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Specificity in Legume-Rhizobia Symbioses

Mitchell Andrews, Morag E. Andrews

International Journal of Molecular Sciences · 2017 · Review · CC BY

doi:10.3390/ijms18040705

Abstract

Most species in the Leguminosae (legume family) can fix atmospheric nitrogen (N2) via symbiotic bacteria (rhizobia) in root nodules. Here, the literature on legume-rhizobia symbioses in field soils was reviewed and genotypically characterised rhizobia related to the taxonomy of the legumes from which they were isolated. The Leguminosae was divided into three sub-families, the Caesalpinioideae, Mimosoideae and Papilionoideae. Bradyrhizobium spp. were the exclusive rhizobial symbionts of species in the Caesalpinioideae, but data are limited. Generally, a range of rhizobia genera nodulated legume species across the two Mimosoideae tribes Ingeae and Mimoseae, but Mimosa spp. show specificity towards Burkholderia in central and southern Brazil, Rhizobium/Ensifer in central Mexico and Cupriavidus in southern Uruguay. These specific symbioses are likely to be at least in part related to the relative occurrence of the potential symbionts in soils of the different regions. Generally, Papilionoideae species were promiscuous in relation to rhizobial symbionts, but specificity for rhizobial genus appears to hold at the tribe level for the Fabeae (Rhizobium), the genus level for Cytisus (Bradyrhizobium), Lupinus (Bradyrhizobium) and the New Zealand native Sophora spp. (Mesorhizobium) and species level for Cicer arietinum (Mesorhizobium), Listia bainesii (Methylobacterium) and Listia angolensis (Microvirga). Specificity for rhizobial species/symbiovar appears to hold for Galega officinalis (Neorhizobium galegeae sv. officinalis), Galega orientalis (Neorhizobium galegeae sv. orientalis), Hedysarum coronarium (Rhizobium sullae), Medicago laciniata (Ensifer meliloti sv. medicaginis), Medicago rigiduloides (Ensifer meliloti sv. rigiduloides) and Trifolium ambiguum (Rhizobium leguminosarum sv. trifolii). Lateral gene transfer of specific symbiosis genes within rhizobial genera is an important mechanism allowing legumes to form symbioses with rhizobia adapted to particular soils. Strain-specific legume rhizobia symbioses can develop in particular habitats.

Full text

From PubMed Central, U.S. National Library of Medicine, as current on Oct 21, 2026. Paragraph numbers are ours, so an answer can point at one.

1. Introduction

The Leguminosae (Fabaceae, the legume family) is comprised of ca. 19,300 species within 750 genera that occur as herbs, shrubs, vines or trees in mainly terrestrial habitats and are components of most of the world’s vegetation types. Currently, the legume family is divided into three sub-families, the Caesalpinioideae, Mimosoideae and Papilionoideae. Members of the Caesalpinioideae are grouped into four tribes, the Caesalpinieae, Cassieae, Cercideae and Detarieae comprising ca. 170 genera and 2250 species. The Mimosoideae are grouped into two tribes, the Ingeae and Mimoseae with ca. 80 genera and 3270 species, while the Papilionoideae consists of 28 tribes with ca. 480 genera and 13,800 species. However, a new classification of the legumes has been proposed with six sub-families based on the plastid matK gene sequences from ca. 20% of all legume species across ca. 90% of all currently recognized genera. The six sub-families proposed are a re-circumscribed Caesalpinioideae, Cercidoideae, Detarioideae, Dialioideae, Duparquetioideae and Papilionoideae. In this system, the currently recognized Mimosoideae is a distinct clade nested within the re-circumscribed Caesalpinioideae. Species within the Cercidoideae, Detarioideae, Dialioideae and Duparquetioideae do not nodulate.

Most legume species can fix atmospheric nitrogen (N2) via symbiotic bacteria (general term “rhizobia”) in root nodules, and this can give them an advantage under low soil nitrogen (N) conditions if other factors are favourable for growth. Furthermore, N2 fixation by legumes can be a major input of N into natural and agricultural ecosystems. Generally, legume nodules can be classified as indeterminate or determinate in growth. Indeterminate nodules maintain meristematic tissue, while determinate nodules have a transient meristem. Nodule type is dependent on host plant, and legume species that can produce both determinate and indeterminate nodules are rare. All genera examined in the Caesalpinioideae and Mimosoideae had indeterminate nodules. Within the Papilionoideae, most tribes had indeterminate nodules, but the Desmodieae, Phaseoleae, Psoraleae and some members of the Loteae show “desmodioid” determinate nodules and the Dalbergieae “aeschynomenoid” determinate nodules. Desmodioid nodules have lenticels, and rhizobia “infected” tissue within them also contains uninfected cells. Aeschynomenoid nodules do not have lenticels, have uniform infected tissue and are always associated with lateral or adventitious roots. Where tested, species within the Desmodieae, Phaseoleae and Psoraleae had ureides as the main N-containing compound transported from nodules, but species in the Dalbergieae and Loteae transported amides/amino acids. Indeterminate nodules have a single or branched apical meristem, and a few genera, such as Lupinus (Genisteae) and Listia (Crotalaria), have “lupinoid” nodules with two or more lateral meristems, which in some cases completely surround the subtending root. Generally, indeterminate nodules have a mixture of infected and uninfected cells in the central nodule tissue, but lupinoid nodules, as for aeschynomenoid nodules (Dalbergiae), have uniformly-infected cells.

The nodulation process for almost all legumes studied is initiated by the legume production of a mix of compounds, mainly flavonoids, which induce the synthesis of NodD protein in rhizobia. Different legumes produce different types/mixes of compounds. The NodD protein activates the transcription of other genes involved in the nodulation process, including those required to produce Nod factors, the signal molecules produced by the rhizobia and detected by the plant, which induce nodule organogenesis. The nodABC genes encode for the proteins required to make the core Nod factor structure. Nod factors from different rhizobia have a similar structure of a chitin-like N-acetyl glucosamine oligosaccharide backbone with a fatty acyl chain at the non-reducing end, but differ in their length of N-acetyl glucosamine oligosaccharide backbone and the length and saturation of the fatty acid chain. The Nod-factor core is modified by species-specific proteins, which results in various substitutions, including acetylation, glycosylation, methylation and sulfation. Perception of the Nod-factor signal in legumes is mediated by Nod factor receptors, which are plasma membrane localized serine/threonine receptor kinases in the case of the model legumes Lotus japonicus and Medicago truncatula.

The available data indicate that rhizobia enter the roots of most legume species via root hair infection. Here, rhizobia enter root hairs, and host cell wall material grows around the developing “infection”, forming an infection thread, which grows through the cortex of the root, branching repeatedly. Generally, rhizobia are released from the tips of these infection threads into membrane-bound structures within host cells called symbiosomes where they differentiate into their N2-fixing form known as bacteroids. However, all species examined in the Caesalpinioideae, except herbaceous Chamaecrista spp. and a few species in the Papilionoideae, retain their rhizobia within infection threads. Bacteroids vary greatly in their level of differentiation and viability depending on the legume host. The process of root hair infection can lead to the formation of either indeterminate or desmodioid determinate nodules. A second mode of rhizobial infection occurs with species in the Dalbergiae (aeschynemonoid nodules) where rhizobia enter roots at the sites of lateral root emergence (“crack” entry), and infection threads are not involved in the infection process. Thirdly, for at least some members of the Genisteae (e.g., Lupinus spp.) and Crotalariae (e.g., Listia spp.), rhizobia enter the roots directly through the root epidermis at the junction between epidermal cells, and again, infection threads are not involved in the infection process.

Over the past twenty-five years, DNA-based methods have become increasingly used to characterize rhizobia. In particular, phylogenetic analyses of sequences of the 16S ribosomal RNA (rRNA) gene, a range of “housekeeping” genes and genes involved in the symbiosis have been developed as a “standard approach”. The 16S rRNA gene sequence on its own can delineate rhizobia at the genus level. The main symbiosis genes studied are the “nif” genes, which encode the subunits of nitrogenase, the rhizobial enzyme that fixes N2, and the “nod” genes, which encode Nod factors that induce various symbiotic responses on legume roots. Specific nod genes have been shown to be major determinants of legume host specificity. The nif and nod genes are often carried on plasmids or symbiotic islands, and these genes can be transferred (lateral transfer) between different bacterial species within a genus and more rarely across genera. Almost all rhizobia tested had nod genes. However, a few Bradyrhizobium strains, which do not possess nodABC genes, can form N2 fixing nodules on particular Aeschynomene spp.. Bacterial species from a range of genera in the α-proteobacteria (most commonly Bradyrhizobium, Ensifer (Sinorhizobium), Mesorhizobium and Rhizobium) and two genera in the β-proteobacteria (Burkholderia (Paraburkholderia) and Cupriavidus) can form functional (N2 fixing) nodules on specific legumes (Table 1, Table 2, Table 3 and Table 4). Reports that Achromobacter and Herbaspirillum (β-proteobacteria) produce N2 fixing nodules on Prosopis juliflora and Aspalathus linearis, respectively and Pseudomonas (Gammaproteobacteria) produces N2 fixing nodules on Robinia pseudoacacia and Acacia confusa have not been confirmed. Furthermore, for Lotus corniculatus, Geobacillus (phylum Firmicutes), Paenibacillus (Firmicutes) and Rhodococcus (Actinobacteria) were for the first time reported as rhizobial symbionts. These bacterial species had similar nodA gene sequences to Mesorhizobium isolated from the same plants, and it was concluded that the lateral gene transfer of these genes had occurred from the Mesorhizobium. However, lateral gene transfer of symbiosis genes is much less common between than within genera, and this work needs to be independently verified.

Legume species differ greatly in their specificity for rhizobial symbionts. Galega officinalis (tribe Galegeae) and Hedysarum coronarium (tribe Hedysareae) have been highlighted as being highly specific with respect to their rhizobial symbionts. Both of these species are in the inverted repeat lacking clade (IRLC). The IRLC is marked by the loss of one copy of the inverted region of the plastid genome. Almost all genera in the IRLC are temperate; all have indeterminate nodules, and where examined, their bacteroids were terminally differentiated and could not return to their bacterial form. The IRLC contains several important temperate grain (e.g., Pisum sativum and Vicia faba) and forage (e.g., Trifolium spp. and Medicago spp.) legumes. There is evidence that at least some of these crop legumes have a high degree of rhizobial specificity. For example, an analysis of core and symbiotic genes of rhizobia nodulating Vicia faba and Vicia sativa from different continents showed that they belong to a phylogenetically-compact group indicating that these species are restrictive hosts. In contrast, Macroptilium purpureum and the grain legumes Phaseolus vulgaris and Vigna unguiculata in the tribe Phaseoleae are nodulated by rhizobia from different genera across the α- and β-proteobacteria. The Phaseoleae are of tropical/subtropical origin, have desmodioid determinate nodules with bacteroids, which are not terminally differentiated.

Here, the literature on legume-rhizobia symbioses in field soils was reviewed and genotypically characterised rhizobia related to the taxonomy of the legumes from which they were isolated. The objectives of the work were to collate data on legume rhizobia symbioses and then assess to what extent legume specificity for rhizobial symbionts is related to legume taxonomy.

2. Framework and Assumptions of Study

The general classification of the Leguminosae follows Lewis et al., 2005, with updates. The sub-families Caesalpinioideae, Mimosoideae and Papilionoideae are considered separately. The Papilionoideae is split into those that show indeterminate nodules and those that show determinate nodules. Those that show indeterminate nodules are further split into the IRLC and all other clades.

Nodulating bacteria were classified at the genus level, on the basis of sequences of the 16S rRNA gene (almost all cases), and/or the 16S–23S DNA intergenic spacer region, and/or common house-keeping genes, and/or DNA-DNA hybridisations, and these results are presented in the tables. Sequences for nif and nod genes are considered in the text. Rhizobial genus and species names validated in the International Journal of Systematic and Evolutionary Microbiology were used with one exception: Burkholderia was retained as opposed to using Paraburkholderia, as a case to reinstate Burkholderia is being prepared by workers in the field. The term symbiovar (sv.) is used when describing rhizobial strains within the same species that differ with respect to the legume species they effectively nodulate.

A comprehensive collation of published legume-rhizobia symbioses up until 30 September 2016 was carried out. Articles were collected by searching the Institute for Scientic Information (ISI) Web of Science using each legume genus partnered with each of the rhizobia, Bradyrhizobium, Burkholderia, Cupriavidus, Ensifer, Mesorhizobium, Rhizobium and Sinorhizobium as the keywords. Further searches were carried out on the literature quoted in the selected papers and those listed as quoting the selected papers in the ISI Web of Science. Only data for plants sampled under field conditions, or for plants grown in soils taken from the field, or supplied field soil extracts were used. Bacteria isolated from legume nodules were accepted as rhizobia if they were shown to produce functional (N2 fixing) nodules on inoculation of their original legume host or a species within the original host legume genus under axenic conditions. The range of measurements and visual assessments used as evidence of the occurrence of N2 fixation were accepted. These were acetylene reduction activity, red/pink nodules (evidence of leghaemoglobin and, hence, nodules assumed to be active), increased total plant or shoot dry matter or N content, visually greener (increased chlorophyll) and increased plant vigour. However, it is acknowledged that in some cases, greater growth, vigour and/or greenness could have been caused by plant hormone production by the bacterium. All data obtained for all species are presented with three exceptions. Representative data are presented for Glycine max, Phaseolus vulgaris and Vigna unguiculata due to the large number of publications on these three species.

3. Caesalpinioideae-Rhizobia Symbioses

Of the three legume sub-families, the Caesalpinioideae contains the smallest proportion of nodulated genera with nodulation confirmed for Campsiandra, Chidlowia, Dimorphandra, Erythrophleum, Jacqueshuberia, Melanoxylon, Moldenhauwera and Tachigali in the tribe Caesalpinieae and Chamaecrista in the tribe Cassieae. Only two studies have genotypically characterised bacteria confirmed as rhizobia of Caesalpinioideae species. Firstly, five rhizobial isolates from Dimorphandra wilsonii and one from Dimorphandra jorgei sampled in the Cerrado biome in Brazil were Bradyrhizobium. Secondly, 166 rhizobial isolates from Erythrophleum fordii sampled at four sites in the Guangdong and Guangsii Provinces of the southern sub-tropical region of China were also all Bradyrhizobium. In both studies, core and symbiosis gene sequences indicated that there were diverse and novel strains amongst the isolates.

Data are available for bacterial isolates from nodules of other Caesalpinioideae species, but their ability to produce N2 fixing nodules on their legume host under axenic conditions was not tested. Specifically, three isolates from Tachigali versicolor sampled on Barro Colorado Island, Panama, which were not tested on their original host plant, but were shown to nodulate Macroptilium atropurpureum, were Bradyrhizobium. Similarly, strain STM934, stated to be confirmed as Bradyrhizobium, was isolated from nodules of Erythrophleum guineensis growing in natural forests of the Ziama reservation in southeast Guinea and shown to produce functional nodules on Macroptilium atropurpureum. In this case, a re-inoculation experiment was carried out on the original host, but the substrate was non-sterile forest soil. Bradyrhizobium was isolated from and shown to nodulate Chamaecrista sampled in Kakadu National Park, Northern Territory, Australia, but N2 fixation was not reported. Furthermore, there are several reports that Bradyrhizobium inoculum can increase nodulation of Chamaecrista spp. under field conditions in Australia and China. Thus, the available evidence indicates that Bradyrhizobium spp. are the dominant, possibly exclusive, rhizobial symbionts of legumes in the Caesalpinioideae, but data are limited, and the degree of specificity between legumes in the Caesalpinioideae and their rhizobial symbionts cannot be assessed without further work.

4. Mimosoideae-Rhizobia Symbioses

Rhizobia have been characterized from 15 species across seven genera in the tribe Ingeae and ca. 120 species from 13 genera in the tribe Mimoseae within the sub-family Mimosoideae (Table 1). Bradyrhizobium, Ensifer, Mesorhizobium and Rhizobium were each reported to nodulate species in the Ingeae and the Mimoseae. Furthermore, Ochrobactrum was reported to nodulate Acacia mangium (Ingeae); Allorhizobium and Devosia were reported to nodulate Neptunia natans (Mimoseae); and there are many reports that Cupriavidus and Burkholderia nodulate Mimosa spp. and related species (Mimoseae) (Table 1). In addition, excepting Acacia auriculiformis (Ingeae) and Mimosa pigra (Mimoseae), all species that were examined in three or more separate studies, Acacia mangium, Acacia saligna, Calliandra grandiflora and Senegalia senegal (Ingeae), Leucaena leucocephala, Mimosa diplotricha, Mimosa pudica, Parapiptadenia rigida, Prosopis alba and Vachellia tortilis (Mimoseae), were nodulated by at least three different rhizobial genera. Thus, a range of rhizobial genera, including both α- and β-proteobacteria, can nodulate legume species across the two Mimosoideae tribes, and generally, where tested over different studies, species within the Ingeae and Mimoseae tribes were promiscuous with respect to their rhizobial symbionts.

The Mimosa species examined across studies were the pan-tropical invasive Mimosa diplotricha and Mimosa pudica, and findings for these species appear not to reflect the situation with most Mimosa spp., which are endemic with a restricted range. The evidence indicates that most Mimosa spp. show specificity towards the rhizobial genus depending on their distribution with Burkholderia, Rhizobium/Ensifer and Cupriavidus, the main rhizobial symbiont of endemic Mimosa spp. in central and southern Brazil, central Mexico and southern Uruguay, respectively. The 16S rRNA and housekeeping gene sequences were diverse for Mimosa Burkholderia symbionts in Brazil, Rhizobium/Ensifer in Mexico and Cupriavidus in Uruguay. For Burkholderia in Brazil and Rhizobium/Ensifer in Mexico, the symbiosis gene sequences were largely congruent with the 16S rRNA and housekeeping gene sequences, indicating that these genes diverged over a long period within Burkholderia without substantial horizontal gene transfer between species. For Cupriavidus rhizobia in Uruguay, the nodA gene sequences were not congruent with the housekeeping gene sequences, but grouped together in a cluster. This is strong evidence that the various Cupriavidus species obtained their symbiosis genes via within group lateral gene transfer. It is not known if endemic Mimosa spp. nodulated by a particular rhizobia genus can form N2-fixing symbioses with Mimosa rhizobia of different genera from outside their region.

5.1. The IRLC

Data are available for 103 species from 27 genera/five tribes in the IRLC with Ensifer, Mesorhizobium and Rhizobium, commonly, and Bradyrhizobium, Neorhizobium and Phyllobacterium, rarely, reported to nodulate species within this clade (Table 2). There are no reports of Burkholderia or Cupriavidus symbionts within the IRLC. Previously, Galega officinalis, Galega orientalis and Hedysarum coronarium within the IRLC clade were reported to only form effective nodules with their respective symbionts Neorhizobium galegeae sv. officinalis, Neorhizobium galegeae sv. orientalis and Rhizobium sullae. The data in Table 2 indicate two other specific relationships between IRLC legumes and rhizobia. Firstly, eight separate studies on Cicer arietinum carried out over different countries and continents reported Mesorhizobium as the only symbiont. The 16S rRNA and housekeeping gene sequences indicated that strains of Mesorhizobium ciceri and M. mediterraneum were common, but not exclusive Mesorhizobium symbionts of Cicer arietinum in most studies outside China, with M. muleiense the main symbiont in Northwest China. Across studies where tested, nifH and nodC gene sequences were similar for all Mesorhizobium isolates shown to produce functional nodules on Cicer arietinum, indicating their specificity towards this legume species and that lateral transfer of these genes had occurred between the different Mesorhizobium spp..

Secondly, for the tribe Fabeae, seventeen studies across five Lathyrus species, Lens culinaris, Pisum sativum and eleven Vicia spp. reported Rhizobium as the only symbiont. Across these studies, Rhizobium leguminosarum (and where tested, R. leguminosarum sv. viciae) was the most common symbiont with some varieties of Pisum sativum, such as cv. Afghanistan, only nodulated by specific strains of Rhizobium leguminosarum sv. viciae, which occur in soils in their native range in Afghanistan/Turkey. Furthermore, in a study of 154 isolates of 18 Vicia species grown in 16 Chinese provinces, only 17 representative Rhizobium Leguminosarum sv. viciae isolates, from a wide range of potential rhizobia, produced fully-developed, effective (“colour red”) nodules. Thus, a highly specific relationship has developed between species in the Fabeae and R. leguminosarum sv. viciae, but it is not an exclusive relationship, as R. fabeae, R. multihospitium, R. pisi, R. laguerreae and R. anhuiense have been reported to effectively nodulate Fabeae species. However, the nifH and nodC gene sequences of all of these rhizobia showed high similarity, indicating their specificity towards the Fabeae species and that, in this case, lateral gene transfer had occurred between different Rhizobium spp..

Within the tribe Trifolieae, 14 out of 16 Medicago/Melilotus spp. had Ensifer as symbiont, but in four cases not exclusively. The most studied species, Medicago sativa (lucerne), was commonly nodulated by Ensifer meliloti, which is the recommended inoculum for this legume crop, but it also had Neorhizobium and Rhizobium symbionts. However, Medicago laciniata and Medicago rigiduloides were found to only nodulate with Ensifer strains sampled in their native range in the Mediterranean Basin. These strains were formally described as Ensifer meliloti sv. medicaginis and Ensifer meliloti sv. rigiduloides, respectively. Similarly, different Trifolium spp. have different compatibility with different strains of Rhizobium leguminosarum sv trifolii, which is the recommended inoculum for most Trifolium crops. Trifolium ambiguum, in particular, has been highlighted as only forming N2-fixing nodules with strains of Rhizobium leguminosarum sv trifolii specific to its region of origin (the Caucasus and Eastern Europe).

In relation to other members of the IRLC, Ensifer, Mesorhizobium and Rhizobium were shown to nodulate species within Astragalus, Colutea, Glycyrrhiza, Oxytropis and Sphaerophyceae (Galegeae), Hedysarum (Hedysareae) and Trifolium. Furthermore, Astragalus adsurgense, Astragalus complanatus, Colutea arborescens, Oxytropis glabra and Sphaerophysa salsula (Galegeae), Caragana intermedia (Hedysareae) and Trifolium fragiferum and Trifolium repens were all nodulated by three different rhizobial genera. Thus, for the IRLC, specificity for the rhizobial genus appears to hold at the tribe level for the Fabeae (Rhizobium spp.) and species level for Cicer arietinum (Mesorhizobium spp.). Specificity for rhizobial species or symbiovar holds for Galega officinalis (Neorhizobium galegeae sv. officinalis), Galega orientalis (Neorhizobium galegeae sv. orientalis), Hedysarum coronarium (Rhizobium sullae), Medicago laciniata (Ensifer meliloti sv. medicaginis), Medicago rigiduloides (Ensifer meliloti sv. rigiduloides) and Trifolium ambiguum (Rhizobium leguminosarum sv. trifolii), but it is not a characteristic of all members of the clade.

5.2. Clades with Indeterminate Nodules, Excluding the IRLC

Data are shown for 113 species from 33 genera across 13 Papilionoideae tribes with indeterminate nodules that do not show the IRLC mutation (Table 3). Azorhizobium, Bradyrhizobium, Burkholderia, Ensifer, Mesorhizobium, Methylobacterium, Microvirga, Neorhizobium, Ochrobactrum, Pararhizobium, Phyllobacterium and Rhizobium were all reported to nodulate species within this group. Amorpha fruticosa and Dalea purpurea (Amorpheae), Retama sphaerocarpa and Spartium junceum (Genisteae), Coronilla varia (Loteae), Tephrosia falciformis and Tephrosia villosa (Millettiea), Gliricidia sepium and Robinia pseudoacacia (Robineae) and Sesbania sericea and Sesbania virgata (Sesbanieae) were nodulated by two rhizobial genera. Aspalathus linearis and Crotalaria pallida (Crotalarieae), Tephrosia purpurea (Millettiea), Sesbania cannabina, Sesbania punicea, Sesbania rostrata and Sesbania sesban (Sesbanieae), Sophora alopecuroides and Sophora flavescens (Sophoreae) and Ammopiptanthus nanus and Ammopiptanthus mongolicus (Thermopsideae) were all nodulated by at least three different rhizobial genera. Thus, generally, where tested, Papilionoideae species with indeterminate nodules excluding the IRLC were promiscuous in relation to rhizobial symbiont. Within the Genisteae, Bradyrhizobium was the only symbiont reported for nine Cytisus spp. across ten separate studies and three Genista spp. across three separate studies (Table 3). Furthermore, eight out of 10 Lupinus spp. (Genisteae) across 11 separate studies were nodulated by Bradyrhizobium. These results indicate that Bradyrhizobium may be the main symbionts of Genisteae species, but further work is required to confirm this. Generally, 16S rRNA and housekeeping gene sequences indicate that diverse Bradyrhizobium spp. form N2-fixing nodules on Cytisus spp. and Lupinus spp., but the diversity of their symbiosis genes is dependent on the geographical origin of the legumes. For example, most Bradyrhizobium isolates from native Lupinus spp. in Europe form a distinct lineage, ‘clade 11’, on the basis of their nodA gene sequences. Similarly, different Bradyrhizobium spp. associated with native Cytisus villosus in Morocco all showed similar nodC and nifH sequences, which were closely related to those of Bradyrhizobium japonicum sv. genistearum. In contrast, rhizobia sampled from invasive Cytisus scoparius sampled in six states in the United States, differed with respect to housekeeping and symbiosis gene sequences. Specifically, one group of isolates had both housekeeping and symbiosis gene sequences similar to a Bradyrhizobium clade from native legumes in Western North America, but two clades had nifD, nifH and nodC sequences highly similar or identical to a Cytisus scoparius strain isolated in Spain, while their housekeeping genes were similar to American Bradyrhizobium clades. Thus, it appears that Bradyrhizobium ancestrally associated with native North American legumes have acquired symbiosis genes from European Cytisus scoparius Bradyrhizobium symbionts via lateral gene transfer.

The two exceptions to Bradyrhizobium as the rhizobial symbiont of Lupinus spp. were Ochrobactrum and Microvirga, both of which are rare as rhizobial symbionts of legumes. The nodD sequence for Ochrobactrum and the nodA sequence for Microvirga indicated that both bacteria obtained their nod genes via horizontal gene transfer from more common rhizobial genera. Microvirga is also the only bacterial genus shown to form N2-fixing nodules on Listia angolensis. Similarly, Listia bainesii has been found to only produce N2-fixing nodules with pink pigmented Methylobacterium. It was suggested that the seasonally waterlogged habitat of Listia spp. may have resulted in the selection of unusual rhizobial symbionts adapted to their environments.

In one study in the Cape Floristic Region (CFR) of South Africa, Burkholderia was reported to be the exclusive symbiont of ten Cyclopia spp., Podalyria calyptera and Virgilia oroboides, all species in the Podalyrieae plus three Hypocalyptus spp. (Hypocalypteae). Burkholderia was confirmed to nodulate Podolyria calyptrata and Virgilia oroboides in the CFR. The majority of Burkholderia isolates had unique nifH and nodA gene sequences, and the specificity of these symbioses needs testing.

Previously, Sesbania sesban was reported to be highly promiscuous with respect to rhizobial symbionts, and the data here indicate that this could be a genus level trait (Table 3). However, the reports that Sophora alopecuroides and Sophora flavescens sampled in China are nodulated by Ensifer, Mesorhizobium, Phyllobacterium and Rhizobium with a wide range of symbiosis gene sequences contrasts with the finding that New Zealand (NZ) native Sophora spp. were exclusively nodulated by Mesorhizobium spp. with almost identical unique nodA and nodC gene sequences. This emphasises that species within the same genus can vary greatly with respect to their specificity for rhizobial symbionts.

5.3. Clades with Determinate Nodules

The Dalbergieae are almost exclusively of tropical/sub-tropical distribution and show an aeschynomenoid determinate nodule structure. Rhizobia have been characterised for 23 species from seven genera in the Dalbergieae, Adesmia, Aeschynomene, Arachis, Centrolobium, Dalbergia, Pterocarpus and Zornia (Table 4). Bradyrhizobium was found to nodulate all species, except Adesmia bicolor (Rhizobium), with Rhizobium also reported for Arachis hypogaea in two studies. Thus, on the data available, the Dalbergieae appear to be primarily nodulated by Bradyrhizobium. For Arachis hypogaea, twelve separate studies reported Bradyrhizobium as a rhizobial symbiont (Table 4). Across these studies, both core and symbiosis gene sequences indicated that Arachis hypogaea was nodulated by a diverse range of Bradyrhizobium spp. and are promiscuous with respect to Bradyrhizobium spp. Excepting Arachis hypogaea, data are limited for rhizobial symbionts of species in the Dalbergieae. However, the unusual ability of specific Bradyrhizobium strains that lack canonical nodABC genes to form N2-fixing nodules on roots and/or stems of particular Aeschynomene spp. is highlighted.

The closely related tribes Desmodieae, Phaseoleae and Psoraleae are also mainly of tropical/sub-tropical distribution, and with rare exceptions, species within these tribes showed a desmodioid nodule structure. Rhizobia have been characterized for 25 species from three genera, Desmodium, Kummerowia and Lespedeza, in the Desmodieae (Table 4). Species from all three genera, Desmodium microphyllum, Desmodium racemosum, Desmodium sequax, Kummerowia striata, Lespedeza bicolor and Lespedeza daurica, were nodulated by rhizobia from three separate genera. Similarly, for 28 species across 14 genera within the Phaseoleae, there was no strong evidence for high specificity for rhizobial symbiont (Table 4). Phaseolus vulgaris and Vigna unguiculata have been highlighted as being promiscuous with respect to their rhizobial symbionts under field conditions. Data in Table 4 show that both species can be nodulated by different rhizobial genera in the α-proteobacteria, as well as Burkholderia in the β-proteobacteria. Across three studies, Phaseolus lunatus was reported to be nodulated by Bradyrhizobium and Rhizobium, while Vigna angularis, Vigna radiata and Vigna subterranea were reported to be nodulated by three separate rhizobial genera. Data are limited for other genera/species within the Phaseoleae with the exception of Glycine max, which is the main grain/oil seed legume grown worldwide, and Glycine soja. Both Glycine spp. were nodulated by Bradyrhizobium, Ensifer and Rhizobium. In the one case where separate studies were carried out on one species within the Psoraleae, Psoralea pinnata was nodulated by Bradyrhizobium, Burkholderia and Mesorhizobium. Thus, where tested, species within the Desmodieae, Phaseoleae and Psoraleae were promiscuous with respect to their rhizobial symbionts.

Species in the Loteae, which show a desmodoid nodule structure, are of temperate distribution. Data are available for 16 Lotus spp. within the Loteae across 13 separate studies. For all species examined in two or more studies, at least two rhizobia genera were reported as symbionts. Overall, the available data indicate that legume species with a desmodioid determinate nodule structure are promiscuous with respect to their rhizobia symbionts.

6. Legume Specificity for Rhizobial Symbionts

The objectives of the work were to collate data on legume rhizobia symbioses and assess the extent that legume specificity for rhizobial symbiont is related to legume taxonomy. Bradyrhizobium spp. were the exclusive rhizobial symbionts of species in the Caesalpinioideae; but, rhizobia were characterised for only three legume species over two studies, and the degree of specificity between legumes in the Caesalpinioideae and their rhizobial symbionts cannot be assessed without further work. Generally, species within the two Mimosoideae tribes, Ingeae and Mimoseae were promiscuous with respect to their rhizobial symbionts, but Mimosa spp. show specificity towards the rhizobia genus depending on their distribution, with Burkholderia, Rhizobium/Ensifer and Cupriavidus the main rhizobial symbiont of endemic Mimosa spp. in central and southern Brazil, central Mexico and southern Uruguay, respectively. Papilionoideae species with indeterminate nodules were split into the IRLC and all other clades. A range of species within both groups nodulated with different rhizobia genera, but there was also strong evidence that some species within both groups showed specificity for rhizobial genus or species/symbiovar. Specificity for rhizobial genus appears to hold at the tribe level for the Fabeae (Rhizobium), the genus level for Cytisus (Bradyrhizobium), Lupinus (Bradyrhizobium) and NZ native Sophora spp. (Mesorhizobium) and the species level for Cicer arietinum (Mesorhizobium), Listia bainesii (Methylobacterium) and Listia angolensis (Microvirga). Specificity for rhizobial species/symbiovar appears to hold for Galega officinalis (Neorhizobium galegeae sv. officinalis), Galega orientalis (Neorhizobium galegeae sv. orientalis), Hedysarum coronarium (Rhizobium sullae), Medicago laciniata (Ensifer meliloti sv. medicaginis), Medicago rigiduloides (Ensifer meliloti sv. rigiduloides) and Trifolium ambiguum (Rhizobium leguminosarum sv. trifolii). For Papilionoideae with determinate nodules, the Dalbergieae (aeschynomenoid nodules) were primarily nodulated by Bradyrhizobium, while those in the Desmodieae, Phaseoleae, Psoraleae and Loteae (desmodioid nodules) were promiscuous with respect to rhizobial genus. Thus, on the data available, species in the Papilionoideae that show specificity for rhizobial genus, species or symbiovar have indeterminate nodules and are generally (but not exclusively) of temperate distribution. However, many temperate legumes with indeterminate nodules are promiscuous with respect to the rhizobial genus indicating that high specificity for rhizobial symbiont only occurs under specific conditions.

For Mimosa spp., specificity towards rhizobial genus depending on distribution is likely to be at least in part related to the relative occurrence of the potential symbionts in soils of the different regions. For example, evidence indicates that Mimosa Cupriavidus symbionts are absent from soils in central and southern Brazil, while Mimosa Burkholderia symbionts are absent from soils in southern Uruguay. This has been related to soil characteristics with low pH favouring Burkholderia over Cupriavidus in Brazil, but high heavy metal content favouring Cupriavidus over Burkholderia in Uruguay. It was proposed that native Mimosa in the different regions have selected symbiotic bacteria adapted to local conditions, which resulted in the development of highly specific associations. However, for this to occur, such rhizobia must be available in the soil. The within genus 16S rRNA and housekeeping gene sequences were diverse for Mimosa symbionts in all regions. For Burkholderia in Brazil and Rhizobium/Ensifer in Mexico, the symbiosis gene sequences were largely congruent with the 16S rRNA and housekeeping gene sequences. For Cupriavidus rhizobia in Uruguay, the nodA gene sequences were not congruent with the housekeeping gene sequences, but grouped together in a cluster, indicating that the various species within the group obtained their symbiosis genes via within group lateral gene transfer. Lateral gene transfer is a mechanism whereby rhizobia and non-rhizobial bacteria adapted to local soil conditions could become specific rhizobial symbionts of legumes growing in these soils. The evidence described above indicates that lateral gene transfer of symbiosis genes has been important within the Papilionoideae in relation to the development of specific relationships between the Fabeae and Rhizobium spp., Cytisus and Bradyrhizobium spp., Lupinus and Bradyrhizobium spp., NZ native Sophora and Mesorhizobium spp. and Cicer arietinum and Mesorhizobium spp. Data are presented for Mesorhizobium isolates from Cicer arietinum and NZ native Sophora spp. to emphasise this point.

Firstly, 20 Mesorhizobium isolates from Cicer arietinum, sampled across three countries in five separate studies, showed diverse 16S rRNA sequences, but highly similar nodC sequences (Figure 1A,B). Here, evidence is strong that native Mesorhizobium muleiense adapted to alkaline soils in Gansu and Xinjiang Provinces of China obtained its Cicer arietinum-specific symbiotic genes from Mesorhizobium ciceri or Mesorhizobium mediterraneum introduced together with Cicer arietinum used as a crop. Secondly, 48 isolates from four NZ native Sophora spp. sampled at eight different field sites separated into eight groups and three individual isolates on the basis of their concatenated recA, gln11 and rpoβ gene sequences, but showed almost identical nodC (and nodA) sequences (Figure 2A,B). Seven of the groups have been formally identified as new species. This relationship between NZ native Sophora spp. and Mesorhizobium spp. with specific symbiosis gene sequences is highly specific as none of twenty rhizobial isolates from common weed and crop legumes in NZ produced functional nodules on the NZ native Sophora microphylla. Furthermore, Mesorhizobium isolates from Carmichaelia, Clianthus and Montigena, the only other NZ native legume genera, did not nodulate NZ native Sophora microphylla or Sophora tetraptera. Mesorhizobium isolates from Carmichaelia, Clianthus and Montigena had unique nodC sequences different from those of Sophora Mesorhizobium isolates (Figure 2B). However, in some cases, their 16S rRNA, recA and gln11 sequences were similar to those of Sophora Mesorhizobium isolates, emphasizing the importance of the specific symbiosis genes in the NZ Sophora Mesorhizobium symbiosis. Generally, Sophora isolates from the same field site grouped together on concatenated recA, gln11 and rpoβ gene sequences (Figure 2B). This apparent link between housekeeping gene sequences and field site is compatible with the proposal that lateral transfer of symbiosis genes to Mesorhizobium strains adapted to local soil conditions has occurred.

Some varieties of Pisum sativum, such as cv. Afghanistan, are only nodulated by specific strains of Rhizobium leguminosarum sv. viciae, which occur in soils in their native range in Afghanistan/Turkey. The ability of these strains to nodulate Pisum sativum cv. Afghanistan is controlled by a single recessive gene, sym2 in the plant. The sym2 allele interacts with a specific gene, nodX, present in R. leguminosarum sv. viciae strains able to nodulate cv. Afghanistan. The nodX gene product acetylates a Nod factor, which mediates a specific compatible interaction with this cultivar. Furthermore, Medicago laciniata and Medicago rigiduloides were found to only nodulate with Ensifer meliloti strains (E. meliloti sv. medicaginis and E. meliloti sv. rigiduloides, respectively) sampled in their native range in the Mediterranean Basin, and Trifolium ambiguum only forms N2-fixing nodules with strains of Rhizobium leguminosarum sv. trifolii specific to its region of origin, the Caucasus and Eastern Europe. The mechanisms of these highly specific relationships are not fully understood, but the nodA gene sequences of E. meliloti sv. medicaginis and nodA, nodB and nodC gene sequences of E. meliloti sv. rigiduloides diverged from those of E. meliloti strains, which nodulated other Medicago spp., while the ability of certain strains of Rhizobium leguminosarum sv. trifolii to effectively nodulate Trifolium ambiguum, but not Trifolium repens (white clover) appears to be linked to a 111-bp insertion in their nifH/fixA intergenic region. The factors that have resulted in these highly specific relationships are not known. Furthermore, it is not known if these highly specific relationships reflect adaptation of the symbioses and result in greater rates of N2 fixation or more efficient N2 fixation, as would be expected on theoretical grounds, and this warrants further study.

7. Conclusions

Overall, the data indicate that lateral gene transfer of specific symbiosis genes within rhizobial genera is an important mechanism allowing legumes to form symbioses with rhizobia adapted to particular soils. It also maintains specificity between legume species and rhizobia species with specific symbiosis genes. Strain-specific legume rhizobia symbioses can develop in particular habitats.

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    Rincón-Rosales R., Villalobos-Escobedo J.M., Rogel M.A., Martinez J., Ormeño-Orrillo E., Martínez-Romero E. Rhizobium calliandrae sp. nov., Rhizobium mayense sp. nov. and Rhizobium jaguaris sp. nov., rhizobial species nodulating the medicinal legume Calliandra grandiflora. Int. J. Syst. Evol. Microbiol. 2013;63:3423-3429.

    Not in our library10.1099/ijs.0.048249-0

  54. 54.

    Odee D.W., Haukka K., McInroy S.G., Sprent J.I., Sutherland J.M., Young J.P.W. Genetic and symbiotic characterization of rhizobia isolated from tree and herbaceous legumes grown in soils from ecologically diverse sites in Kenya. Soil Biol. Biochem. 2002;34:801-811.

    Not in our library10.1016/s0038-0717(02)00009-3

  55. 55.

    Leblanc H.A., McGraw R.L., Nygren P., Le Roux C. Neotropical legume tree Inga edulis forms N2-fixing symbiosis with fast-growing Bradyrhizobium strains. Plant Soil. 2005;275:123-133.

    Not in our library10.1007/s11104-005-0808-8

  56. 56.

    Da Silva K., de Meyer S.E., Rouws L.F.M., Farias E.N.C., dos Santos M.A.O., O’Hara G., Ardley J.K., Willems A., Pitard R.M., Zilli J.E. Bradyrhizobium ingae sp. nov., isolated from effective nodules of Inga laurina grown in Cerrado soil. Int. J. Syst. Evol. Microbiol. 2014;64:3395-3401.

    Not in our library10.1099/ijs.0.063727-0

  57. 57.

    Toledo I., Lloret L., Martinez-Romero E. Sinorhizobium americanus sp. nov., a new Sinorhizobium species nodulating native Acacia spp. in Mexico. Syst. Appl. Microbiol. 2003;26:54-64.

    Not in our library10.1078/072320203322337317

  58. 58.

    Fall D., Diouf D., Ourarhi M., Faye A., Abdelmounen H., Neyra M., Sylla S.N., Missbah el Idrissi M. Phenotypic and genotypic characteristics of Acacia Senegal (L.) Willd. root-nodulating bacteria isolated from soils in the dryland part of Senegal. Lett. Appl. Microbiol. 2008;47:85-97.

    Not in our library10.1111/j.1472-765x.2008.02389.x

  59. 59.

    Bournaud C., de Faria S.M., dos Santos J.M.F., Tisseyre P., Silva M., Chaintreuil C., Gross E., James E.K., Prin Y., Moulin L. Burkholderia species are the most common and preferred nodulating symbionts of the Piptadenia group (Tribe Mimoseae). PLoS ONE. 2013;8:e63478.

    Not in our library10.1371/journal.pone.0063478

  60. 60.

    Beyhaut E., Tlusty B., van Berkum P., Graham P.H. Rhizobium giardinii is the microsymbiont of Illinois bundleflower (Desmanthus illinoensis (Michx.) Mcmillan) in Midwestern prairies. Can. J. Microbiol. 2006;52:903-907.

    Not in our library10.1139/w06-051

  61. 61.
    Phenotypic, molecular and symbiotic characterization of the rhizobial symbionts of Desmanthus paspalaceus (Lindm.) Burkart that grow in the province of Santa Fe, Argentina. · 2014
    Not checked
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    Wang E.T., Martínez-Romero J., Martínez-Romero E. Genetic diversity of rhizobia from Leucaena leucocephala nodules in Mexican soils. Mol. Ecol. 1999;8:711-724.

    Not in our library10.1046/j.1365-294x.1999.00608.x

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    Xu K.W., Penttinen P., Chen Y.X., Chen Q., Zhang X. Symbiotic efficiency and phylogeny of the rhizobia isolated from Leucaena leucocephala in arid-hot river valley area in Panxi, Sichuan, China. Appl. Microbiol. Biotchnol. 2013;97:783-793.

    Not in our library10.1007/s00253-012-4246-2

  64. 64.

    López-López A., Rogel-Hernández M.A., Barois I., Ortis Ceballos A.I., Martínez J., Ormeño-Orrillo E., Martínez-Romero E. Rhizobium grahamii sp. nov., from nodules of Dalea leporina, Leucaena leucocephala and Clitoria ternatea, and Rhizobium mesoamericanum sp. nov., from nodules of Phaseolus vulgaris, siratro, cowpea and Mimosa pudica. Int. J. Syst. Evol. Microbiol. 2012;62:2264-2271.

    Not in our library10.1099/ijs.0.033555-0

  65. 65.

    Chen W.-M., Moulin L., Bontemps C., Vandamme P., Béna G., Boivin-Masson C. Legume symbiotic nitrogen fixation by β-proteobacteria is widespread in nature. J. Bacteriol. 2003;185:7266-7272.

    Not in our library10.1128/jb.185.24.7266-7272.2003

  66. 66.

    Chen W.-M., de Faria S.M., Straliotto R., Pitard R.M., Simões-Araùjo J.L., Chou J.-H., Chou Y.-J., Barrios E., Prescott A.R., Elliott G.N., et al. Proof that Burkholderia strains form effective symbioses with legumes: A study of novel Mimosa-nodulating strains from South America. Appl. Environ. Microbiol. 2005;71:7461-7471.

    Not in our library10.1128/aem.71.11.7461-7471.2005

  67. 67.

    Chen W.-M., James E.K., Chou J.-H., Sheu S.-Y., Yang S.-Z., Sprent J.I. β-Rhizobia from Mimosa pigra, a newly discovered invasive plant in Taiwan. New Phytol. 2005;168:661-675.

    Not in our library10.1111/j.1469-8137.2005.01533.x

  68. 68.

    Barrett C.F., Parker M.A. Prevalence of Burkholderia sp. nodule symbionts on four mimosoid legumes from Barro Colorado Island, Panama. Syst. Appl. Microbiol. 2005;28:57-65.

    Not in our library10.1016/j.syapm.2004.09.002

  69. 69.

    Barrett C.F., Parker M.A. Coexistence of Burkholderia, Cupriavidus, and Rhizobium sp. nodule bacteria on two Mimosa spp. in Costa Rica. Appl. Environ. Microbiol. 2006;72:1198-1206.

    Not in our library10.1128/aem.72.2.1198-1206.2006

  70. 70.

    Liu X.Y., Wang E.T., Li Y., Chen W.X. Diverse bacteria isolated from root nodules of Trifolium, Crotalaria and Mimosa grown in the subtropical regions of China. Arch. Microbiol. 2007;188:1-14.

    Not in our library10.1007/s00203-007-0209-x

  71. 71.

    Parker M.A., Wurtz A.K., Paynter Q. Nodule symbiosis of invasive Mimosa pigra in Australia and in ancestral habitats: A comparative analysis. Biol. Invasions. 2007;9:127-138.

    Not in our library10.1007/s10530-006-0009-2

  72. 72.

    Elliott G.N., Chou J.-H., Chen W.-M., Bloemberg G.V., Bontemps C., Martínez-Romero E., Velázquez E., Young J.P.W., Sprent J.I., James E.K. Burkholderia spp. are the most competitive symbionts of Mimosa, particularly under N-limited conditions. Environ. Microbiol. 2009;11:762-778.

    Not in our library10.1111/j.1462-2920.2008.01799.x

  73. 73.

    Bontemps C., Elliott G.N., Simon M.F., dos Reis F.B., Gross E., Lawton R.C., Neto N.E., Loureiro M.deF., de Faria S.M., Sprent J.I., et al. Burkholderia species are ancient symbionts of legumes. Mol. Ecol. 2010;19:44-52.

    Not in our library10.1111/j.1365-294x.2009.04458.x

  74. 74.

    Bontemps C., Rogel M.A., Wiechmann A., Mussabekova A., Moody S., Simon M.F., Moulin L., Elliott G.N., Lacercat-Didier L., Dasilva C., et al. Endemic Mimosa species from Mexico prefer α-proteobacterial rhizobial symbionts. New Phytol. 2016;209:319-333.

    Not in our library10.1111/nph.13573

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    Liu X.Y., Wu W., Wang E.T., Zhang B., Macdermott J., Chen W.X. Phylogenetic relationships and diversity of β-rhizobia associated with Mimosa species grown in Sishuangbanna, China. Int. J. Syst. Evol. Microbiol. 2011;61:334-342.

    Not in our library10.1099/ijs.0.020560-0

  76. 76.

    Liu X.Y., Wei S., Wang F., James E.K., Guo X.Y., Zagar C., Xia L.G., Dong X., Wang Y.P. Burkholderia and Cupriavidus spp. are the preferred symbionts of Mimosa spp. in Southern China. FEMS Microbiol. Ecol. 2012;80:417-426.

    Not in our library10.1111/j.1574-6941.2012.01310.x

  77. 77.

    Gehlot H.S., Tak N., Kaushik M., Mitra S., Chen W.-M., Poweleit N., Panwar D., Poonar N., Parihar R., Tak A., et al. An invasive Mimosa in India does not adopt the symbionts of its native relatives. Ann. Bot. 2013;112:179-196.

    Not in our library10.1093/aob/mct112

  78. 78.

    Andam C.P., Mondo S.J., Parker M.A. Monophyly of nodA and nifH genes across Texan and Costa Rican populations of Cupriavidus nodule symbionts. Appl. Environ. Microbiol. 2007;73:4686-4690.

    Not in our library10.1128/aem.00160-07

  79. 79.

    Platero R., James E.K., Rios C., Iriarte A., Sandes L., Zabaleta M., Battistoni F., Fabiano E. Novel Cupriavidus strains isolated from root nodules of native Uruguayan Mimosa species. Appl. Environ. Microbiol. 2016;82:3150-3164.

    Not in our library10.1128/aem.04142-15

  80. 80.

    De Lajudie P., Laurent-Fulele E., Willems A., Torck U., Coopman R., Collins M.D., Kersters K., Dreyfus B., Gillis M. Allorhizobium undicola gen. nov., sp. nov., nitrogen-fixing bacteria that efficiently nodulate Neptunia natans in Senegal. Int. J. Syst. Bacteriol. 1998;48:1277-1290.

    Not in our library10.1099/00207713-48-4-1277

  81. 81.

    Rivas R., Velázquez E., Willems A., Vizcaíno N., Subba-Rao N.S., Mateos P.F., Gillis M., Dazzo F.B., Martínez-Molina E. A new species of Devosia that forms a unique nitrogen-fixing root-nodule symbiosis with the aquatic legume Neptunia natans (L.f.) Druce. Appl. Environ. Microbiol. 2002;68:5217-5222.

    Not in our library10.1128/aem.68.11.5217-5222.2002

  82. 82.

    Taulé C., Zabaleta M., Mareque C., Platero R., Sanjurjo L., Sicardi M., Frioni L., Battistoni F., Fabiano E. New β-proteobacterial Rhizobium strains able to efficiently nodulate Parapiptadenia rigida (Benth.) Brenan. Appl. Environ. Microbiol. 2012;78:1692-1700.

    Not in our library10.1128/aem.06215-11

  83. 83.

    Diaz L.C., González P., Rubio E., Melchiorre M. Diversity and stress tolerance in rhizobia from Parque Chaqueño region of Argentina nodulating Prosopis alba. Biol. Fertil. Soils. 2013;49:1153-1165.

    Not in our library10.1007/s00374-013-0814-6

  84. 84.

    Iglesias O., Rivas R., García-Fraile P., Abril A., Mateos P.F., Martinez-Molina E., Velázquez E. Genetic characterization of fast-growing rhizobia able to nodulate Prosopis alba in North Spain. FEMS Microbiol. Lett. 2007;277:210-216.

    Not in our library10.1111/j.1574-6968.2007.00968.x

  85. 85.

    Velázquez E., Igual J.M., Willems A., Fernández M.P., Muñoz E., Mateos P.F., Abril A., Toro N., Normand P., Cervantes E., et al. Mesorhizobium chacoense sp. nov., a novel species that nodulates Prosopis alba in the Chaco Arido region (Argentina). Int. J. Syst. Evol. Microbiol. 2001;51:1011-1021.

    Not in our library10.1099/00207713-51-3-1011

  86. 86.

    Nick G., de Lajudie P., Eardly B.D., Suomalainen S., Paulin L., Zhang X., Gillis M., Lindström K. Sinorhizobium arboris sp. nov. and Sinorhizobium kostiense sp. nov., isolated from leguminous trees in Sudan and Kenya. Int. J. Syst. Bacterial. 1999;49:1359-1368.

    Not in our library10.1099/00207713-49-4-1359

  87. 87.

    Gehlot H.S., Panwar D., Tak N., Tak A., Sankhla I.S., Poonar N., Parihar R., Shekhawat N.S., Kumar M., Tiwari R., et al. Nodulation of legumes from the Thar desert of India and molecular characterization of their rhizobia. Plant Soil. 2012;357:227-243.

    Not in our library10.1007/s11104-012-1143-5

  88. 88.

    Fterich A., Mahdhi M., Caviedes M.A., Pajuelo E., Rivas R., Rodriguez-Llorente I.D., Mars M. Characterization of root-nodulating bacteria associated to Prosopis farcta growing in the arid regions of Tunisia. Arch. Microbiol. 2011;193:385-397.

    Not in our library10.1007/s00203-011-0683-z

  89. 89.

    Degefu T., Wolde-meskel E., Frostegård Å. Multilocus sequence analyses reveal several unnamed Mesorhizobium genospecies nodulating Acacia species and Sesbania sesban trees in Southern regions of Ethiopia. Syst. Appl. Microbiol. 2011;34:216-226.

    Not in our library10.1016/j.syapm.2010.09.006

  90. 90.

    Degefu T., Wolde-meskel E., Frostegård Å. Phylogenetic multilocus sequence analysis identifies seven novel Ensifer genospecies isolated from a less-well-explored biogeographical region in East Africa. Int. J. Syst. Evol. Microbiol. 2012;62:2286-2295.

    Not in our library10.1099/ijs.0.039230-0

  91. 91.

    Sankhla I.S., Tak N., Meghwal R.R., Choudhary S., Tak A., Rathi S., Sprent J.I., James E.K., Gehlot H.S. Molecular characterization of nitrogen fixing microsymbionts from root nodules of Vachellia (Acacia) jacquemontii, a native legume from the Thar Desert of India. Plant Soil. 2017;410:21-40.

    Not in our library10.1007/s11104-016-2838-9

  92. 92.

    Cordero I., Ruiz-Díez B., de la Peña T.C., Balaguer L., Lucas M.M., Rincón A., Pueyo J.J. Rhizobial diversity, symbiotic effectiveness and structure of nodules of Vachellia macracantha. Soil Biol. Biochem. 2016;96:39-54.

    Not in our library10.1016/j.soilbio.2016.01.011

  93. 93.

    Ba S., Willems A., de Lajudie P., Roche P., Jeder H., Quatrini P., Neyra M., Ferro M., Promé J.-C., Gillis M., et al. Symbiotic and taxonomic diversity of rhizobia isolated from Acacia tortilis sp. subsp. raddiana in Africa. Syst. Appl. Microbiol. 2002;25:130-145.

    Not in our library10.1078/0723-2020-00091

  94. 94.

    Nour S.M., Fernandez M.P., Normand P., Cleyet-Marel J.-C. Rhizobium ciceri sp. nov., consisting of strains that nodulate chickpeas (Cicer arietinum L.). Int. J. Syst. Bacteriol. 1994;44:511-522.

    Not in our library10.1099/00207713-44-3-511

  95. 95.

    Aouani M.E., Mhamdi R., Jebara M., Amarger N. Characterization of rhizobia nodulating chickpea in Tunisia. Agronomie. 2001;21:577-581.

    Not in our library10.1051/agro:2001147

  96. 96.

    Maâtallah J., Berraho E.B., Muñoz S., Sanjuan J., Lluch C. Phenotypic and molecular characterization of chickpea rhizobia isolated from different areas of Morocco. J. Appl. Microbiol. 2002;93:531-540.

    Not in our library10.1046/j.1365-2672.2002.01718.x

  97. 97.

    Rivas R., Laranjo M., Mateos P.F., Oliveira S., Martinez-Molina E., Velázquez E. Strains of Mesorhizobium amorphae and Mesorhizobium tianshanense, carrying symbiotic genes of common chickpea endosymbiotic species, constitute a novel biovar (ciceri) capable of nodulating Cicer arietinum. Lett. Appl. Microbiol. 2007;44:412-418.

    Not in our library10.1111/j.1472-765x.2006.02086.x

  98. 98.

    Ben Romdhane S., Trabelsi M., Aouani M.E., de Lajudie P., Mhamdi R. The diversity of rhizobia nodulating chickpea (Cicer arietinum) under water deficiency as a source of more efficient inoculants. Soil Biol. Biochem. 2009;41:2568-2572.

    Not in our library10.1016/j.soilbio.2009.09.020

  99. 99.

    Zhang J.J., Lou K., Jin X., Mao P.H., Wang E.T., Tian C.F., Sui X.H., Chen W.F., Chen W.X. Distinctive Mesorhizobium populations associated with Cicer arietinum L. in alkaline soils of Xinjiang, China. Plant Soil. 2012;353:123-134.

    Not in our library10.1007/s11104-011-1014-5

  100. 100.

    Zhang J., Yang X., Guo C., de Lajudie P., Singh R.P., Wang E., Chen W. Mesorhizobium muleiense and Mesorhizobium gsp. Nov. are symbionts of Cicer arietinum L. in alkaline soils of Gansu, Northwest China. Plant Soil. 2017;410:103-112.

    Not in our library10.1007/s11104-016-2987-x

  101. 101.

    Zahran H.H., Chahboune R., Moreno S., Bedmar E.J., Abdel-Fattah M., Yasser M.M., Mahmoud A.M. Identification of rhizobial strains nodulating Egyptian grain legumes. Int. Microbiol. 2013;16:157-163.

    Not in our library10.2436/20.1501.01.190

  102. 102.

    Armas-Carpote N., Pérez-Yépez J., Martínez-Hidalgo P., Garzón-Machado V., del Arco-Aguilar M., Velázquez E., Léon-Barrios M. Core and symbiotic genes reveal nine Mesorhizobium genospecies and three symbiotic lineages among the rhizobia nodulating Cicer canariense in its natural habitat (La Palma, Canary Islands). Syst. Appl. Microbiol. 2014;37:140-148.

    Not in our library10.1016/j.syapm.2013.08.004

  103. 103.

    Mutch L.A., Young J.P.W. Diversity and specificity of Rhizobium leguminosarum biovar viciae on wild and cultivated legumes. Mol. Ecol. 2004;13:2435-2444.

    Not in our library10.1111/j.1365-294x.2004.02259.x

  104. 104.

    Aoki S., Kondo T., Prévost D., Nakata S., Kajita T., Itó M. Genotypic and phenotypic diversity of rhizobia isolated from Lathyrus japonicus indigenous to Japan. Syst. Appl. Microbiol. 2010;33:383-397.

    Not in our library10.1016/j.syapm.2010.07.001

  105. 105.

    Han T.X., Wang E.T., Wu L.J., Chen W.F., Gu J.G., Gu C.T., Tian C.F., Chen W.X. Rhizobium multihospitium sp. nov., isolated from multiple legume species native of Xinjiang, China. Int. J. Syst. Evol. Microbiol. 2008;58:1693-1699.

    Not in our library10.1099/ijs.0.65568-0

  106. 106.

    Rashid M.H., Schäfer H., Gonzalez J., Wink M. Genetic diversity of rhizobia nodulating lentil (Lens culinaris) in Bangladesh. Syst. Appl. Microbiol. 2012;35:98-109.

    Not in our library10.1016/j.syapm.2011.11.008

  107. 107.

    Riah N., Béna G., Djekoun A., Heulin K., de Lajudie P., Laguerre G. Genotypic and symbiotic diversity of Rhizobium populations associated with cultivated lentil and pea in sub-humid and semi-arid regions of Eastern Algeria. Syst. Appl. Microbiol. 2014;37:368-375.

    Not in our library10.1016/j.syapm.2013.12.008

  108. 108.

    Zhang Y.J., Zheng W.T., Everall I., Young J.P.W., Zhang X.X., Tian C.F., Sui X.H., Wang E.T., Chen W.X. Rhizobium anhuiense sp. nov., isolated from effective nodules of Vicia faba and Pisum sativum. Int. J. Syst. Evol. Microbiol. 2015;65:2960-2967.

    Not in our library10.1099/ijs.0.000365

  109. 109.

    Kan F.L., Chen Z.Y., Wang E.T., Tian C.F., Sui X.H., Chen W.X. Characterization of symbiotic and endophytic bacteria isolated from root nodules of herbaceous legumes grown in Qinghai-Tibet plateau and in other zones of China. Arch. Microbiol. 2007;188:103-115.

    Not in our library10.1007/s00203-007-0211-3

  110. 110.

    Ampomah O.Y., Huss-Danell K. Genetic diversity of rhizobia nodulating native Vicia spp. in Sweden. Syst. Appl. Microbiol. 2016;39:203-210.

    Not in our library10.1016/j.syapm.2016.02.002

  111. 111.

    Santillana N., Ramírez-Bahena M.H., García-Fraile P., Velázquez E., Zúñiga D. Phylogenetic diversity based on rrs, atpD, recA genes and 16S–23S intergenic sequence analyses of rhizobial strains isolated from Vicia faba and Pisum sativum in Peru. Arch. Microbiol. 2008;189:239-247.

    Not in our library10.1007/s00203-007-0313-y

  112. 112.

    Saïdi S., Chebil S., Gtari M., Mhamdi R. Characterization of root-nodule bacteria isolated from Vicia faba and selection of plant growth promoting isolates. World J. Microbiol. Biotechnol. 2013;29:1099-1106.

    Not in our library10.1007/s11274-013-1278-4

  113. 113.

    Youseif S.H., Abd El-Megeed F.H., Ageez A., Cocking E.C. Saleh, S.A. Phylogenetic multilocus sequence analysis of native rhizobia nodulating faba bean (Vicia faba L.) in Egypt. Syst. Appl. Microbiol. 2014;37:560-569.

    Not in our library10.1016/j.syapm.2014.10.001

  114. 114.

    Xu K.W., Zou L., Penttinen P., Wang K., Heng N.N., Zhang X.P., Chen Q., Zhao K., Chen Y.X. Symbiotic effectiveness and phylogeny of rhizobia isolated from faba bean (Vicia faba L.) in Sichuan hilly areas, China. Syst. Appl. Microbiol. 2015;38:515-523.

    Not in our library10.1016/j.syapm.2015.06.009

  115. 115.

    Lei X., Wang E.T., Chen W.F., Sui X.H., Chen W.X. Diverse bacteria isolated from root nodules of wild Vicia species grown in temperate region of China. Arch. Microbiol. 2008;190:657-671.

    Not in our library10.1007/s00203-008-0418-y

  116. 116.

    Tian C.F., Wang E.T., Wu L.J., Han T.X., Chen W.F., Gu C.T., Gu J.G., Chen W.X. Rhizobium fabae sp. nov., a bacterium that nodulates Vicia faba. Int. J. Syst. Evol. Microbiol. 2008;58:2871-2875.

    Not in our library10.1099/ijs.0.2008/000703-0

  117. 117.

    Alvarez-Martínez E.R., Valverde Á., Ramírez-Bahena M.H., García-Fraile P., Tejedor C., Mateos P.F., Santillana N., Zúñiga D., Peix A., Velázquez E. The analysis of core and symbiotic genes of rhizobia nodulating Vicia from different continents reveals their common phylogenetic origin and suggests the distribution of Rhizobium leguminosarium strains together with Vicia seeds. Arch. Microbiol. 2009;191:659-668.

    Not in our library10.1007/s00203-009-0495-6

  118. 118.

    Rejili M., Mahdhi M., Fterich A., Dhaoui S., Guefrachi I., Abdeddayem R., Mars M. Symbiotic nitrogen fixation of wild legumes in Tunisia: Soil fertility dynamics, field nodulation and nodules effectiveness. Agric. Ecosyst. Environ. 2012;157:60-69.

    Not in our library10.1016/j.agee.2012.01.015

  119. 119.

    Radeva G., Jurgens G., Niemi M., Nick G., Suominen L., Lindström K. Description of two biovars in the Rhizobium galegae species: Biovar orientalis and biovar officinalis. System. Appl. Microbiol. 2001;24:192-205.

    Not in our library10.1078/0723-2020-00029

  120. 120.

    Liu W.Y.Y., Ridgway H.J., James T.K., Premaratne M., Andrews M. Characterisation of rhizobia nodulating Galega officinalis (goat’s rue) and Hedysarum coronarium (sulla). NZ Plant Prot. 2012;65:192-196.

    Not in our library

  121. 121.

    Chen W., Sun L., Lu J., Bi L., Wang E., Wei G. Diverse nodule bacteria were associated with Astragalus species in arid region of northwestern China. J. Basic Microbiol. 2015;55:121-128.

    Not in our library10.1002/jobm.201300209

  122. 122.

    Wei G.H., Zhang Z.X., Chen C., Chen W.M., Ju W.T. Phenotypic and genetic diversity of rhizobia isolated from nodules of the legume genera Astragalus, Lespedeza and Hedysarum in northwestern China. Microbial. Res. 2008;163:651-662.

    Not in our library10.1016/j.micres.2006.09.005

  123. 123.

    Zhao C.T., Wang E.T., Zhang Y.M., Chen W.F., Sui X.H., Chen W.X., Liu H.C., Zhang X.X. Mesorhizobium silamurunense sp. nov., isolated from root nodules of Astragalus species. Int. J. Syst. Evol. Microbiol. 2012;62:2180-2186.

    Not in our library10.1099/ijs.0.031229-0

  124. 124.

    Yan H., Ji Z.J., Jiao Y.S., Wang E.T., Chen W.F., Guo B.L., Chen W.X. Genetic diversity and distribution of rhizobia associated with the medicinal legumes Astragalus spp. and Hedysarum polybotrys in agricultural soils. Syst. Appl. Microbiol. 2016;39:141-149.

    Not in our library10.1016/j.syapm.2016.01.004

  125. 125.

    Nandasena K.G., O’Hara G.W., Tiwari R.P., Yates R.J., Howieson J.G. Phylogenetic relationships of three bacterial strains isolated from the pasture legume Biserrula pelecinus L. Int. J. Syst. Evol. Microbiol. 2001;51:1983-1986.

    Not in our library10.1099/00207713-51-6-1983

  126. 126.

    Nandasena K.G., O’Hara G.W., Tiwari R.P., Willems A., Howieson J.G. Mesorhizobium australicum sp. nov. and Mesorhizobium opportunistum sp. nov., isolated from Biserrula pelecinus L. in Australia. Int. J. Syst. Evol. Microbiol. 2009;59:2140-2147.

    Not in our library10.1099/ijs.0.005728-0

  127. 127.
    Rhizobia with 16S rRNA and nifH similar to Mesorhizobium huakuii but Novel recA, glnII, nodA and nodC genes are symbionts of New Zealand Carmichaelinae. · 2012
    Not checked
  128. 128.

    Ourarhi M., Abdelmoumen H., Guerrouj K., Benata H., Muresu R., Squartini A., El Idrissi M.M. Colutea arborescens is nodulated by diverse rhizobia in Eastern Morocco. Arch. Microbiol. 2011;193:115-124.

    Not in our library10.1007/s00203-010-0650-0

  129. 129.

    Ruiz-Díez B., Fajardo S., Puertas-Mejía M.A., del Felipe M.R., Fernández-Pascual M. Stress tolerance, genetic analysis and symbiotic properties of root-nodulating bacteria isolated from Mediterranean leguminous shrubs in Central Spain. Arch. Microbiol. 2009;191:35-46.

    Not in our library10.1007/s00203-008-0426-y

  130. 130.

    Li L., Sinkko H., Montonen L., Wei G., Lindström K., Räsänen L.A. Biogeography of symbiotic and other endophytic bacteria isolated from medicinal Glycyrrhiza species in China. FEMS Microbiol. Ecol. 2012;79:46-68.

    Not in our library10.1111/j.1574-6941.2011.01198.x

  131. 131.

    Wei G.H., Yang X.-Y., Zhang Z.-X., Yang Y.-Z., Lindström K. Strain Mesorhizobium sp. CCNWGX035: A stress-tolerant isolate from Glycyrrhiza glabra displaying a wide host range of nodulation. Pedosphere. 2008;18:102-112.

    Not in our library10.1016/s1002-0160(07)60108-8

  132. 132.

    Tan Z.Y., Wang E.T., Peng G.X., Zhu M.E., Martínez-Romero E., Chen W.X. Characterization of bacteria isolated from wild legumes in the north-western regions of China. Int. J. Syst. Bacteriol. 1999;49:1457-1469.

    Not in our library10.1099/00207713-49-4-1457

  133. 133.

    Chen W., Wang E., Wang S., Li Y., Chen X., Li Y. Characteristics of Rhizobium tianshanense sp. nov., a moderately and slowly growing root nodule bacterium isolated from an arid saline environment in Xinjiang, People’s Republic of China. Int. J. Syst. Bacteriol. 1995;45:153-159.

    Not in our library10.1099/00207713-45-1-153

  134. 134.

    Tan Z.Y., Kan F.L., Peng G.X., Wang E.T., Reinhold-Hurek B., Chen W.X. Rhizobium yanglingense sp. nov., isolated from arid and semi-arid regions in China. Int. J. Syst. Evol. Microbiol. 2001;51:909-914.

    Not in our library10.1099/00207713-51-3-909

  135. 135.

    Gerding M., O’Hara G.W., Bräu L., Nandasena K., Howieson J.G. Diverse Mesorhizobium spp. with unique nodA nodulating the South African legume species of the genus Lessertia. Plant Soil. 2012;358:385-401.

    Not in our library10.1007/s11104-012-1153-3

  136. 136.

    Lemaire B., Dlodlo O., Chimphango S., Stirton C., Schrire B., Boatwright J.S., Honnay O., Smets E., Sprent J., James E.K., et al. Symbiotic diversity, specificity and distribution of rhizobia in native legumes of the Core Cape Subregion (South Africa). FEMS Microbiol. Ecol. 2015;91:1-17.

    Not in our library10.1093/femsec/fiu024

  137. 137.

    Tan H.W., Heenan P., Ridgway H., Andrews M. The New Zealand alpine endemic Montigena novae-zelandiae (Fabaceae) shares rhizobial symbionts with Carmichaelia and Clianthus. N. Z. J. Bot. 2013;51:297-307.

    Not in our library10.1080/0028825x.2013.831360

  138. 138.

    Han T.X., Han L.L., Wu L.J., Chen W.F., Sui X.H., Gu J.G., Wang E.T., Chen W.X. Mesorhizobium gobiense sp. nov. and Mesorhizobium tarimense sp. nov., isolated from wild legumes growing in desert soils of Xinjiang, China. Int. J. Syst. Evol. Microbiol. 2008;58:2610-2618.

    Not in our library10.1099/ijs.0.2008/000125-0

  139. 139.

    Deng Z.S., Zhao L.F., Kong Z.Y., Yang W.Q., Lindström K., Wang E.T., Wei G.H. Diversity of endophytic bacteria within nodules of the Sphaerophysa salsula in different regions of Loess Plateau in China. FEMS Microbiol. Ecol. 2011;76:463-475.

    Not in our library10.1111/j.1574-6941.2011.01063.x

  140. 140.

    Xu L., Shi J.F., Zhao P., Chen W.M., Qin W., Tang M., Wei G.H. Rhizobium sphaerophysae sp. nov., a novel species isolated from root nodules of Sphaerophysa salsula in China. Antonie van Leeuwenhoek. 2011;99:845-854.

    Not in our library10.1007/s10482-011-9559-0

  141. 141.

    Yates R.J., Howieson J.G., Nandasena K.G., O’Hara G.W. Root-nodule bacteria of indigenous legumes in the north-west of Westen Australia and their interaction with exotic legumes. Soil Biol. Biochem. 2004;36:1319-1329.

    Not in our library10.1016/j.soilbio.2004.04.013

  142. 142.

    Wei G., Chen W., Young J.P.W., Bontemps C. A new clade of Mesorhizobium nodulating Alhagi sparsifolia. Syst. Appl. Microbiol. 2009;32:8-16.

    Not in our library10.1016/j.syapm.2008.11.003

  143. 143.

    Lu Y.L., Chen W.F., Wang E.T., Guan S.H., Yan X.R., Chen W.X. Genetic diversity and biogeography of rhizobia associated with Caragana species in three ecological regions of China. Syst. Appl. Microbiol. 2009;32:351-361.

    Not in our library10.1016/j.syapm.2008.10.004

  144. 144.

    Guan S.H., Chen W.F., Wang E.T., Lu Y.L., Yan X.R., Zhang X.X., Chen W.X. Mesorhizobium caraganae sp. nov., a novel rhizobial species nodulated with Caragana spp. in China. Int. J. Syst. Evol. Microbiol. 2008;58:2646-2653.

    Not in our library10.1099/ijs.0.65829-0

  145. 145.

    Squartini A., Struffi P., Döring H., Selenska-Pobell S., Tola E., Giacomini A., Vendramin E., Velázquez E., Mateos P.F., Martinez-Molina E., et al. Rhizobium sullae sp. nov. (formerly “Rhizobium hedysari”), the root-nodule microsymbiont of Hedysarum coronarium L. Int. J. Syst. Evol. Microbiol. 2002;52:1267-1276.

    Not in our library10.1099/00207713-52-4-1267

  146. 146.

    Baimiev A.K., Baimiev A.K., Gubaidullin I.I., Kulikova O.L., Chemeris A.V. Bacteria closely related to Phyllobacterium trifolii according to their 16S rRNA gene are discovered in the nodules of Hungarian sainfoin. Genetika. 2007;43:587-590.

    Not in our library10.1134/s1022795407050146

  147. 147.

    El Batanony N.H., Castellano-Hinojosa A., Correa-Galeote D., Bedmar E.J. The diversity of rhizobia nodulating the Medicago, Melilotus and Trigonella inoculation group in Egypt is marked by the dominance of two genetic types. Symbiosis. 2015;67:3-10.

    Not in our library10.1007/s13199-015-0365-8

  148. 148.

    Del Villegas M.C., Rome S., Mauré L., Domergue O., Gardan L., Bailly X., Cleyet-Marel J.-C., Brunel B. Nitrogen-fixing sinorhizobia with Medicago laciniata constitute a novel biovar (bv. medicaginis) of S. meliloti. Syst. Appl. Microbiol. 2006;29:526-538.

    Not in our library10.1016/j.syapm.2005.12.008

  149. 149.

    Badri Y., Zribi K., Badri M., Huguet T., van Berkum P., Aouani M.E. Comparison of rhizobia that nodulate Medicago laciniata and Medicago truncatula present in a single Tunisian arid soil. Can. J. Microbiol. 2007;53:277-283.

    Not in our library10.1139/w06-130

  150. 150.

    Mnasri B., Badri Y., Saïdi S., de Lajudie P., Mhamdi R. Symbiotic diversity of Ensifer meliloti strains recovered from various legume species in Tunisia. Syst. Appl. Microbiol. 2009;32:583-592.

    Not in our library10.1016/j.syapm.2009.07.007

  151. 151.

    Wang H., Man C.X., Wang E.T., Chen W.X. Diversity of rhizobia and interactions among the host legumes and rhizobial genotypes in an agricultural-forestry ecosystem. Plant Soil. 2009;314:169-182.

    Not in our library10.1007/s11104-008-9716-z

  152. 152.

    Rome S., Fernandez M.P., Brunel B., Normand P., Cleyet-Marel J.-C. Sinorhizobium medicae sp. nov., isolated from annual Medicago spp. Int. J. Syst. Bacteriol. 1996;46:972-980.

    Not in our library10.1099/00207713-46-4-972

  153. 153.

    Gubry-Rangin C., Béna G., Cleyet-Merel J.-C., Brunel B. Definition and evolution of a new symbiovar, sv. rigiduloides, among Ensifer meliloti efficiently nodulating Medicago species. Syst. Appl. Microbiol. 2013;36:490-496.

    Not in our library10.1016/j.syapm.2013.06.004

  154. 154.

    Van Berkum P., Beyene D., Bao G., Campbell T.A., Eardly B.D. Rhizobium mongolense sp. nov. is one of three rhizobial genotypes identified which nodulate and form nitrogen-fixing symbioses with Medicago ruthenica (L. Ledebour). Int. J. Syst. Bacteriol. 1998;48:13-22.

    Not in our library10.1099/00207713-48-1-13

  155. 155.

    Yan A.M., Wang E.T., Kan F.L., Tan Z.Y., Sui X.H., Reinhold-Hurek B., Chen W.X. Sinorhizobium meliloti associated with Medicago sativa and Melilotus spp. in arid saline soils in Xinjiang, China. Int. J. Syst. Evol. Microbiol. 2000;50:1887-1891.

    Not in our library10.1099/00207713-50-5-1887

  156. 156.

    Bromfield E.S.P., Tambong J.T., Cloutier S., Prévost D., Laguerre G., van Berkum P., Tran Thi T.V., Assabgui R., Barran L.R. Ensifer, Phyllobacterium and Rhizobium species occupy nodules of Medicago sativa (alfalfa) and Melilotus alba (sweet clover) grown at a Canadian site without a history of cultivation. Microbiology. 2010;156:505-520.

    Not in our library10.1099/mic.0.034058-0

  157. 157.

    Merabet C., Martens M., Mahdi M., Zakhia F., Sy A., Le Roux C., Domergue O., Coopman R., Bekki A., Mars M., et al. Multilocus sequence analysis of root nodule isolates from Lotus arabicus (Senegal), Lotus creticus, Argyrolobium uniflorum and Medicago sativa (Tunisia) and description of Ensifer numidicus sp. nov. and Ensifer garamanticus sp. nov. Int. J. Syst. Evol. Microbiol. 2010;60:664-674.

    Not in our library10.1099/ijs.0.012088-0

  158. 158.

    Djedidi S., Yokoyama T., Tomooka N., Ohkama-Ohtsu N., Risal C.P., Abdelly C., Sekimoto H. Phenotypic and genetic characterization of rhizobia associated with alfalfa in the Hokkaido and Ishigaki regions of Japan. Syst. Appl. Microbiol. 2011;34:453-461.

    Not in our library10.1016/j.syapm.2011.04.006

  159. 159.

    Valverde A., Velázquez E., Fernández-Santos F., Vizcaíno N., Rivas R., Mateos P.F., Martínez-Molina E., Igual J.M., Willems A. Phyllobacterium trifolii sp. nov., nodulating Trifolium and Lupinus in Spanish soils. Int. J. System. Evol. Microbiol. 2005;55:1985-1989.

    Not in our library10.1099/ijs.0.63551-0

  160. 160.

    Zhang J.J., Jing X.Y., de Lajudie P., Ma C., He P.X., Singh R.P., Chen W.F., Wang E.T. Association of white clover (Trifolium repens L.) with rhizobia of sv. trifolii belonging to three genomic species in alkaline soils in North and East China. Plant Soil. 2016;407:417-427.

    Not in our library10.1007/s11104-016-2899-9

  161. 161.

    Ogasawara M., Suzuki T., Mutoh I., Annapurna K., Arora N.K., Nishimura Y., Maheshwari D.K. Sinorhizobium indiaense sp. nov. and Sinorhizobium abri sp. nov. isolated from tropical legumes, Sesbania rostrata and Abrus precatorius, respectively. Symbiosis. 2003;34:53-68.

    Not in our library

  162. 162.

    Wang E.T., van Berkum P., Sui X.H., Beyene D., Chen W.X., Martínez-Romero E. Diversity of rhizobia associated with Amorpha fruticosa isolated from Chinese soils and description of Mesorhizobium amorphae sp. nov. Int. J. Syst. Bacteriol. 1999;49:51-65.

    Not in our library10.1099/00207713-49-1-51

  163. 163.

    Tlusty B., van Berkum P., Graham P.H. Characteristics of the rhizobia associated with Dalea spp. in the Ordway, Kellogg-Weaver Dunes, and Hayden prairies. Can. J. Microbiol. 2005;51:15-23.

    Not in our library10.1139/w04-107

  164. 164.

    Sy A., Giraud E., Jourand P., Garcia N., Willems A., de Lajudie P., Prin Y., Neyra M., Gillis M., Boivin-Masson C., et al. Methylotrophic Methylobacterium bacteria nodulate and fix nitrogen in symbiosis with legumes. J. Bacteriol. 2001;183:214-220.

    Not in our library10.1128/jb.183.1.214-220.2001

  165. 165.

    Howieson J.G., de Meyer S.E., Vivas-Marfisi A., Ratnayake S., Ardley J.K., Yates R.J. Novel Burkholderia bacteria isolated from Lebeckia ambigua—A perennial suffrutescent legume of the fynbos. Soil Biol. Biochem. 2013;60:55-64.

    Not in our library10.1016/j.soilbio.2013.01.009

  166. 166.

    Ardley J.K., Parker M.A., de Meyer S.E., Trengove R.D., O’Hara G.W., Reeve W.G., Yates R.J., Dilworth M.J., Willems A., Howieson J.G. Microvirga lupini sp. nov., Microvirga lotononidis sp. nov. and Microvirga zambiensis sp. nov. are α proteobacterial root-nodule bacteria that specifically nodulate and fix nitrogen with geographically and taxonomically separate legume hosts. Int. J. Syst. Evol. Microbiol. 2012;62:2579-2588.

    Not in our library10.1099/ijs.0.035097-0

  167. 167.

    Cardinale M., Lanza A., Bonnì M.L., Marsala S., Puglia A.M., Quatrini P. Diversity of rhizobia nodulating wild shrubs of Sicily and some neighbouring islands. Arch. Microbiol. 2008;190:461-470.

    Not in our library10.1007/s00203-008-0394-2

  168. 168.

    Rodríguez-Echeverría S., Pérez-Fernández M.A., Vlaar S., Finnan T. Analysis of the legume-rhizobia symbiosis in shrubs from central western Spain. J. Appl. Microbiol. 2003;95:1367-1374.

    Not in our library10.1046/j.1365-2672.2003.02118.x

  169. 169.

    Vinuesa P., Rademaker J.L.W., de Bruijn F.J., Werner D. Genotypic characterization of Bradyrhizobium strains nodulating endemic woody legumes of the Canary Islands by PCR-restriction fragment length polymorphism analysis of genes encoding 16S rRNA (16S rDNA) and 16S–23S rDNA intergenic spacers, repetitive extragenic palindromic PCR genomic fingerprinting, and partial 16S rDNA sequencing. Appl. Environ. Microbiol. 1998;64:2096-2104.

    Not in our library10.1128/aem.64.6.2096-2104.1998

  170. 170.

    Vinuesa P., Léon-Barrios M., Silva C., Willems A., Jarabo-Lorenzo A., Pérez-Galdona R., Werner D., Martínez-Romero E. Bradyrhizobium canariense sp. nov., an acid-tolerant endosymbiont that nodulates endemic genistoid legumes (Papilionoideae: Genisteae) from the Canary Islands, along with Bradyrhizobium japonicum bv. genistearum, Bradyrhizobium genospecies alpha and Bradyrhizobium genospecies beta. Int. J. Syst. Evol. Microbiol. 2005;55:569-575.

    Not in our library10.1099/ijs.0.63292-0

  171. 171.

    Jarabo-Lorenzo A., Velázquez E., Pérez-Galdona R., Vega-Hernández M.C., Martínez-Molina E., Mateos P.F., Vinuesa P., Martínez-Romero E., Léon-Barrios M. Restriction fragment length polymorphism analysis of 16S rDNA and low molecular weight RNA profiling of rhizobial isolates from shrubby legumes endemic to the Canary Islands. System. Appl. Microbiol. 2000;23:418-425.

    Not in our library10.1016/s0723-2020(00)80073-9

  172. 172.

    Jarabo-Lorenzo A., Pérez-Galdona R., Donate-Correa J., Rivas R., Velázquez E., Hernández M., Temprano F., Martínez-Molina E., Ruiz-Argüeso T., Léon-Barrios M. Genetic diversity of Bradyrhizobial populations from diverse geographic origins that nodulate Lupinus spp. and Ornithopus spp. System. Appl. Microbiol. 2003;26:611-623.

    Not in our library10.1078/072320203770865927

  173. 173.

    Kalita M., Malek W., Kaznowski A. Analysis of genetic relationship of Sarothamnus scoparius microsymbionts and Bradyrhizobium sp. by hybridization in microdilution wells. J. Biosci. Bioeng. 2004;97:158-161.

    Not in our library10.1016/s1389-1723(04)70185-1

  174. 174.

    Horn K., Parker I.M., Malek W., Rodríguez-Echeverria S., Matthew A.P. Disparate origins of Bradyrhizobium symbionts for invasive populations of Cytisus scoparius (Leguminosae) in North America. FEMS Microbiol. Ecol. 2014;89:89-98.

    Not in our library10.1111/1574-6941.12335

  175. 175.

    Chahboune R., Barrijal S., Moreno S., Bedmar E.J. Characterization of Bradyrhizobium species isolated from root nodules of Cytisus villosus grown in Morocco. Syst. Appl. Microbiol. 2011;34:440-445.

    Not in our library10.1016/j.syapm.2011.04.008

  176. 176.

    Cobo-Díaz J.F., Martínez-Hidalgo P., Fernández-González A.J., Martínez-Molina E., Toro N., Velázquez E., Fernández-López M. The endemic Genista versicolor from sierra nevada national park in Spain is nodulated by putative new Bradyrhizobium species and a novel symbiovar (sierranevadense). Syst. Appl. Microbiol. 2014;37:177-185.

    Not in our library10.1016/j.syapm.2013.09.008

  177. 177.

    Stroschein M.R.D., Eltz F.L.F., Antoniolli Z.I., Lupatini M., Vargas L.K., Giongo A., Pontelli M.P. Symbiotic efficiency and genetic characteristics of Bradyrhizobium sp. strain UFSM LA 1.3 isolated from Lupinus albescens (H. et Arn). Sci. Agric. 2010;67:702-706.

    Not in our library10.1590/s0103-90162010000600012

  178. 178.

    Granada C.E., Beneduzi A., Lisboa B.B., Turchetto-Zolet A.C., Vargas L.K., Passaglia L.M.P. Multilocus sequence analysis reveals taxonomic differences among Bradyrhizobium sp. symbionts of Lupinus albescens plants growing in arenized and non-arenized areas. Syst. Appl. Microbiol. 2015;38:323-329.

    Not in our library10.1016/j.syapm.2015.03.009

  179. 179.

    Velázquez E., Valverde A., Rivas R., Gomis V., Peix A., Gantois I., Igual J.M., León-Barrios M., Willems A., Mateos P.F., et al. Strains nodulating Lupinus albus on different contintents belong to several new chromosomal and symbiotic lineages within Bradyrhizobium. Antonie van Leeuwenhoek. 2010;97:363-376.

    Not in our library10.1007/s10482-010-9415-7

  180. 180.

    Stępkowski T., Żak M., Moulin L., Króliczak J., Golińska B., Narożna D., Safronova V.I., Mądrzak C.J. Bradyrhizobium canariense and Bradyrhizobium japonicum are the two dominant rhizobium species in root nodules of lupin and serradella plants growing in Europe. Syst. Appl. Microbiol. 2011;34:368-375.

    Not in our library10.1016/j.syapm.2011.03.002

  181. 181.

    Trujillo M.E., Willems A., Abril A., Planchuelo A.-M., Rivas R., Ludeña D., Mateos P.F., Martínez-Molina E., Velázquez E. Nodulation of Lupinus albus by strains of Ochrobactrum lupini sp. nov. Appl. Environ. Microbiol. 2005;71:1318-1327.

    Not in our library10.1128/aem.71.3.1318-1327.2005

  182. 182.

    Sánchez-Cañizares C., Rey L., Durán D., Temprano F., Sánchez-Jiménez P., Navarro A., Polajnar M., Imperial J., Ruiz-Argüeso T. Endosymbiotic bacteria nodulating a new endemic lupine Lupinus mariae-josephi from alkaline soils in Eastern Spain represent a new lineage within the Bradyrhizobium genus. Syst. Appl. Microbiol. 2011;34:207-215.

    Not in our library10.1016/j.syapm.2010.11.020

  183. 183.

    Durán D., Rey L., Sánchez-Cañizares C., Navarro A., Imperial J., Ruiz-Argueso T. Genetic diversity of indigenous rhizobial symbionts of the Lupinus mariae-josephae endemism form alkaline-limed soils within its area of distribution in Eastern Spain. Syst. Appl. Microbiol. 2013;36:128-136.

    Not in our library10.1016/j.syapm.2012.10.008

  184. 184.

    Bourebaba Y., Durán D., Boulila F., Ahnia H., Boulila A., Temprano F., Palacios J.M., Imperial J., Ruiz-Argüeso T., Rey L. Diversity of Bradyrhizobium strains nodulating Lupinus micranthus on both sides of the Western Mediterranean: Algeria and Spain. Syst. Appl. Microbiol. 2016;39:266-274.

    Not in our library10.1016/j.syapm.2016.04.006

  185. 185.

    Ryan-Salter T.P., Black A.D., Andrews M., Moot D.J. Identification and effectiveness of rhizobial strains that nodulate Lupinus polyphyllus. Proc. NZ Grassland Assoc. 2014;76:61-66.

    Not in our library

  186. 186.

    Guerrouj K., Ruíz-Díez B., Chahboune R., Ramírez-Bahena M.-H., Abdelmoumen H., Quiñones M.A., El Idrissi M.M., Velázquez E., Fernández-Pascual M., Bedmar E.J., Peix A. Definition of a novel symbiovar (sv. retamae) within Bradyrhizobium retamae sp. nov., nodulating Retama sphaerocarpa and Retama monosperma. Syst. Appl. Microbiol. 2013;36:218-223.

    Not in our library10.1016/j.syapm.2013.03.001

  187. 187.

    Farida B., Géraldine D., Abdelghani B., Djellali B., Said B., Gisèle L. Retama species growing in different ecological-climatic areas of northeastern Algeria have a narrow range of rhizobia that form a novel phylogenetic clade within the Bradyrhizobium genus. Syst. Appl. Microbiol. 2009;32:245-255.

    Not in our library10.1016/j.syapm.2009.01.005

  188. 188.

    Rodríguez-Echeverría S., Moreno S., Bedmar E.J. Genetic diversity of root nodulating bacteria associated with Retama sphaerocarpa in sites with different soil and environmental conditions. Syst. Appl. Microbiol. 2014;37:305-310.

    Not in our library10.1016/j.syapm.2013.11.003

  189. 189.

    Quatrini P., Scaglione G., Cardinale M., Caradonna F., Puglia A.M. Bradyrhizobium sp. nodulating the Mediterranean shrub Spanish broom (Spartium junceum L.). J. Appl. Microbiol. 2002;92:13-21.

    Not in our library10.1046/j.1365-2672.2002.01485.x

  190. 190.

    Liu W.Y.Y. Characterisation of Rhizobia and Studies on N2 Fixation of Common Weed Legumes in New Zealand. Ph.D. Thesis. 2014.

    Not in our library

  191. 191.

    Beukes C.W., Venter S.N., Law I.J., Phalane F.L., Steenkamp E.T. South African papilionoid legumes are nodulated by diverse Burkholderia with unique nodulation and nitrogen-fixation loci. PLoS ONE. 2013;8:e68406.

    Not in our library10.1371/journal.pone.0068406

  192. 192.

    Doignon-Bourcier F., Sy A., Willems A., Torck U., Dreyfus B., Gillis M., de Lajudie P. Diversity of bradyrhizobia from 27 tropical Leguminosae species native of Senegal. System. Appl. Microbiol. 1999;22:647-661.

    Not in our library10.1016/s0723-2020(99)80018-6

  193. 193.

    Lemaire B., Chimphango S.B.M., Stirton C., Rafudeen S., Honnay O., Smets E., Chen W.-M., Sprent J., James E.K., Muasya A.M. Biogeographical patterns of legume-nodulating Burkholderia spp.: From African fynbos to continental scales. Appl. Environ. Microbiol. 2016;82:5099-5115.

    Not in our library10.1128/aem.00591-16

  194. 194.

    Yang W., Kong Z., Chen W., Wei G. Genetic diversity and symbiotic evolution of rhizobia from root nodules of Coronilla varia. Syst. Appl. Microbiol. 2013;36:49-55.

    Not in our library10.1016/j.syapm.2012.10.004

  195. 195.

    Stępkowski T., Moulin L., Krzyżańska A., McInnes A., Law I.J., Howieson J. European origin of Bradyrhizobium populations infecting lupins and serradella in soils of Western Australia and South Africa. Appl. Environ. Microbiol. 2005;71:7041-7052.

    Not in our library10.1128/aem.71.11.7041-7052.2005

  196. 196.

    Kesari V., Ramesh A.M., Rangan L. Rhizobium pongamiae sp. nov. from root nodules of Pongamia pinnata. Biomed. Res. Int. 2013;2013:165198.

    Not in our library10.1155/2013/165198

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    Lemaire B., van Cauwenberghe J., Verstraete B., Chimphango S., Stirton C., Honnay O., Smets E., Sprent J., James E.K., Muasya A.M. Characterization of the papilionoid-Burkholderia interaction in the Fynbos biome: The diversity and distribution of β-rhizobia nodulating Podalyria calyptrata (Fabaceae, Podalyrieae). Syst. Appl. Microbiol. 2016;39:41-48.

    Not in our library10.1016/j.syapm.2015.09.006

  198. 198.

    Ulrich A., Zaspel I. Phylogenetic diversity of rhizobial strains nodulating Robinia pseudoacacia L. Microbiology. 2000;146:2997-3005.

    Not in our library10.1099/00221287-146-11-2997

  199. 199.

    Mierzwa B., Wdowiak-Wróbel S., Malek W. Phenotypic, genomic and phylogenetic characteristics of rhizobia isolated from root nodules of Robinia pseudoacacia (black locust) growing in Poland and Japan. Arch. Microbiol. 2009;191:697-710.

    Not in our library10.1007/s00203-009-0500-0

  200. 200.

    Chen W.-M., Lee T.-M. Genetic and phenotypic diversity of rhizobial isolates from sugarcane-Sesbania cannabina-rotation fields. Biol. Fertil. Soils. 2001;34:14-20.

    Not in our library10.1007/s003740100346

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    Wang Y.C., Wang F., Hou B.C., Wang E.T., Chen W.F., Sui X.H., Chen W.X., Li Y., Zhang Y.B. Proposal of Ensifer psoraleae sp. nov., Ensifer sesbaniae sp. nov., Ensifer morelense comb. nov. and Ensifer americanum comb. nov. Syst. Appl. Microbiol. 2013;36:467-473.

    Not in our library10.1016/j.syapm.2013.05.001

  202. 202.

    Li Y., Li X., Liu Y., Wang E.T., Ren C., Liu W., Xu H., Wu H., Jiang N., Li Y., Zhang X., Xie Z. Genetic diversity and community structure of rhizobia nodulating Sesbania cannabina in saline-alkaline soils. Syst. Appl. Microbiol. 2016;39:195-202.

    Not in our library10.1016/j.syapm.2016.02.004

  203. 203.

    Wang E.T., van Berkum P., Beyene D., Sui X.H., Dorado O., Chen W.X., Martínez-Romero E. Rhizobium huautlense sp. nov., a symbiont of Sesbania herbacea that has a close phylogenetic relationship with Rhizobium galegae. Int. J. Syst. Bacteriol. 1998;48:687-699.

    Not in our library10.1099/00207713-48-3-687

  204. 204.

    Blanco A.R., Csukasi F., Abreu C., Sicardi M. Characterization of rhizobia from Sesbania species native to seasonally wetland areas in Uruguay. Biol. Fertil. Soils. 2008;44:925-932.

    Not in our library10.1007/s00374-008-0275-5

  205. 205.

    Dreyfus B., Garcia J.L., Gillis M. Characterisation of Azorhizobium caulinodans gen. nov., sp. nov., a stem nodulating nitrogen-fixing bacterium isolated from Sesbania rostrata. Int. J. Syst. Bacteriol. 1988;38:89-98.

    Not in our library10.1099/00207713-38-1-89

  206. 206.

    De Moreira F.M.S., Cruz L., de Faria S.M., Marsh T., Martínez-Romero E., de Pedrosa F.O., Pitard R.M., Young J.P.W. Azorhizobium doebereinerae sp. nov. microsymbiont of Sesbania virgata (Caz.) Pers. Syst. Appl. Microbiol. 2006;29:197-206.

    Not in our library10.1016/j.syapm.2005.09.004

  207. 207.

    Zhao L., Deng Z., Yang W., Cao Y., Wang E., Wei G. Diverse rhizobia associated with Sophora alopecuroides grown in different regions of Loess Plateau in China. Syst. Appl. Microbiol. 2010;33:468-477.

    Not in our library10.1016/j.syapm.2010.08.004

  208. 208.
    Rhizobial Diversity and Nodulation Characteristics of the Extremely Promiscuous Legume Sophora flavescens · 2015
    Not checked
  209. 209.

    Jiao Y.S., Yan H., Ji Z.J., Liu Y.H., Sui X.H., Zhang X.X., Wang E.T., Chen W.X., Chen W.F. Phyllobacterium sophorae sp. nov., a symbiotic bacterium isolated from root nodules of Sophora flavescens. Int. J. Syst. Evol. Microbiol. 2015;65:399-406.

    Not in our library10.1099/ijs.0.067017-0

  210. 210.

    Tan H.W., Heenan P.B., de Meyer S.E., Willems A., Andrews M. Diverse novel mesorhizobia nodulate New Zealand native Sophora species. Syst. Appl. Microbiol. 2015;38:91-98.

    Not in our library10.1016/j.syapm.2014.11.003

  211. 211.

    Zhao L., Wang X., Huo H., Yuan G., Sun Y., Zhang D., Cao Y., Xu L., Wei G. Phylogenetic diversity of Ammopiptanthus rhizobia and distribution of rhizobia associated with Ammopiptanthus mongolicus in diverse regions of Northwest China. Microb. Ecol. 2016;72:231-239.

    Not in our library10.1007/s00248-016-0759-z

  212. 212.

    Donate-Correa J., Léon-Barrios M., Hernández M., Pérez-Galdona R., del Arco-Aguilar M. Different Mesorhizobium species sharing the same symbiotic genes nodulate the shrub legume Anagyris latifolia. Syst. Appl. Microbiol. 2007;30:615-623.

    Not in our library10.1016/j.syapm.2007.07.002

  213. 213.

    Ampomah O.Y., Huss-Danell K. Nodulation of Thermopsis lupinoides by a Mesorhizobium huakuii strain with a unique nodA gene in Kamtchatka, Russia. Appl. Environ. Microbiol. 2011;77:5513-5516.

    Not in our library10.1128/aem.00622-11

  214. 214.

    Bianco L., Angelini J., Fabra A., Malpassi R. Diversity and symbiotic effectiveness of indigenous rhizobia-nodulating Adesmia bicolor in soils of Central Argentina. Curr. Microbiol. 2013;66:174-184.

    Not in our library10.1007/s00284-012-0260-y

  215. 215.

    Noisangiam R., Teamtisong K., Tittabutr P., Boonkerd N., Toshiki U., Minamisawa K., Teaumroong N. Genetic diversity, symbiotic evolution, and proposed infection process of Bradyrhizobium strains isolated from root nodules of Aeschynomene americana L. in Thailand. Appl. Environ. Microbiol. 2012;78:6236-6250.

    Not in our library10.1128/aem.00897-12

  216. 216.

    Van Berkum P., Eardly B.D. The aquatic budding bacterium Blastobacter denitrificans is a nitrogen-fixing symbiont of Aeschynomene indica. Appl. Environ. Microbiol. 2002;68:1132-1136.

    Not in our library10.1128/aem.68.3.1132-1136.2002

  217. 217.

    Montecchia M.S., Kerber N.L., Pucheu N.L., Perticari A., García A.F. Analysis of genomic diversity among photosynthetic stem-nodulating rhizobial strains from Northeast Argentina. Syst. Appl. Microbiol. 2002;25:423-433.

    Not in our library10.1078/0723-2020-00123

  218. 218.

    Chen J.Y., Gu J., Wang E.T., Ma X.X., Kang S.T., Huang L.Z., Cao X.P., Li L.B., Wu Y.L. Wild peanut Arachis duranensis are nodulated by diverse and novel Bradyrhizobium species in acid soils. Syst. Appl. Microbiol. 2014;37:525-532.

    Not in our library10.1016/j.syapm.2014.05.004

  219. 219.

    Urtz B.E., Elkan G.H. Genetic diversity among Bradyrhizobium isolates that effectively nodulate peanut (Arachis hypogaea). Can. J. Microbiol. 1996;42:1121-1130.

    Not in our library10.1139/m96-144

  220. 220.

    Yang J.K., Xie F.L., Zou J., Zhou Q., Zhou J.C. Polyphasic characteristics of bradyrhizobia isolated from nodules of peanut (Arachis hypogaea) in China. Soil Biol. Biochem. 2005;37:141-153.

    Not in our library10.1016/j.soilbio.2004.06.016

  221. 221.

    Taurian T., Ibañez F., Fabra A., Aguilar O.M. Genetic diversity of rhizobia nodulating Arachis hypogaea L. in Central Argentinean soils. Plant Soil. 2006;282:41-52.

    Not in our library10.1007/s11104-005-5314-5

  222. 222.

    El-Akhal M.R., Rincón A., Arenal F., Lucas M.M., El Mourabit N., Barrijal S., Pueyo J.J. Genetic diversity and symbiotic efficiency of rhizobial isolates obtained from nodules of Arachis hypogaea in northwestern Morocco. Soil Biol. Biochem. 2008;40:2911-2914.

    Not in our library10.1016/j.soilbio.2008.08.005

  223. 223.

    Steenkamp E.T., Stępkowski T., Przymusiak A., Botha W.J., Law I.J. Cowpea and peanut in southern Africa are nodulated by diverse Bradyrhizobium strains harboring nodulation genes that belong to the large pantropical clade common in Africa. Mol. Phylogenet. Evol. 2008;48:1131-1144.

    Not in our library10.1016/j.ympev.2008.04.032

  224. 224.

    Chang Y.L., Wang J.Y., Wang E.T., Liu H.C., Sui X.H., Chen W.X. Bradyrhizobium lablabi sp. nov., isolated from effective nodules of Lablab purpureus and Arachis hypogaea. Int. J. Syst. Evol. Microbiol. 2011;61:2496-2502.

    Not in our library10.1099/ijs.0.027110-0

  225. 225.

    Muñoz V., Ibañez F., Tonelli M.L., Valetti L., Anzuay M.S., Fabra A. Phenotypic and phylogenetic characterization of native peanut Bradyrhizobium isolates obtained from Córdoba, Argentina. Syst. Appl. Microbiol. 2011;34:446-452.

    Not in our library10.1016/j.syapm.2011.04.007

  226. 226.

    Wang R., Chang Y.L., Zheng W.T., Zhang D., Zhang X.X., Sui X.H., Wang E.T., Hu J.Q., Zhang L.Y., Chen W.X. Bradyrhizobium arachidis sp. nov., isolated from effective nodules of Arachis hypogaea grown in China. Syst. Appl. Microbiol. 2013;36:101-105.

    Not in our library10.1016/j.syapm.2012.10.009

  227. 227.

    Grönemeyer J.L., Kulkarni A., Berkelmann D., Hurek T., Reinhold-Hurek B. Rhizobia indigenous to the Okavango region in Sub-Saharan Africa: Diversity, adaptations, and host specificity. Appl. Environ. Microbiol. 2014;80:7244-7257.

    Not in our library10.1128/aem.02417-14

  228. 228.

    Li Y.H., Wang R., Zhang X.X., Young J.P.W., Wang E.T., Sui X.H., Chen W.X. Bradyrhizobium guangdongense sp. nov. and Bradyrhizobium guangxiense sp. nov., isolated from effective nodules of peanut. Int. J. Syst. Evol. Microbiol. 2015;65:4655-4661.

    Not in our library10.1099/ijsem.0.000629

  229. 229.

    Chen J., Hu M., Ma H., Wang Y., Wang E.T., Zhou Z., Gu J. Genetic diversity and distribution of bradyrhizobia nodulating peanut in acid-neutral soils in Guangdong Province. Syst. Appl. Microbiol. 2016;39:418-427.

    Not in our library10.1016/j.syapm.2016.06.002

  230. 230.
    Diversity and nitrogen fixation efficiency of rhizobia isolated from nodules of Centrolobium paraense · 2014
    Not checked
  231. 231.

    Zilli J.E., Baraúna A.C., da Silva K., de Meyer S.E., Farias E.N.C., Kaminski P.E., da Costa I.B., Ardley J.K., Willems A., Camacho N.N., et al. Bradyrhizobium neotropicale sp. nov., isolate from effective nodules of Centrolobium paraense. Int. J. Syst. Evol. Microbiol. 2014;64:3950-3957.

    Not in our library10.1099/ijs.0.065458-0

  232. 232.

    Rasolomampianina R., Bailly X., Fetiarison R., Rabevohitra R., Béna G., Ramaroson L., Raherimandimby M., Moulin L., de Lajudie P., Dreyfus B., et al. Nitrogen-fixing nodules from rose wood legume trees (Dalbergia spp.) endemic to Madagascar host seven different genera belonging to α- and β-proteobacteria. Mol. Ecol. 2005;14:4135-4146.

    Not in our library10.1111/j.1365-294x.2005.02730.x

  233. 233.

    Le Roux C., Muller F., Bouvet J.-M., Dreyfus B., Béna G., Galiana A., Bâ A.M. Genetic diversity patterns and functional traits of Bradyrhizobium strains associated with Pterocarpus officinalis Jacq. in Caribbean islands and Amazonian forest (French Guiana). Microb. Ecol. 2014;68:329-338.

    Not in our library10.1007/s00248-014-0392-7

  234. 234.

    Gueye F., Moulin L., Sylla S., Ndoye I., Béna G. Genetic diversity and distribution of Bradyrhizobium and Azorhizobium strains associated with the herb legume Zornia glochidiata sampled from across Senegal. Syst. Appl. Microbiol. 2009;32:387-399.

    Not in our library10.1016/j.syapm.2009.04.004

  235. 235.

    Gu J., Wang E.T., Chen W.X. Genetic diversity of rhizobia associated with Desmodium species grown in China. Lett. Appl. Microbiol. 2007;44:286-292.

    Not in our library10.1111/j.1472-765x.2006.02071.x

  236. 236.

    Xu K.W., Zou L., Penttinen P., Zeng X., Liu M., Zhao K., Chen C., Chen Y.X., Zhang X. Diversity and phylogeny of rhizobia associated with Desmodium spp. in Panxi, Sichuan, China. Syst. Appl. Microbiol. 2016;39:33-40.

    Not in our library10.1016/j.syapm.2015.10.005

  237. 237.

    Delamuta J.R.M., Ribeiro R.A., Ormeño-Orrillo E., Parma M.M., Melo I.S., Martínez-Romero E., Hungria M. Bradyrhizobium tropiciagri sp. nov. and Bradyrhizobium embrapense sp. nov., nitrogen-fixing symbionts of tropical forage legumes. Int. J. Syst. Evol. Microbiol. 2015;65:4424-4433.

    Not in our library10.1099/ijsem.0.000592

  238. 238.

    Chen W.-X., Tan Z.-Y., Gao J.-L., Li Y., Wang E.-T. Rhizobium hainanense sp. nov., isolated from tropical legumes. Int. J. Syst. Bacteriol. 1997;47:870-873.

    Not in our library10.1099/00207713-47-3-870

  239. 239.

    Lin D.X., Man C.X., Wang E.T., Chen W.X. Diverse rhizobia that nodulate two species of Kummerowia in China. Arch. Microbiol. 2007;188:495-507.

    Not in our library10.1007/s00203-007-0271-4

  240. 240.

    Yao Z.Y., Kan F.L., Wang E.T., Wei G.H., Chen W.X. Characterization of rhizobia that nodulate legume species of the genus Lespedeza and description of Bradyrhizobium yuanmingense sp. nov. Int. J. Syst. Evol. Microbiol. 2002;52:2219-2230.

    Not in our library10.1099/00207713-52-6-2219

  241. 241.

    Parker M.A., Doyle J.L., Doyle J.J. Comparative phylogeography of Amphicarpaea legumes and their root-nodule symbionts in Japan and North America. J. Biogeogr. 2004;31:425-434.

    Not in our library10.1046/j.0305-0270.2003.01030.x

  242. 242.

    Araujo J., Díaz-Alcántara C.-A., Velázquez E., Urbano B., González-Andrés F. Bradyrhizobium yuanmingense related strains form nitrogen-fixing symbiosis with Cajanus cajan L. in Dominican Republic and are efficient biofertilizers to replace N fertilization. Sci. Hort. 2015;192:421-428.

    Not in our library10.1016/j.scienta.2015.06.009

  243. 243.

    Chen W.-M., Lee T.-M., Lan C.-C., Cheng C.-P. Characterization of halotolerant rhizobia isolated from root nodules of Canavalia rosea from seaside areas. FEMS Microbiol. Ecol. 2000;34:9-16.

    Not in our library10.1111/j.1574-6941.2000.tb00749.x

  244. 244.

    Xu L.M., Ge C., Cui Z., Li J., Fan H. Bradyrhizobium liaoningense sp. nov., isolated from the root nodules of soybeans. Int. J. Syst. Bacteriol. 1995;45:706-711.

    Not in our library10.1099/00207713-45-4-706

  245. 245.

    Barcellos F.G., Menna P., da Batista J.S.S., Hungria M. Evidence of horizontal transfer of symbiotic genes from a Bradyrhizobium japonicum inoculant strain to indigenous diazotrophs Sinorhizobium (Ensifer) fredii and Bradyrhizobium elkanii in a Brazilian savannah soil. Appl. Environ. Microbiol. 2007;73:2635-2643.

    Not in our library10.1128/aem.01823-06

  246. 246.

    Appunu C., Sasirekha N., Prabavathy V.R., Nair S. A significant proportion of indigenous rhizobia from India associated with soybean (Glycine max L.) distinctly belong to Bradyrhizobium and Ensifer genera. Biol. Fertil. Soils. 2009;46:57-63.

    Not in our library10.1007/s00374-009-0405-8

  247. 247.

    Zhang Y.M., Li Y., Chen W.F., Wang E.T., Tian C.F., Li Q.Q., Zhang Y.Z., Sui X.H., Chen W.X. Biodiversity and biogeography of rhizobia associated with soybean plants grown in the North China Plain. Appl. Environ. Microbiol. 2011;77:6331-6342.

    Not in our library10.1128/aem.00542-11

  248. 248.

    Jaiswal S.K., Anand A., Dhar B., Vaishampayan A. Genotypic characterization of phage-typed indigenous soybean Bradyrhizobia and their host range symbiotic effectiveness. Microb. Ecol. 2012;63:116-126.

    Not in our library10.1007/s00248-011-9950-4

  249. 249.

    Tang J., Bromfield E.S.P., Rodrigue N., Cloutier S., Tambong J.T. Microevolution of symbiotic Bradyrhizobium populations associated with soybeans in east North America. Ecol. Evol. 2012;2:2943-2961.

    Not in our library10.1002/ece3.404

  250. 250.

    Wang J.Y., Wang R., Zhang Y.M., Liu H.C., Chen W.F., Wang E.T., Sui X.H., Chen W.X. Bradyrhizobium daqingense sp. nov., isolated from soybean nodules. Int. J. Syst. Evol. Microbiol. 2013;63:616-624.

    Not in our library10.1099/ijs.0.034280-0

  251. 251.

    Ribeiro R.A., Ormeño-Orrillo E., Dall’Agnol R.F., Graham P.H., Martinez-Romero E., Hungria M. Novel Rhizobium lineages isolated from root nodules of the common bean (Phaseolus vulgaris L.) in Andean and Mesoamerican areas. Res. Microbiol. 2013;164:740-748.

    Not in our library10.1016/j.resmic.2013.05.002

  252. 252.

    Peng G.X., Tan Z.Y., Wang E.T., Reinhold-Hurek B., Chen W.F., Chen W.X. Identification of isolates from soybean nodules in Xinjiang Region as Sinorhizobium xinjiangense and genetic differentiation of S. xinjiangense from Sinorhizobium fredii. Int. J. Syst. Evol. Microbiol. 2002;52:457-462.

    Not in our library10.1099/00207713-52-2-457

  253. 253.

    Li Q.Q., Wang E.T., Chang Y.L., Zhang Y.Z., Zhang Y.M., Sui X.H., Chen W.F., Chen W.X. Ensifer sojae sp. nov., isolated from root nodules of Glycine max grown in saline-alkaline soils. Int. J. Syst. Evol. Microbiol. 2011;61:1981-1988.

    Not in our library10.1099/ijs.0.025049-0

  254. 254.

    Alam F., Bhuiyan M.A.H., Alam S.S., Waghmode T.R., Kim P.J. Effect of Rhizobium sp. BARIRGm901 inoculation on nodulation, nitrogen fixation and yield of soybean (Glycine max) genotypes in gray terrace soil. Biosci. Biotechnol. Biochem. 2015;1660-1668.

    Not in our library10.1080/09168451.2015.1044931

  255. 255.

    Wu L.J., Wang H.Q., Wang E.T., Chen W.X., Tian C.F. Genetic diversity of nodulating and non-nodulating rhizobia associated with wild soybean (Glycine soja Sieb. & Zucc.) in different ecoregions of China. FEMS Microbiol. Ecol. 2011;76:439-450.

    Not in our library10.1111/j.1574-6941.2011.01064.x

  256. 256.

    Zhao L., Fan M., Zhang D., Yang R., Zhang F., Xu L., Wei X., Shen Y., Wei G. Distribution and diversity of rhizobia associated with wild soybean (Glycine soja Sieb. & Zucc.) in Northwest China. Syst. Appl. Microbiol. 2014;37:449-456.

    Not in our library10.1016/j.syapm.2014.05.011

  257. 257.

    Fuentes J.B., Abe M., Uchiumi T., Suzuki A., Higashi S. Symbiotic root nodule bacteria isolated from yam bean (Pachyrhizus erosus). J. Gen. Appl. Microbiol. 2002;48:181-191.

    Not in our library10.2323/jgam.48.181

  258. 258.

    Rodríguez-Navarro D.N., Camacho M., Leidi E.O., Rivas R., Velázquez E. Phenotypic and genotypic characterization of rhizobia from diverse geographical origin that nodulate Pachyrhizus species. Syst. Appl. Microbiol. 2004;27:737-745.

    Not in our library10.1078/0723202042369839

  259. 259.

    Ramírez-Bahena M.H., Peix A., Rivas R., Camacho M., Rodríguez-Navarro D.N., Mateos P.F., Martínez-Molina E., Willems A., Velázquez E. Bradyrhizobium pachyrhizi sp. nov. and Bradyrhizobium jicamae sp. nov., isolated from effective nodules of Pachyrhizus erosus. Int. J. Syst. Evol. Microbiol. 2009;59:1929-1934.

    Not in our library10.1099/ijs.0.006320-0

  260. 260.

    López-López A., Negrete-Yankelevich S., Rogel M.A., Ormeño-Orrillo E., Martínez J., Martínez-Romero E. Native bradyrhizobia from Los Tuxtlas in Mexico are symbionts of Phaseolus lunatus (Lima bean). Syst. Appl. Microbiol. 2013;36:33-38.

    Not in our library10.1016/j.syapm.2012.10.006

  261. 261.

    Durán D., Rey L., Mayo J., Zúñiga-Dávila D., Imperial J., Ruiz-Argüeso T., Martínez-Romero E., Ormeño-Orrillo E. Bradyrhizobium paxllaeri sp. nov. and Bradyrhizobium icense sp. nov., nitrogen-fixing rhizobial symbionts of Lima bean (Phaseolus lunatus L.) in Peru. Int. J. Syst. Evol. Microbiol. 2014;64:2072-2078.

    Not in our library10.1099/ijs.0.060426-0

  262. 262.

    Matsubara M., Zúñiga-Dávila D. Phenotypic and molecular differences among rhizobia that nodulate Phaseolus lunatus in the Supe valley in Peru. Ann. Microbiol. 2015;65:1803-1808.

    Not in our library10.1007/s13213-015-1054-9

  263. 263.

    Wang L., Cao Y., Wang E.T., Qiao Y.J., Jiao S., Liu Z.S., Zhao L., Wei G.H. Biodiversity and biogeography of rhizobia associated with common bean (Phaseolus vulgaris L.) in Shaanxi Province. Syst. Appl. Microbiol. 2016;39:211-219.

    Not in our library10.1016/j.syapm.2016.02.001

  264. 264.

    Talbi C., Delgado M.J., Girard L., Ramirez-Trujillo A., Caballero-Mellado J., Bedmar E.J. Burkholderia phymatum strains capable of nodulating Phaseolus vulgaris are present in Moroccan soils. Appl. Environ. Microbiol. 2010;76:4587-4591.

    Not in our library10.1128/aem.02886-09

  265. 265.

    Dall’Agnol R.F., Plotegher F., Souza R.C., Mendes I.C., dos Reis Junior F.B., Béna G., Moulin L., Hungria M. Paraburkholderia nodosa is the main N2-fixing species trapped by promiscuous common bean (Phaseolus vulgaris L.) in the Brazilian “Cerradão”. FEMS Microbiol. Ecol. 2016;92:fiw108.

    Not in our library10.1093/femsec/fiw108

  266. 266.

    Mhamdi R., Laguerre G., Aouani M.E., Mars M., Amarger N. Different species and symbiotic genotypes of field rhizobia can nodulate Phaseolus vulgaris in Tunisian soils. FEMS Microbiol. Ecol. 2002;41:77-84.

    Not in our library10.1111/j.1574-6941.2002.tb00968.x

  267. 267.

    Mnasri B., Mrabet M., Laguerre G., Aouani M.E., Mhamdi R. Salt-tolerant rhizobia isolated from a Tunisian oasis that are highly effective for symbiotic N2-fixation with Phaseolus vulgaris constitute a novel biovar (bv. mediterranense) of Sinorhizobium meliloti. Arch. Microbiol. 2007;187:79-85.

    Not in our library10.1007/s00203-006-0173-x

  268. 268.

    Mnasri B., Saïdi S., Chihaoui S.-A., Mhamdi R. Sinorhizobium americanum symbiovar mediterranense is a predominant symbiont that nodulates and fixes nitrogen with common bean (Phaseolus vulgaris L.) in a Northern Tunisian field. Syst. Appl. Microbiol. 2012;35:263-269.

    Not in our library10.1016/j.syapm.2012.04.003

  269. 269.

    Martínez-Romero E., Segovia L., Mercante F.M., Franco A.A., Graham P., Pardo M.A. Rhizobium tropici, a novel species nodulating Phaseolus vulgaris L. beans and Leucaena sp. trees. Int. J. System. Bacteriol. 1991;41:417-426.

    Not in our library10.1099/00207713-41-3-417

  270. 270.

    Amarger N., Macheret V., Laguerre G. Rhizobium gallicum sp. nov. and Rhizobium giardinii sp. nov., from Phaseolus vulgaris nodules. Int. J. Syst. Bacteriol. 1997;47:996-1006.

    Not in our library10.1099/00207713-47-4-996

  271. 271.

    Mostasso L., Mostasso F.L., Dias B.G., Vargas M.A.T., Hungria M. Selection of bean (Phaseolus vulgaris L.) rhizobial strains for the Brazilian Cerrados. Field Crops Res. 2002;73:121-132.

    Not in our library10.1016/s0378-4290(01)00186-1

  272. 272.

    Valverde A., Igual J.M., Peix A., Cervantes E., Velázquez E. Rhizobium lusitanum sp. nov. a bacterium that nodulates Phaseolus vulgaris. Int. J. System. Evol. Microbiol. 2006;56:2631-2637.

    Not in our library10.1099/ijs.0.64402-0

  273. 273.

    Wang F., Wang E.T., Wu L.J., Sui X.H., Li Y., Chen W.X. Rhizobium vallis sp. nov., isolated from nodules of three leguminous species. Int. J. Syst. Evol. Microbiol. 2011;61:2582-2588.

    Not in our library10.1099/ijs.0.026484-0

  274. 274.

    De Ribeiro P.R.A., dos Santos J.V., da Costa E.M., Lebbe L., Assis E.S., Louzada M.O., Guimarães A.A., Willems A., de Moreira F.M.S. Symbiotic efficiency and genetic diversity of soybean bradyrhizobia in Brazilian soils. Agric. Ecosyst. Environ. 2015;212:85-93.

    Not in our library10.1016/j.agee.2015.06.017

  275. 275.

    Cao Y., Wang E.-T., Zhao L., Chen W.-M., Wei G.-H. Diversity and distribution of rhizobia nodulated with Phaseolus vulgaris in two ecoregions of China. Soil Biol. Biochem. 2014;78:128-137.

    Not in our library10.1016/j.soilbio.2014.07.026

  276. 276.

    Sarr P.S., Araki S., Begoude D.A., Yemefack M., Manga G.A., Yamakawa T., Htwe A.Z. Phylogeny and nitrogen fixation potential of Bradyrhizobium species isolated from the legume cover crop Pueraria phaseoloides (Roxb.) Benth. in Eastern Cameroon. Soil Sci. Plant Nutr. 2016;62:13-19.

    Not in our library10.1080/00380768.2015.1086279

  277. 277.

    Garau G., Yates R.J., Deiana P., Howieson J.G. Novel strains of nodulating Burkholderia have a role in nitrogen fixation with papilionoid herbaceous legumes adapted to acid, infertile soils. Soil Biol. Biochem. 2009;41:125-134.

    Not in our library10.1016/j.soilbio.2008.10.011

  278. 278.

    De Meyer S.E., Cnockaert M., Ardley J.K., Trengove R.D., Garau G., Howieson J.G., Vandamme P. Burkholderia rhynchosiae sp. nov., isolated from Rhynchosia ferulifolia root nodules. Int. J. Syst. Evol. Microbiol. 2013;63:3944-3949.

    Not in our library10.1099/ijs.0.048751-0

  279. 279.

    Han L.L., Wang E.T., Lu Y.L., Zhang Y.F., Sui X.H., Chen W.F., Chen W.X. Bradyrhizobium spp. and Sinorhizobium fredii are predominant in root nodules of Vigna angularis, a native legume crop in the subtropical region of China. J. Microbiol. 2009;47:287-296.

    Not in our library10.1007/s12275-009-0001-5

  280. 280.

    Zhang Y.F., Wang E.T., Tian C.F., Wang F.Q., Han L.L., Chen W.F., Chen W.X. Bradyrhizobium elkanii, Bradyrhizobium yuanmingense and Bradyrhizobium japonicum are the main rhizobia associated with Vigna unguiculata and Vigna radiata in the subtropical region of China. FEMS Microbiol. Lett. 2008;285:146-154.

    Not in our library10.1111/j.1574-6968.2008.01169.x

  281. 281.

    Risal C.P., Djedidi S., Dhakal D., Ohkama-Ohtsu N., Sekimoto H., Yokoyama T. Phylogenetic diversity and symbiotic functioning in mungbean (Vigna radiata L. Wilczek) bradyrhizobia from contrast agro-ecological regions of Nepal. Syst. Appl. Microbiol. 2012;35:45-53.

    Not in our library10.1016/j.syapm.2011.06.004

  282. 282.

    Onyango B., Anyango B., Nyunja R., Koech P.K., Skilton R.A., Stomeo F. Morphological, genetic and symbiotic characterization of root nodule bacteria isolated from Bambara groundnuts (Vigna subterranea L. Verdc) from soils of Lake Victoria basin, western Kenya. J. Appl. Biol. Biotechnol. 2015;3:1-10.

    Not in our library

  283. 283.

    Guimarães A.A., Jaramillo P.M.D., Nóbrega R.S.A., Florentino L.A., Silva K.B., de Moreira F.M.S. Genetic and symbiotic diversity of nitrogen-fixing bacteria isolated from agricultural soils in the Western Amazon by using cowpea as the trap plant. Appl. Environ. Microbiol. 2012;78:6726-6733.

    Not in our library10.1128/aem.01303-12

  284. 284.

    Bejarano A., Ramírez-Bahena M.-H., Velázquez E., Peix A. Vigna unguiculata is nodulated in Spain by endosymbionts of Genisteae legumes and by a new symbiovar (vignae) of the genus Bradyrhizobium. Syst. Appl. Microbiol. 2014;37:533-540.

    Not in our library10.1016/j.syapm.2014.04.003

  285. 285.

    Silva F.V., de Meyer S.E., Simões-Araújo J.L., da Barbé T.C., Xavier G.R., O’Hara G., Ardley J.K., Rumjanek N.G., Willems A., Zilli J.E. Bradyrhizobium manausense sp. nov., isolated from effective nodules of Vigna unguiculata grown in Brazilian Amazonian rainforest soils. Int. J. Syst. Evol. Microbiol. 2014;64:2358-2363.

    Not in our library10.1099/ijs.0.061259-0

  286. 286.

    Radl V., Simões-Araújo J.L., Leite J., Passos S.R., Martins L.M.V., Xavier G.R., Rumjanek N.G., Baldani J.I., Zilli J.E. Microvirga vignae sp. nov., a root nodule symbiotic bacterium isolated from cowpea grown in semi-arid Brazil. Int. J. Syst. Evol. Microbiol. 2014;64:725-730.

    Not in our library10.1099/ijs.0.053082-0

  287. 287.

    Kanu S.A., Dakora F.D. Symbiotic nitrogen contribution and biodiversity of root-nodule bacteria nodulating Psoralea species in the Cape Fynbos, South Africa. Soil Biol. Biochem. 2012;54:68-76.

    Not in our library10.1016/j.soilbio.2012.05.017

  288. 288.

    Lorite M.J., Donate-Correa J., del Arco-Aguilar M., Galdona R.P., Sanjuán J., Léon-Barrios M. Lotus endemic to the Canary Islands are nodulated by diverse and novel rhizobial species and symbiotypes. Syst. Appl. Microbiol. 2010;33:282-290.

    Not in our library10.1016/j.syapm.2010.03.006

  289. 289.

    Jarvis B.D.W., van Berkum P., Chen W.X., Nour S.M., Fernandez M.P., Cleyet-Marel J.C., Gillis M. Transfer of Rhizobium loti, Rhizobium huakuii, Rhizobium ciceri, Rhizobium mediterraneum, and Rhizobium tianshanense to Mesorhizobium gen. nov. Int. J. Syst. Bacteriol. 1997;47:895-898.

    Not in our library10.1099/00207713-47-3-895

  290. 290.

    Lorite M.J., Muñoz S., Olivares J., Soto M.J., Sanjuán J. Characterization of strains unlike Mesorhizobium loti that nodulate Lotus spp. in saline soils of Granada, Spain. Appl. Environ. Microbiol. 2010;76:4019-4026.

    Not in our library10.1128/aem.02555-09

  291. 291.

    Marcos-García M., Menéndez E., Cruz-González X., Velázquez E., Mateos P.F., Rivas R. The high diversity of Lotus corniculatus endosymbionts in soils of northwest Spain. Symbiosis. 2015;67:11-20.

    Not in our library10.1007/s13199-015-0368-5

  292. 292.

    Léon-Barrios M., Lorite M.J., Donate-Correa J., Sanjuán J. Ensifer meliloti bv. lancerottense establishes nitrogen-fixing symbiosis with Lotus endemic to the Canary Islands and shows distinctive symbiotic genotypes and host range. Syst. Appl. Microbiol. 2009;32:413-420.

    Not in our library10.1016/j.syapm.2009.04.003

  293. 293.

    Estrella M.J., Muñoz S., Soto M.J., Ruiz O., Sanjuán J. Genetic diversity and host range of rhizobia nodulating Lotus tenuis in typical soils of the Salado River basin (Argentina). Appl. Environ. Microbiol. 2009;75:1088-1098.

    Not in our library10.1128/aem.02405-08

  294. 294.

    Sannazzaro A.I., Bergottini V.M., Paz R.C., Castagno L.N., Menéndez A.B., Ruiz O.A., Pieckenstain F.L., Estrella M.J. Comparative symbiotic performance of native rhizobia of the Flooding Pampa and strains currently used for inoculating Lotus tenuis in this region. Antonie van Leeuwenhoek. 2011;99:371-379.

    Not in our library10.1007/s10482-010-9502-9

  295. 295.

    Lorite M.J., Videira e Castro I., Muñoz S., Sanjuán J. Phylogenetic relationship of Lotus uliginosus symbionts with bradyrhizobia nodulating genistoid legumes. FEMS Microbiol. Ecol. 2012;79:454-464.

    Not in our library10.1111/j.1574-6941.2011.01230.x

  296. 296.

    Lindström K. Rhizobium galegae, a new species of legume root nodule bacteria. Int. J. Syst. Bacteriol. 1989;39:365-367.

    Not in our library10.1099/00207713-39-3-365

  297. 297.

    Franche C., Lindström K., Elmerich C. Nitrogen-fixing bacteria associated with leguminous and non-leguminous plants. Plant Soil. 2009;321:35-59.

    Not in our library10.1007/s11104-008-9833-8

  298. 298.

    Wojciechowski M.F., Lavin M., Sanderson M.J. A phylogeny of legumes (Leguminosae) based on analysis of the plastid MATK gene resolves many well-supported subclades within the family. Am. J. Bot. 2004;91:1846-1862.

    Not in our library10.3732/ajb.91.11.1846

  299. 299.

    Schwarz E.N., Ruhlman T.A., Sabir J.S.M., Hajirah N.H., Alharbi N.S., Al-Malki A.L., Bailey C.D., Jansen R.K. Plastid genome sequences of legumes reveal parallel inversions and multiple losses of rps16 in papilionoids. J. Syst. Evol. 2015;53:458-468.

    Not in our library10.1111/jse.12179

  300. 300.

    Martínez-Romero E. Diversity of Rhizobium-Phaseolus vulgaris symbiosis: Overview and perspectives. Plant Soil. 2003;252:11-23.

    Not in our library10.1023/a:1024199013926

  301. 301.

    Oren A., Garrity G.M. List of new names and new combinations previously effectively, but not validly, published. Int. J. Syst. Evol. Microbiol. 2015;65:2017-2025.

    Not in our library10.1099/ijs.0.000317

  302. 302.

    Dobritsa A.P., Samadpour M. Transfer of eleven Burkholderia species to the genus Paraburkholderia and proposal of Caballeronia gen. nov., a new genus to accommodate twelve species of Burkholderia and Paraburkholderia. Int. J. Syst. Evol. Microbiol. 2016;66:2836-2846.

    Not in our library10.1099/ijsem.0.001065

  303. 303.

    Rogel M.A., Ormeño-Orrillo E., Martinez-Romero E. Symbiovars in rhizobia reflect bacterial adaptation to legumes. Syst. Appl. Microbiol. 2011;34:96-104.

    Not in our library10.1016/j.syapm.2010.11.015

  304. 304.

    Andrews M., Hodge S., Raven J.A. Positive plant microbial interactions. Ann. Appl. Biol. 2010;157:317-321.

    Not in our library10.1111/j.1744-7348.2010.00440.x

  305. 305.

    Fonseca M.B., Peix A., de Faria S.M., Mateos P.F., Rivera L.P., Simões-Araujo J.L., França M.G.C., dos Isaias R.M.S., Cruz C., Velázquez E., et al. Nodulation in Dimorphandra wilsonii Rizz. (Caesalpinioideae), a threatened species native to the Brazilian Cerrado. PLoS ONE. 2012;7:e49520.

    Not in our library10.1371/journal.pone.0049520

  306. 306.

    Yao Y., Wang R., Lu J.K., Sui X.H., Wang E.T., Chen W.X. Genetic diversity and evolution of Bradyrhizobium populations nodulating Erythrophleum fordii, an evergreen tree indigenous to the southern subtropical region of China. Appl. Environ. Microbiol. 2014;80:6184-6194.

    Not in our library10.1128/aem.01595-14

  307. 307.

    Parker M.A. Divergent Bradyrhizobium symbionts on Tachigali versicolor from Barro Colorado Island, Panama. Syst. Appl. Microbiol. 2000;23:585-590.

    Not in our library10.1016/s0723-2020(00)80034-x

  308. 308.

    Diabate M., Munive A., de Faria S.M., Ba A., Dreyfus B., Galiana A. Occurrence of nodulation in unexplored leguminous trees native to the West African tropical rainforest and inoculation response of native species useful in reforestation. New Phytol. 2005;166:231-239.

    Not in our library10.1111/j.1469-8137.2005.01318.x

  309. 309.
    Molecular diversity of legume root-nodule bacteria in Kakadu National Park, Northern Territory, Australia. · 2007
    Not checked
  310. 310.

    Michalk D.L., Zhi-Kai H. Grassland improvement in subtropical Guangdong province, China. 1. Evaluation of pasture legumes. Trop. Grassl. 1994;28:129-138.

    Not in our library

  311. 311.

    Keller K.R. Mutualistic rhizobia reduce plant diversity and alter community composition. Oecologia. 2014;176:1101-1109.

    Not in our library10.1007/s00442-014-3089-1

  312. 312.

    Australian Centre for International Agricultural Research. Forages fact sheet.

    Not in our library

  313. 313.
    Evolution of rhizobia by acquisition of a 500-kb symbiosis island that integrates into a phe-tRNA gene · 1998
    Not checked
  314. 314.

    Saidi S., Ramírez-Bahena M.H., Santillana N., Zúñiga D., Álvarez-Martínez E.R., Peix A., Mhamdi R., Velázquez E. Rhizobium laguerreae sp. nov. nodulates Vicia faba on several continents. Int. J. Syst. Evol. Microbiol. 2014;64:242-247.

    Not in our library10.1099/ijs.0.052191-0

  315. 315.

    Miller S.H., Elliot R.M., Sullivan J.T., Ronson C.W. Host-specific regulation of symbiotic nitrogen fixation in Rhizobium leguminosarum biovar trifolii. Microbiology. 2007;153:3184-3195.

    Not in our library10.1099/mic.0.2007/006924-0

  316. 316.

    De Meyer S.E., Tan H.W., Heenan P.B., Andrews M., Willems A. Mesorhizobium waimense sp. nov. isolated from Sophora longicarinata root nodules and Mesorhizobium cantuariense sp. nov. isolated from Sophora microphylla root nodules in New Zealand. Int. J. Syst. Evol. Microbiol. 2015;65:3419-3426.

    Not in our library10.1099/ijsem.0.000430

  317. 317.

    De Meyer S.E., Tan H.W., Andrews M., Heenan P.B., Willems A. Mesorhizobium calcicola sp. nov., Mesorhizobium waitakense sp. nov., Mesorhizobium sophorae sp. nov., Mesorhizobium newzealandense sp. nov. and Mesorhizobium kowhaii sp. nov. isolated from Sophora root nodules in New Zealand. Int. J. Syst. Evol. Microbiol. 2016;66:786-795.

    Not in our library10.1099/ijsem.0.000796

  318. 318.

    Perret X., Staehelin C., Broughton W.J. Molecular basis of symbiotic promiscuity. Microbiol. Mol. Bio. Rev. 2000;64:180-201.

    Not in our library10.1128/mmbr.64.1.180-201.2000

  319. 319.

    Davis E.O., Evans I.J., Johnston A.W. Identification of nodX, a gene that allows Rhizobium leguminosarum biovar viciae strain TOM to nodulate Afghanistan peas. Mol. Gen. Genet. 1988;212:531-535.

    Not in our library10.1007/bf00330860

  320. 320.

    Firmin J.L., Wilson K.E., Carlson R.W., Davies A.E., Downie J.A. Resistance to nodulation of cv. Afghanistan peas is overcome by nodX, which mediates an O-acetylation of the Rhizobium leguminosarum lipo-oligosaccharide nodulation factor. Mol. Microbiol. 1993;10:351-360.

    Not in our library10.1111/j.1365-2958.1993.tb01961.x

  321. 321.

    Geurts R., Heidstra R., Hadri A.E., Downie J.A., Franssen H., van Kammen A., Bisseling T. Sym2 of pea is involved in a nodulation factor-perception mechanism that controls the infection process in the epidermis. Plant Physiol. 1997;115:351-359.

    Not in our library10.1104/pp.115.2.351

  322. 322.

    Ehinger M., Mohr T.J., Starcevich J.B., Sachs J.L., Porter S.S., Simms E.L. Specialisation-generalisation trade off in a Bradyrhizobium symbiosis with wild legume hosts. BMC Ecol. 2014;14:8.

    Not in our library10.1186/1472-6785-14-8

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