Poor Competitiveness of Bradyrhizobium in Pigeon Pea Root Colonization in Indian Soils

Pigeon pea, a legume crop native to India, is the primary source of protein for more than a billion people in developing countries. The plant can form symbioses with N-2-fixing bacteria; however, reports of poor crop nodulation in agricultural soils abound. We report here a study of the bacterial community associated with pigeon pea, with a special focus on the symbiont population in different soils and vegetative and non-vegetative plant growth. Location with respect to the plant roots was determined to be the main factor controlling the bacterial community, followed by developmental stage and soil type. Plant genotype plays only a minor role. Pigeon pea roots have a reduced microbial diversity compared to the surrounding soil and select for Proteobacteria, especially for Rhizobium spp., during vegetative growth. While Bradyrhizobium, a native symbiont of pigeon pea, can be found associating with roots, its presence is dependent on plant variety and soil conditions. A combination of 16S rRNA gene amplicon survey, strain isolation, and co-inoculation with nodule-forming Bradyrhizobium spp. and non-N-2-fixing Rhizobium spp. demonstrated that the latter is a much more successful colonizer of pigeon pea roots. Poor nodulation of pigeon pea in Indian soils may be caused by a poor Bradyrhizobium competitiveness against non-nodulating root colonizers such as Rhizobium. Hence, inoculant strain selection of symbionts for pigeon pea should be based not only on their nitrogen fixation potential but, more importantly, on their competitiveness in agricultural soils. IMPORTANCE Plant symbiosis with N-2-fixing bacteria is a key to sustainable, low-input agriculture. While there are ongoing projects aiming to increase the yield of cereals using plant genetics and host-microbiota interaction engineering, the biggest potential lies in legume plants. Pigeon pea is a basic food source for a billion low-income people in India. Improving its interactions with N-2-fixing rhizobia could dramatically reduce food poverty in India. Despite the Indian origin of this plant, pigeon pea nodulates only poorly in native soils. While there have been multiple attempts to select the best N-2-fixing symbionts, there are no reliable strains available for geographically widespread use. In this article, using 16S rRNA gene amplicon, culturomics, and plant co-inoculation assays, we show that the native pigeon pea symbionts such as Bradyrhizobium spp. are able to nodulate their host, despite being poor competitors for colonizing roots. Hence, in this system, the establishment of effective symbiosis seems decoupled from microbial competition on plant roots. Thus, the effort of finding suitable symbionts should focus not only on their N-2-fixing potential but also on their ability to colonize. Increasing pigeon pea yield is a low-hanging fruit to reduce world hunger and degradation of the environment through the overuse of synthetic fertilizers.

Automated summary

Pigeon pea, a primary protein source for over a billion people in developing countries, forms symbiosis with N-2-fixing bacteria, particularly Rhizobium spp. The bacterial community associated with pigeon pea is significantly influenced by plant roots location, developmental stage, and soil type, with Proteobacteria being the dominant group. Native symbiont Bradyrhizobium spp. struggles to effectively colonize pigeon pea roots, leading to poor nodulation in Indian soils. This emphasizes the importance of symbiont competitiveness in agricultural soils for improving pigeon pea yield and reducing food poverty.