Cluster-root formation and carboxylate release in three Lupinus species as dependent on phosphorus supply, internal phosphorus concentration and relative growth rate

Abstract

Background and aims: Some Lupinus species produce cluster roots in response to low plant phosphorus (P) status. The cause of variation in cluster-root formation among cluster-root-forming Lupinus species is unknown. The aim of this study was to investigate if cluster-root formation is, in part, dependent on different relative growth rates (RGRs) among Lupinus species when they show similar shoot P status.

Methods: Three cluster-root-forming Lupinus species, L. albus, L. pilosus and L. atlanticus, were grown in washed river sand at 0, 7·5, 15 or 40 mg P kg(-1) dry sand. Plants were harvested at 34, 42 or 62 d after sowing, and fresh and dry weight of leaves, stems, cluster roots and non-cluster roots of different ages were measured. The percentage of cluster roots, tissue P concentrations, root exudates and plant RGR were determined.

Key results: Phosphorus treatments had major effects on cluster-root allocation, with a significant but incomplete suppression in L. albus and L. pilosus when P supply exceeded 15 mg P kg(-1) sand. Complete suppression was found in L. atlanticus at the highest P supply; this species never invested more than 20 % of its root weight in cluster roots. For L. pilosus and L. atlanticus, cluster-root formation was decreased at high internal P concentration, irrespective of RGR. For L. albus, there was a trend in the same direction, but this was not significant.

Conclusions: Cluster-root formation in all three Lupinus species was suppressed at high leaf P concentration, irrespective of RGR. Variation in cluster-root formation among the three species cannot be explained by species-specific variation in RGR or leaf P concentration.

Keywords: Cluster roots; L. atlanticus; L. pilosus; Lupinus albus; net assimilation rate; phosphorus acquisition; relative growth rate.

Fig. 1.

(A–C) Total plant dry biomass of Lupinus atlanticus, L. albus and L. pilosus supplied with either 0, 7·5, 15 or 40 mg P kg⁻¹ sand in the form of KH₂PO₄, harvested at 34, 42 or 62 d after sowing. Error bars represent the s.e. (n = 4, with the exception of L. pilosus at day 62, n = 3). Treatment means marked with the same lower case letter are not significantly different within each group using a two-way ANOVA for each harvest followed by Duncan's multiple test (P ≤ 0·05).

Fig. 2.

(A–C) Percentage of cluster roots formed on lateral roots, based on total root dry mass, of Lupinus atlanticus, L. albus and L. pilosus supplied with 0, 7·5, 15 or 40 mg P kg⁻¹ sand in the form of KH₂PO₄, harvested at 34, 42 or 62 d after sowing. The percentages were calculated from the dry mass of cluster roots divided by total root dry mass. Error bars represent the s.e. (n = 4). Treatment means marked with the same lower case letter are not significantly different within each group using a one-way ANOVA for each harvest followed by Duncan's multiple test (P ≤ 0·05).

Fig. 3.

Relationship between percentage of cluster roots as compared with total roots (based on dry mass) and P concentration in recently fully expanded leaves (RFELs) for three Lupinus species at day 62. The solid lines indicate significant regressions (P ≤ 0·05).

Fig. 4.

Relationship between percentage of cluster roots as compared with total roots (based on dry mass) at day 62 and relative growth rate (RGR; between day 42 and day 62) of Lupinus albus, L. pilosus and L. atlanticus. The broken line indicates a non-significant regression; solid lines indicate significant regressions (P ≤ 0·05).

Fig. 5.

Relationship between percentage of cluster roots of total roots (based on dry mass) and both P concentration in recently fully expanded leaves (RFELs) on day 62 and relative growth rate (RGR; between day 42 and day 62) of Lupinus albus, L. pilosus and L. atlanticus. n.s. indicates a non-significant regression; ***(P ≤ 0·001) and *(P ≤ 0·05) indicate significant regressions.

Fig. 6.

Concentration of carboxylates in the rhizosphere of Lupinus atlanticus, L. albus and L. pilosus supplied with 0, 7·5, 15 or 40 mg P kg⁻¹ sand in the form of KH₂PO₄, harvested at (A) 34, (B) 42 or (C) 62 d after sowing. Error bars represent the s.e. (n = 4). Treatment means marked with the same lower case letter are not significantly different within each group using a one-way ANOVA for each harvest followed by Duncan's multiple test (P ≤ 0·05); means with no letters marked are not significant.

Fig. 7.

Phosphorus (P) concentration of expanding, recently fully expanded and mature leaves of Lupinus atlanticus, L. albus and L. pilosus at (A) 34, (B) 42 and (C) 62 d after sowing; and (D) P concentration of senesced leaves, stems, cluster roots and non-cluster roots at day 62 supplied with either 0, 7·5, 15 or 40 mg P kg⁻¹ sand in the form of KH₂PO₄. Error bars represent the s.e. (n = 4). Treatment means marked with the same lower case letter are not significantly different within each organ group using a one-way ANOVA for each tissue for all the harvests followed by Duncan's multiple test (P ≤ 0·05).

Fig. 8.

Interaction between cluster-root formation, plant phosphorus (P) uptake, shoot P status and relative growth rate (RGR). Positive effects are depicted as solid black lines, and negative effects as solid light grey lines. Cluster roots increase the P uptake rate, which stimulates plant growth and increases the plant P status. Contrary to our expectations, cluster-root investment does not correlate with RGR.