Lupin, a Unique Legume That Is Nodulated by Multiple Microsymbionts: The Role of Horizontal Gene Transfer

Abstract

Lupin is a high-protein legume crop that grows in a wide range of edaphoclimatic conditions where other crops are not viable. Its unique seed nutrient profile can promote health benefits, and it has been proposed as a phytoremediation plant. Most rhizobia nodulating Lupinus species belong to the genus Bradyrhizobium, comprising strains that are phylogenetically related to B. cytisi, B. hipponenese, B. rifense, B. iriomotense/B. stylosanthis, B. diazoefficiens, B. japonicum, B. canariense/B. lupini, and B. retamae/B. valentinum. Lupins are also nodulated by fast-growing bacteria within the genera Microvirga, Ochrobactrum, Devosia, Phyllobacterium, Agrobacterium, Rhizobium, and Neorhizobium. Phylogenetic analyses of the nod and nif genes, involved in microbial colonization and symbiotic nitrogen fixation, respectively, suggest that fast-growing lupin-nodulating bacteria have acquired their symbiotic genes from rhizobial genera other than Bradyrhizobium. Horizontal transfer represents a key mechanism allowing lupin to form symbioses with bacteria that were previously considered as non-symbiotic or unable to nodulate lupin, which might favor lupin's adaptation to specific habitats. The characterization of yet-unstudied Lupinus species, including microsymbiont whole genome analyses, will most likely expand and modify the current lupin microsymbiont taxonomy, and provide additional knowledge that might help to further increase lupin's adaptability to marginal soils and climates.

Keywords: 16S rRNA; Bradyrhizobium; Lupinus; horizontal gene transfer; nifH; nodC; rhizobia; symbiotic genes.

Figure 1

Neighbor-joining phylogenetic analysis of 16S rRNA gene sequence of different species of Lupinus spp. microsymbionts and their closest relatives. Lupin microsymbionts are highlighted in color as follows: Bradyrhizobium spp. in green; Microvirga spp. in blue; Phyllobacterium spp. in orange; Ochrobactrum spp. in yellow; Devosia spp. in red. Values of bootstrap probability greater than 50% are indicated. The host legume and place of isolation are reported when known.

Figure 2

Neighbor-joining phylogenetic analysis of nodC gene sequences of different species of Lupinus spp. microsymbionts (highlighted in red) and their closest relatives. Bootstrap probability values greater than 50% are indicated.

Figure 3

Neighbor-joining phylogenetic analysis of nifH gene sequences of different species of Lupinus spp. microsymbionts (highlighted in red) and their closest relatives. Values of bootstrap probability greater than 50% are indicated.