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Legumes have an intrinsic capacity to accommodate both symbiotic and endophytic bacteria within root nodules. For the symbionts, a complex genetic mechanism that allows mutual recognition and plant infection has emerged from genetic studies under axenic conditions. In contrast, little is known about the mechanisms controlling the endophytic infection. Here we investigate the contribution of both the host and the symbiotic microbe to endophyte infection and development of mixed colonised nodules in Lotus japonicus. We found that infection threads initiated by Mesorhizobium loti, the natural symbiont of Lotus, can selectively guide endophytic bacteria towards nodule primordia, where competent strains multiply and colonise the nodule together with the nitrogen-fixing symbiotic partner. Further co-inoculation studies with the competent coloniser, Rhizobium mesosinicum strain KAW12, show that endophytic nodule infection depends on functional and efficient M. loti-driven Nod factor signalling. KAW12 exopolysaccharide (EPS) enabled endophyte nodule infection whilst compatible M. loti EPS restricted it. Analysis of plant mutants that control different stages of the symbiotic infection showed that both symbiont and endophyte accommodation within nodules is under host genetic control. This demonstrates that when legume plants are exposed to complex communities they selectively regulate access and accommodation of bacteria occupying this specialized environmental niche, the root nodule.

In the last decade, analyses of both molecular and morphological characters, including nodulation, have led to major changes in our understanding of legume taxonomy. In parallel there has been an explosion in the number of genera and species of rhizobia known to nodulate legumes. No attempt has been made to link these two sets of data or to consider them in a biogeographical context. This review aims to do this by relating the data to the evolution of the two partners: it highlights both longitudinal and latitudinal trends and considers these in relation to the location of major land masses over geological time. Australia is identified as being a special case and latitudes north of the equator as being pivotal in the evolution of highly specialized systems in which the differentiated rhizobia effectively become ammonia factories. However, there are still many gaps to be filled before legume nodulation is sufficiently understood to be managed for the benefit of a world in which climate change is rife.

Burkholderia legume symbionts (also called α-rhizobia) are ancient in origin and are the main nitrogen-fixing symbionts of species belonging to the large genus Mimosa in Brazil. We investigated the extent of the affinity between Burkholderia and species in the tribe Mimoseae by studying symbionts of the genera Piptadenia (P.), Parapiptadenia (Pp.), Pseudopiptadenia (Ps.), Pityrocarpa (Py.), Anadenanthera (A.) and Microlobius (Mi.), all of which are native to Brazil and are phylogenetically close to Mimosa, and which together with Mimosa comprise the \"Piptadenia group\". We characterized 196 strains sampled from 18 species from 17 locations in Brazil using two neutral markers and two symbiotic genes in order to assess their species affiliations and the evolution of their symbiosis genes. We found that Burkholderia are common and highly diversified symbionts of species in the Piptadenia group, comprising nine Burkholderia species, of which three are new ones and one was never reported as symbiotic (B. phenoliruptrix). However, α-rhizobia were also detected and were occasionally dominant on a few species. A strong sampling site effect on the rhizobial nature of symbionts was detected, with the symbiont pattern of the same legume species changing drastically from location to location, even switching from β to α-rhizobia. Coinoculation assays showed a strong affinity of all the Piptadenia group species towards Burkholderia genotypes, with the exception of Mi. foetidus. Phylogenetic analyses of neutral and symbiotic markers showed that symbiosis genes in Burkholderia from the Piptadenia group have evolved mainly through vertical transfer, but also by horizontal transfer in two species.

Some species of legumes and nine other flowering plant families form symbioses with bacteria that fix atmospheric nitrogen within specialized plant structures called nodules. How and how often nodulation symbiosis originated has implications for engineering symbiotic nitrogen fixation in non-legume crops. The prevailing hypothesis of a single origin with massive parallel losses has been challenged in a phylogenomic study favoring 16 origins and 10 losses. Nodulation has been assembled once or many times from existing processes (e.g., mycorrhizal symbiosis) and therefore almost nothing about it is truly novel. Because any feature of nodulation can be explained either as divergence from a common origin or as convergence in unrelated taxa, tests are needed that can distinguish whether assembly of homologous components has occurred uniquely or convergently. Much needs to be learned about nodulation symbioses across the proposed independent origins, especially involving the master nodulation transcription factor, Nodule Inception ( NIN ). Symbiosis of nitrogen-fixing bacteria in evolutionarily novel “nodules” of diverse flowering plants including legume crops was assembled from pre-existing functions. Testing hypotheses of single vs. multiple origins is the focus of this Perspective.

In Lotus japonicus , a LysM receptor kinase, EPR3, distinguishes compatible and incompatible rhizobial exopolysaccharides at the epidermis. However, the role of this recognition system in bacterial colonization of the root interior is unknown. Here we show that EPR3 advances the intracellular infection mechanism that mediates infection thread invasion of the root cortex and nodule primordia. At the cellular level, Epr3 expression delineates progression of infection threads into nodule primordia and cortical infection thread formation is impaired in epr3 mutants. Genetic dissection of this developmental coordination showed that Epr3 is integrated into the symbiosis signal transduction pathways. Further analysis showed differential expression of Epr3 in the epidermis and cortical primordia and identified key transcription factors controlling this tissue specificity. These results suggest that exopolysaccharide recognition is reiterated during the progressing infection and that EPR3 perception of compatible exopolysaccharide promotes an intracellular cortical infection mechanism maintaining bacteria enclosed in plant membranes. The Lotus japonicus LysM receptor kinase EPR3 perceives rhizobial exopolysaccharides to initiate infection of the root epidermis. Here the authors show that EPR3 also mediates infection thread progression in the root cortex and show that key transcription factors that regulate symbiosis specify the expression of Epr3 .

Root nodule symbiosis (RNS) is a complex trait that enables plants to access atmospheric nitrogen converted into usable forms through a mutualistic relationship with soil bacteria. Pinpointing the evolutionary origins of RNS is critical for understanding its genetic basis, but building this evolutionary context is complicated by data limitations and the intermittent presence of RNS in a single clade of ca. 30,000 species of flowering plants, i.e., the nitrogen-fixing clade (NFC). We developed the most extensive de novo phylogeny for the NFC and an RNS trait database to reconstruct the evolution of RNS. Our analysis identifies evolutionary rate heterogeneity associated with a two-step process: An ancestral precursor state transitioned to a more labile state from which RNS was rapidly gained at multiple points in the NFC. We illustrate how a two-step process could explain multiple independent gains and losses of RNS, contrary to recent hypotheses suggesting one gain and numerous losses, and suggest a broader phylogenetic and genetic scope may be required for genome-phenome mapping. Kates et al. propose that nitrogen-fixing symbiosis between bacteria and angiosperms has been gained and lost multiple times, based on ancestral reconstructions of nodulation across a deeply sampled, 13,000-species phylogeny, in contrast to a single origin with many losses.

The genus Burkholderia comprises more than 60 species isolated from a wide range of niches. Although they have been shown to be diverse and ubiquitously distributed, most studies have thus far focused on the pathogenic species due to their clinical importance. However, the increasing number of recently described Burkholderia species associated with plants or with the environment has highlighted the division of the genus into two main clusters, as suggested by phylogenetical analyses. The first cluster includes human, animal, and plant pathogens, such as Burkholderia glumae, Burkholderia pseudomallei, and Burkholderia mallei, as well as the 17 defined species of the Burkholderia cepacia complex, while the other, more recently established cluster comprises more than 30 nonpathogenic species, which in most cases have been found to be associated with plants, and thus might be considered to be potentially beneficial. Several species from the latter group share characteristics that are of use when associating with plants, such as a quorum sensing system, the presence of nitrogen fixation and/or nodulation genes, and the ability to degrade aromatic compounds. This review examines the commonalities in this growing subgroup of Burkholderia species and discusses their prospective biotechnological applications.

A century after the discovery of rhizobia, the first Beta-proteobacteria species (beta-rhizobia) were isolated from legume nodules in South Africa and South America. Since then, numerous species belonging to the Burkholderiaceae family have been isolated. The presence of a highly branching lineage of nodulation genes in beta-rhizobia suggests a long symbiotic history. In this review, we focus on the beta-rhizobial genus Paraburkholderia, which includes two main groups: the South American mimosoid-nodulating Paraburkholderia and the South African predominantly papilionoid-nodulating Paraburkholderia. Here, we discuss the latest knowledge on Paraburkholderia nitrogen-fixing symbionts in each step of the symbiosis, from their survival in the soil, through the first contact with the legumes until the formation of an efficient nitrogen-fixing symbiosis in root nodules. Special attention is given to the strain P. phymatum STM815T that exhibits extraordinary features, such as the ability to: (i) enter into symbiosis with more than 50 legume species, including the agriculturally important common bean, (ii) outcompete other rhizobial species for nodulation of several legumes, and (iii) endure stressful soil conditions (e.g., high salt concentration and low pH) and high temperatures.

Bacterial infection of interior tissues of legume root nodules is controlled at the epidermal cell layer and is closely coordinated with progressing organ development. Using spontaneous nodulating Lotus japonicus plant mutants to uncouple nodule organogenesis from infection, we have determined the role of 16 genes in these two developmental processes. We show that host-encoded mechanisms control three alternative entry processes operating in the epidermis, the root cortex and at the single cell level. Single cell infection did not involve the formation of trans-cellular infection threads and was independent of host Nod-factor receptors and bacterial Nod-factor signals. In contrast, Nod-factor perception was required for epidermal root hair infection threads, whereas primary signal transduction genes preceding the secondary Ca 2+ oscillations have an indirect role. We provide support for the origin of rhizobial infection through direct intercellular epidermal invasion and subsequent evolution of crack entry and root hair invasions observed in most extant legumes. Plant and bacteria symbiosis in some species results in the coordinate formation of nitrogen fixing nodules and infection of the plant host. Using mutant Lotus japonicus plants, Madsen and colleagues have determined the role of 16 different genes in these two processes.

Rhizobial symbiosis genes are often carried on symbiotic islands or plasmids that can be transferred (horizontal transfer) between different bacterial species. Symbiosis genes involved in horizontal transfer have different phylogenies with respect to the core genome of their ‘host’. Here, the literature on legume–rhizobium symbioses in field soils was reviewed, and cases of phylogenetic incongruence between rhizobium core and symbiosis genes were collated. The occurrence and importance of horizontal transfer of rhizobial symbiosis genes within and between bacterial genera were assessed. Horizontal transfer of symbiosis genes between rhizobial strains is of common occurrence, is widespread geographically, is not restricted to specific rhizobial genera, and occurs within and between rhizobial genera. The transfer of symbiosis genes to bacteria adapted to local soil conditions can allow these bacteria to become rhizobial symbionts of previously incompatible legumes growing in these soils. This, in turn, will have consequences for the growth, life history, and biogeography of the legume species involved, which provides a critical ecological link connecting the horizontal transfer of symbiosis genes between rhizobial bacteria in the soil to the above-ground floral biodiversity and vegetation community structure.