Manganese modulates the responses of nitrogen-supplied and Rhizobium-nodulated Phaseolus vulgaris L. to inoculation with arbuscular mycorrhizal fungi

In Venezuela, low yields of black bean crops are attributed, in part, to the low manganese (Mn) and phosphorus (P) contents in the Quartzipsamment soils where this crop is usually sown. To test this hypothesis, black bean plants were grown in sterilized sand to simulate soil physical properties, were fertilized with increasing Mn concentrations (0.1–20 μM) and inoculated with a commercial mixture of Rhizobium leguminosarum bv phaseoli strains 127K44, 127K89, 127K105 (+Rh), in combination with arbuscular mycorrhizal fungi Scutellospora heterogama and Entrophospora colombiana (+AMF). Non-inoculated plants fertilized with 6 mM NO3 and 2 mM P served as controls. Plants were harvested at 18, 25, 33, and 40 days after emergence. At all harvests, the greatest growth and highest P and iron (Fe) leaf concentrations occurred in control plants grown in 5 μM Mn. The growth of +AMF plants was promoted at 0.1 μM Mn and inhibited at higher than 1 μM Mn. Whereas, concentrations of 5–10 μM Mn enhanced the growth and the Mn concentrations in leaves of +Rh plants 40 days after emergence. The tripartite symbiosis (+Rh+AMF) decreased growth, nodulation and leaf ureide and chlorophyll concentrations in plants grown in less than 20 μM Mn, imputed to severe ultrastructural alterations in the leaf and nodule tissues. Only +Rh+AMF plants grown in 20 μM Mn were effectively nodulated, AMF colonized and reached the flowering stage, although with diminished growth and low chlorophyll concentrations. Results confirm the high Mn requirement of +Rh plants for growth and nodulation and question the implementation of the tripartite symbiosis to improve yields in early flowering black bean varieties planted in soils deficient in Mn and P.

Graphical abstractIn Venezuela, low yields of black bean crops are attributed, in part, to the low manganese (Mn) and phosphorus (P) contents in the Quartzipsamment soils where this crop is usually sown. To test this hypothesis, black bean plants were grown in sterilized sand to simulate soil physical properties, were fertilized with increasing Mn concentrations (0.1–20 μM) and inoculated with a commercial mixture of Rhizobium leguminosarum bv phaseoli (+Rh), in combination with arbuscular mycorrhizal fungi Scutellospora heterogama and Entrophospora colombiana (+AMF). Results indicate that +Rh black beans require much higher levels of Mn that plants fertilized with 6 mM nitrate for growth. The establishment of the tripartite symbiosis (+Rh+AMF) hindered the growth and nodulation of the plants and increased the concentration of Mn needed for maximum growth. It can be concluded that, under present experimental conditions, AMF did not promote the growth of the plants, questioning the benefits of the tripartite symbiosis in early flowering legume varieties. Nevertheless, the apparent exigency of high doses of Mn by +Rh+AMF plants for optimal growth and nodulation needs to be verify under field conditions before new recommendations are issue to farmers regarding crop Mn fertilization. The amendment of crops with Mn is a difficult task and constitutes an extra cost for the low-income farmers. Results also indicate the need to breed for black bean genotypes tolerant to low Mn, since most efforts have been paid to screen beans for tolerance to Mn toxicity. Finally, present observations that the type and magnitude of the plant responses to the different treatment combinations varied along the plant life cycle supports the need for long term experiments.Figure optionsDownload full-size imageDownload as PowerPoint slideResearch Highlights► The growth of Rhizobium-nodulated local black bean varieties is always significantly smaller that that of N-fertilized plants, possible attributed to the inability of plants to carry out the catabolism of ureide at high rates. ► Deficiency of Mn in tropical acid soils is an important constrains for the growth of black beans, and the tripartite symbiosis seems to be a burden for early flowering bean cultivars. ► More work is needed to screen for black bean genotypes with higher symbiotic efficiency and tolerance to Mn soil deficiencies.