comparison of dry matter yield in varieties of three lupine species independent on P dose. The plants were supplemented with 0 (0P; control), 22 (1P), 44 (2P) and 88 (3P) mg kg⁻¹ of P. Data points represent the means ± SE (n = 16). The same letter denote homogenous groups after two-way ANOVA and Bonferroni post hoc test at p = 0.05.

Fig. 2

The effect of P dose on dry matter yield in Lupine varieties. The plants were supplemented with 0 (0P; control), 22 (1P), 44 (2P) and 88 (3P) mg kg⁻¹ of P. Data points represent the means ± SE (n = 4). The same letter denote homogenous groups after two-way ANOVA and Bonferroni post hoc test at p = 0.05.

Fig. 3

The comparison of shoot P content in varieties of three lupine species independent on P dose. The plants were supplemented with 0 (0P; control), 22 (1P), 44 (2P) and 88 (3P) mg kg⁻¹ of P. Data points represent the means ± SE (n = 16). The same letter denote homogenous groups after two-way ANOVA and Bonferroni post hoc test at p = 0.05.

Fig. 4

The effect of P dose on shoot P content in Lupine varieties. The plants were supplemented with 0 (0P; control), 22 (1P), 44 (2P) and 88 (3P) mg kg⁻¹ of P. Data points represent the means ± SE (n = 4). The same letter denote homogenous groups after two-way ANOVA and Bonferroni post hoc test at p = 0.05.

Fig. 5

The phosphorus use efficiency in L. angustifolius, L. albus and L. luteus independent on P dose (a), and in lupine species in relation to P dose (b). The plants were supplemented with 0 (0P; control), 22 (1P), 44 (2P) and 88 (3P) mg kg⁻¹ of P. Bars represent the means ± SE. The same letters denote homogeneous groups for: species (a) n = 64 and interaction P dose × species (b) n = 16, after two-way ANOVA and Bonferroni post hoc test at p = 0.05.

Fig. 6

The content of low molecular weight organic acids in the root exudates collected from varieties of narrow-leafed (a), white (b) and yellow (c) lupines, grown under variable P supplementation: citric acid, malic acid, acetic acid and succinic acid. The plants were supplemented with 0 (0P; control), 22 (1P), 44 (2P) and 88 (3P) mg kg⁻¹ of P. Data points represent the means ± SE (n = 4). The same letter denote homogenous groups (interaction P dose × variety) within species after two-way ANOVA and Bonferroni post hoc test at p = 0.05.

Fig. 7

The hydrolytic activity of H⁺-ATPase () and the H⁺-ATPase-mediated proton efflux () in roots of narrow-leafed (a), white (b) and yellow (c) lupines, grown under variable P supplementation. The plants were supplemented with 0 (0P; control), 22 (1P), 44 (2P) and 88 (3P) mg kg⁻¹ of P. The values of the H⁺/ATP coupling ratio are presented in brackets. Data points represent the means ± SE (n = 4). The same letter denote homogenous groups (interaction P dose × variety) within species after two-way ANOVA and Bonferroni post hoc test at p = 0.05.

Fig. 8

Photosynthetic parameters: the maximum PSII efficiency (Fv/Fm), the actual photochemical efficiency (ΦPSII), the nonphotochemical quenching (NPQ), and the CO₂ assimilation rate (A), measured in leaves of narrow-leafed (a-d), white (e–h) and yellow (i-l) lupines. The plants were supplemented with 0 (0P; control), 22 (1P), 44 (2P) and 88 (3P) mg kg⁻¹ of P. Data points represent the means ± SE (n = 4). The letters denoting homogeneous groups after two-way ANOVA and Bonferroni post hoc test are omitted for a clear view.

Fig. 9

Changes in the intracellular concentration of adenosine triphosphate in roots of narrow-leafed (a), white (b) and yellow (c) lupines, grown under variable P supplementation. The plants were supplemented with 0 (0P; control), 22 (1P), 44 (2P) and 88 (3P) mg kg⁻¹ of P. Data points represent the means ± SE (n = 4). The letters denoting homogeneous groups after two-way ANOVA and Bonferroni post hoc test are omitted for a clear view.

Fig. 10

Regression analysis for the relationship between the level of organic acid exudation (a–c), H⁺-ATPase-mediated proton efflux (d–f) and P concentration in soil solutions; and the relationship between the level of organic acid exudation (g–i), H⁺-ATPase-mediated proton efflux (j–l), and photosynthetic rate. The coefficients of determination (R²) and curve fitting were determined using the data from all treatments (p < 0.05).

Fig. 11

Principal component analysis (PCA) of eight traits in varieties of three lupine species in response to different P availability (Low—22, Medium—44, High—88 mg supplemented P kg⁻¹) relative to the control. Biplot vectors are trait factor loadings, whereas the position of individual varieties is shown in triangles (L. angustifolius), diamonds (L. albus) and squares (L. luteus). Trait abbreviations: shoot dry mass yield (DM), the H⁺-ATPase-mediated proton efflux in roots (H⁺ efflux), the organic acid exudation in roots (OA), the Pi concentration in the soil solution (P_i), P uptake in plants, mg pot⁻¹ (Puptake), shoot P concentration, mg g⁻¹ (Pconc), P acquisition efficiency (PAE), P uptake efficiency (PUpE).